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Why is polyploidy lethal for some organisms while for others is not?

Why is polyploidy lethal for some organisms while for others is not?


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Polyploidy is the multiplication of number of chromosomal sets from 2n to 3n (triploidy), 4n (tetraploidy) and so on. It is quite common in plants, for example many crops like wheat or Brassica forms. It seems to be rarer in animals but still it is present among some amphibian species like Xenopus.

As I know in mammals polyploidy is lethal (I don't mean tissue - limited polyploidy). I understand that triploidy is harmful due to stronger influence of maternal or paternal epigenetic traits that cause abnormal development of placenta, but why there is no tetraploid mammals?


Great question, and one about which there has historically been a lot of speculation, and there is currently a lot of misinformation. I will first address the two answers given by other users, which are both incorrect but have been historically suggested by scientists. Then I will try to explain the current understanding (which is not simple or complete). My answer is derived directly from the literature, and in particular from Mable (2004), which in turn is part of the 2004 special issue of the Biological Journal of the Linnean Society tackling the subject.

The 'sex' answer…

In 1925 HJ Muller addressed this question in a famous paper, "Why polyploidy is rarer in animals than in plants" (Muller, 1925). Muller briefly described the phenomenon that polyploidy was frequently observed in plants, but rarely in animals. The explanation, he said, was simple (and is approximate to that described in Matthew Piziak's answer):

animals usually have two sexes which are differentiated by means of a process involving the diploid mechanism of segregation and combination whereas plants-at least the higher plants-are usually hermaphroditic.

Muller then elaborated with three explanations of the mechanism:

  1. He assumed that triploidy was usually the intermediate step in chromosome duplication. This would cause problems, because if most animals' sex was determined by the ratios of chromosomes (as in Drosophila), triploidy would lead to sterility.
  2. In the rare cases when a tetraploid was accidentally created, it would have to breed with diploids, and this would result in a (presumably sterile) triploid.
  3. If, by chance, two tetraploids were to arise and mate, they would be at a disadvantage because, he said, they would be randomly allocated sex chromosomes and this would lead to a higher proportion of non-viable offspring, and thus the polyploid line would be outcompeted by the diploid.

Unfortunately, whilst the first two points are valid facts about polyploids, the third point is incorrect. A major flaw with Muller's explanation is that it only applies to animals with chromosomal ratio-based sex determination, which we have since discovered is actually relatively few animals. In 1925 there was comparatively little systematic study of life, so we really didn't know what proportion of plant or animal taxa showed polyploidy. Muller's answer doesn't explain why most animals, e.g. those with Y-dominant sex determination, exhibit relatively little polyploidy. Another line of evidence disproving Muller's answer is that, in fact, polyploidy is very common among dioecious plants (those with separate male and female plants; e.g. Westergaard, 1958), while Muller's theory predicts that prevalence in this group should be as low as in animals.

The 'complexity' answer…

Another answer with some historical clout is the one given by Daniel Standage in his answer, and has been given by various scientists over the years (e.g. Stebbins, 1950). This answer states that animals are more complex than plants, so complex that their molecular machinery is much more finely balanced and is disturbed by having multiple genome copies.

This answer has been soundly rejected (e.g. by Orr, 1990) on the basis of two key facts. Firstly, whilst polyploidy is unusual in animals, it does occur. Various animals with hermaphroditic or parthenogenetic modes of reproduction frequently show polyploidy. There are also examples of Mammalian polyploidy (e.g. Gallardo et al., 2004). In addition, polyploidy can be artificially induced in a wide range of animal species, with no deleterious effects (in fact it often causes something akin to hybrid vigour; Jackson, 1976).

It's also worth noting here that since the 1960s Susumo Ohno (e.g. Ohno et al. 1968; Ohno 1970; Ohno 1999) has been proposing that vertebrate evolution involved multiple whole-genome duplication events (in addition to smaller duplications). There is now significant evidence to support this idea, reviewed in Furlong & Holland (2004). If true, it further highlights that animals being more complex (itself a large, and in my view false, assumption) does not preclude polyploidy.

The modern synthesis…

And so to the present day. As reviewed in Mable (2004), it is now thought that:

  • Polyploidy is an important evolutionary mechanism which was and is probably responsible for a great deal of biological diversity.
  • Polyploidy arises easily in both animals and plants, but reproductive strategies might prevent it from propagating in certain circumstances, rather than any reduction in fitness resulting from the genome duplication.
  • Polyploidy may be more prevalent in animals than previously expected, and the imbalance in data arises from the fact that cytogenetics (i.e. chromosome counting) of large populations of wild specimens is a very common practise in botany, and very uncommon in zoology.

In addition, there are now several new suspected factors involved in ploidy which are currently being investigated:

  • Polyploidy is more common in species from high latitudes (temperate climates) and high altitudes (Soltis & Soltis, 1999). Polyploidy frequently occurs by the production of unreduced gametes (through meiotic non-disjunction), and it has been shown that unreduced gametes are produced with higher frequency in response to environmental fluctuations. This predicts that polyploidy should be more likely to occur in the first place in fluctuating environments (which are more common at higher latitudes and altitudes).
  • Triploid individuals, the most likely initial result of a genome duplication event, in animals and plants often die before reaching sexual maturity, or have low fertility. However, if triploid individuals do reproduce, there is a chance of even-ploid (fertile) individuals resulting. This probability is increased if the species produces large numbers of both male and female gametes, or has some mechanism of bypassing the triploid individual stage. This may largely explain why many species with 'alternative' sexual modes (apomictic, automictic, unisexual, or gynogenetic) show polyploidy, as they can keep replicating tetraploids, thus increasing the chance that eventually a sexual encounter with another tetraploid will create a new polyploid line. In this way, non-sexual species may be a crucial evolutionary intermediate in generating sexual polyploid species. Species with external fertilisation are more likely to establish polyploid lines - a greater proportion of gametes are involved in fertilisation events and therefore two tetraploid gametes are more likely to meet.
  • Finally, polyploidy is more likely to occur in species with assortative mixing. That is, when a tetraploid gamete is formed, if the genome duplication somehow affects the individual so as to make it more likely that it will be fertilised by another tetraploid, then it is more likely that a polyploid line will be established. Thus it may be partly down to evolutionary chance as to how easily a species' reproductive traits are affected. For example in plants, tetraploids often have larger flowers or other organs, and thus are preferentially attractive to pollinators. In frogs, genome duplication leads to changes in the vocal apparatus which can lead to immediate reproductive isolation of polyploids.

References

  • Furlong, R.F. & Holland, P.W.H. (2004) Polyploidy in vertebrate ancestry: Ohno and beyond. Biological Journal of the Linnean Society. 82 (4), 425-430.
  • Gallardo, M.H., Kausel, G., Jiménez, A., Bacquet, C., González, C., Figueroa, J., Köhler, N. & Ojeda, R. (2004) Whole-genome duplications in South American desert rodents (Octodontidae). Biological Journal of the Linnean Society. 82 (4), 443-451.
  • Jackson, R.C. (1976) Evolution and Systematic Significance of Polyploidy. Annual Review of Ecology and Systematics. 7209-234.
  • Mable, B.K. (2004) 'Why polyploidy is rarer in animals than in plants': myths and mechanisms. Biological Journal of the Linnean Society. 82 (4), 453-466.
  • Muller, H.J. (1925) Why Polyploidy is Rarer in Animals Than in Plants. The American Naturalist. 59 (663), 346-353.
  • Ohno, S. (1970) Evolution by gene duplication.
  • Ohno, S. (1999) Gene duplication and the uniqueness of vertebrate genomes circa 1970-1999. Seminars in Cell & Developmental Biology. 10 (5), 517-522.
  • Ohno, S., Wolf, U. & Atkin, N.B. (1968) EVOLUTION FROM FISH TO MAMMALS BY GENE DUPLICATION. Hereditas. 59 (1), 169-187.
  • Orr, H.A. (1990) 'Why Polyploidy is Rarer in Animals Than in Plants' Revisited. The American Naturalist. 136 (6), 759-770.
  • Soltis, D.E. & Soltis, P.S. (1999) Polyploidy: recurrent formation and genome evolution. Trends in Ecology & Evolution. 14 (9), 348-352.
  • Stebbins, C.L. (1950) Variation and evolution in plants. Westergaard, M. (1958) The Mechanism of Sex Determination in Dioecious Flowering Plants. In: Advances in Genetics. Academic Press. pp. 217-281.

(I'll come back and add links to the references later)


Plants have a simpler anatomical structure than mammals (is anatomical the right word, or would physiological be more appropriate?). Mammals on average don't have more genes than plants, so my understanding is that this additional complexity is the result of finer and more complex regulatory mechanisms.

When you remove or duplicate an individual gene in an organism, that organism must compensate somehow. The more complex the regulatory system, more likely that even small perturbations will cause severe defects or even lethality.

Extend this to the scale of a whole genome, and it shouldn't be surprising that polyploidy is lethal for a lot of organisms. It find it extremely fascinating that it's not lethal for some organisms, but it makes sense that organisms with simpler regulatory mechanisms would be more successful handling a genome duplication event through gene subfunctionalization, neofunctionalization, etc.


In animals, polyploidy is not tolerated and very few polyploid species are known to exist. Those that do exist are usually asexual, parthenogenetic, or hermaphroditic. Most of the problems resulting from polyploidy occur during synapsis of homologues during prophase I.

As plants do not have a chromosomal mechanism for sex determination, synapsis and subsequent disjunction is not as great a problem. In fact, most plants are monoecious.

These paragraphs are taken from these lecture notes from an Emporia State University genetics course.

Supporting information looks to be present in Why Polyploidy is Rarer in Animals Than in Plants (H. J. Muller, The American Naturalist, 1925), but I didn't get a chance to access the article.


My point in stating what is below is to emphasize even when polyploidy is present in closely related species there is a question of why an organism can survive one ploidy event but not another and why tolerance of polyploidy varies among similar organisms?

Several species of deciduous azaleas are tetraploid. Closely related diploid deciduous azaleas are more than happy to accept pollen and produce seedpods. We have attempted such crosses many times and they almost always success in terms of seedpod development.

Tetraploid deciduous azaleas on the other hand are very reluctant to accept pollen from diploid deciduous azaleas. We have attempted such crosses nearly 100 times without success.

However producing seedpods and producing viable seeds are of course different. Some crosses of diploid X tetraploid produce 1 or only a few viable seedlings (We have never gotten none to date.) while others produce viable seedlings measured in dozens while still others produce hundreds of viable seedlings. In some instances, the same diploid parent will produce many more viable seedlings from one tetraploid parent than from another.

To date all seedlings of diploid X tetraploid have measured as triploid using flow cytometry. Most seedlings appear to be sterile but some are fertile and occasionally some are very fertile to the point of setting open pollinated seed.

When these triploid seedling are successfully crossed with tetraploids, we get what appears based on flow cytometry to be triploids, aneuploids between triploid and tetraploid, tetraploids, and pentaploids. The few pentaploids old enough to flower appear to set seedpods when crossed with tetraploids.

In elepidote Rhododendron which has only diploid species, hybridizers over the last 150 years have had very limited success in producing polyploid elepidote Rhododendrons (less than 100 named hybrids) despite amazing success at creating and naming complex interspecies crosses (more than 20,000).

In other words, the pathway from diploid to polyploid can be a struggle for an organism even when polyploidy is present in closely related organisms.

Yet even the human lineage underwent polyploidy events. Humans were not simply created having 46 chromosomes. There is nothing to say that an organism or a set of organisms unable to tolerate almost all polyploid events are therefore unable to survive all polyploid events.

References

Rules of Engagement: Have Pollen-Will Travel by John Perkins · Sally Perkins in Azalean 2010

Ploidy level estimations in deciduous and elepidote hybrids of Rhododendron by José Cerca de Oliveira, Mariana Castro, Francisco J. do Nascimento, Sílvia Castro, John Perkins,Sally Perkins, João Loureiro in Jornadas Portuguesas de Genética, Coimbra, Portugal; 05/2011

Weighing in: Discovering the ploidy of hybrid elepidote rhododendrons by Sally Perkins, John Perkins, José Monteiro de Oliveira, Mariana Castro, Sílvia Castro, João Loureiro in Rhododendrons, Camellias and Magnolias, Royal Horticultural Society, Editors: Simon Maughan, pp.34-48 2012


Maurine Neiman

Why is sexual reproduction so common? Sexual females produce both sons and daughters, while asexual females make only daughters. Because only females produce offspring, this "cost of males" predicts that sex should be rare because asexual females will leave many more descendants than will sexual females. In reality, however, sex predominates. Despite years of study, why sex is so common remains unclear, and is considered one of the most important unanswered questions in evolutionary biology.

A clear understanding of the advantages of sex, which is distinguished from asexuality by the production of genetically variable offspring, is also of direct relevance to understanding the value of preserving genetic diversity within and among populations, species, and ecological communities. More broadly, our research program is relevant to scientists who use our snail study system as a model for ecotoxicology and host-parasite coevolution as well as those studying the causes and consequences of biological invasions. Our lab group is also very committed to mentoring and community engagement, and we are involved in a variety of such efforts, from regular collaborations with 10th grade Biology students at a local high school to the development and testing of a genomics module for a national high school computer science curriculum to our central role in organizing the annual Iowa City Darwin Day celebrations.

Research Projects.

Many research projects in our lab use Potamopyrgus antipodarum, a freshwater snail native to New Zealand. Natural lake populations of this snail vary in the frequency of obligately sexual and obligately asexual individuals, which sets the stage for investigation of why sex persists in some populations but not others. This species has been the focus of research into the maintenance of sex for nearly 20 years, and is now the best-characterized natural system available for studying why sexual reproduction is so common. While our research is based in evolution, we bring together ideas and tools from across biology to study sex in P. antipodarum. Several of the main research themes in our lab are outlined below.

Genetic and genomic consequences of asexuality.One set of projects revolves around testing the hypothesis that asexuality is rare at least in part because sex is required to prevent the accumulation of harmful mutations and facilitate the spread of beneficial mutations. We are using a variety of genetic and genomic approaches to address these questions in P. antipodarum. Related projects assess whether mutation accumulation in asexual P. antipodarum has detectable negative effects.

Potamopyrgus antipodarum genome project. We are leading an NSF-funded genome sequencing project for P. antipodarum, in collaboration with John Logsdon (U. Iowa) and Jeffrey Boore (UC-Berkeley). This project promises to provide unique and important new insights into how sexual reproduction and ploidy-level variation influence the evolution of genome composition and structure.

Disadvantages of polyploidy. Another major research focus in our lab is centered on the consequences of the higher ploidy of asexual vs. sexual snails. Like most sexual organisms, sexual P. antipodarum have two chromosome sets, while asexual P. antipodarum (like most asexuals) have at least three. Changes in ploidy level can dramatically affect key organismal traits such as cell size, body composition, and growth rate. We are currently addressing whether these possible consequences of polyploidy affect asexual P. antipodarum in a manner that could help compensate for the costs of sex and/or influence the distribution of ploidy level variation within and across natural populations.

Population dynamics of asexuals. We have also used laboratory experiments to demonstrate that asexual females have a negative impact on one another's reproduction. We are conducting research into snail behavior and population ecology to better understand why and how this happens, especially in light of the fact that P. antipodarum is invading freshwaters in Europe, Australia, and North America. Since the invasive populations are nearly all asexual, our research can provide new understanding of invasion dynamics as well as sex, and perhaps inspire ideas about how better to control the invading populations.


Contents

Types Edit

Polyploid types are labeled according to the number of chromosome sets in the nucleus. The letter x is used to represent the number of chromosomes in a single set:

  • haploid (one set 1x)
  • diploid (two sets 2x)
  • triploid (three sets 3x), for example sterile saffron crocus, or seedless watermelons, also common in the phylumTardigrada[5]
  • tetraploid (four sets 4x), for example Salmonidae fish, [6] the cotton Gossypium hirsutum[7]
  • pentaploid (five sets 5x), for example Kenai Birch (Betula papyrifera var. kenaica)
  • hexaploid (six sets 6x), for example wheat, kiwifruit[8]
  • heptaploid or septaploid (seven sets 7x)
  • octaploid or octoploid, (eight sets 8x), for example Acipenser (genus of sturgeon fish), dahlias
  • decaploid (ten sets 10x), for example certain strawberries
  • dodecaploid (twelve sets 12x), for example the plants Celosia argentea and Spartina anglica[9] or the amphibian Xenopus ruwenzoriensis.

Classification Edit

Autopolyploidy Edit

Autopolyploids are polyploids with multiple chromosome sets derived from a single taxon.

Two examples of natural autopolyploids are the piggyback plant, Tolmiea menzisii [10] and the white sturgeon, Acipenser transmontanum. [11] Most instances of autopolyploidy result from the fusion of unreduced (2n) gametes, which results in either triploid (n + 2n = 3n) or tetraploid (2n + 2n = 4n) offspring. [12] Triploid offspring are typically sterile (as in the phenomenon of 'triploid block'), but in some cases they may produce high proportions of unreduced gametes and thus aid the formation of tetraploids. This pathway to tetraploidy is referred to as the “triploid bridge”. [12] Triploids may also persist through asexual reproduction. In fact, stable autotriploidy in plants is often associated with apomictic mating systems. [13] In agricultural systems, autotriploidy can result in seedlessness, as in watermelons and bananas. [14] Triploidy is also utilized in salmon and trout farming to induce sterility. [15] [16]

Rarely, autopolyploids arise from spontaneous, somatic genome doubling, which has been observed in apple (Malus domesticus) bud sports. [17] This is also the most common pathway of artificially induced polyploidy, where methods such as protoplast fusion or treatment with colchicine, oryzalin or mitotic inhibitors are used to disrupt normal mitotic division, which results in the production of polyploid cells. This process can be useful in plant breeding, especially when attempting to introgress germplasm across ploidal levels. [18]

Autopolyploids possess at least three homologous chromosome sets, which can lead to high rates of multivalent pairing during meiosis (particularly in recently formed autopolyploids, also known as neopolyploids) and an associated decrease in fertility due to the production of aneuploid gametes. [19] Natural or artificial selection for fertility can quickly stabilize meiosis in autopolyploids by restoring bivalent pairing during meiosis, but the high degree of homology among duplicated chromosomes causes autopolyploids to display polysomic inheritance. [20] This trait is often used as a diagnostic criterion to distinguish autopolyploids from allopolyploids, which commonly display disomic inheritance after they progress past the neopolyploid stage. [21] While most polyploid species are unambiguously characterized as either autopolyploid or allopolyploid, these categories represent the ends of a spectrum of divergence between parental subgenomes. Polyploids that fall between these two extremes, which are often referred to as segmental allopolyploids, may display intermediate levels of polysomic inheritance that vary by locus. [22] [23]

About half of all polyploids are thought to be the result of autopolyploidy, [24] [25] although many factors make this proportion hard to estimate. [26]

Allopolyploidy Edit

Allopolyploids or amphipolyploids or heteropolyploids are polyploids with chromosomes derived from two or more diverged taxa.

As in autopolyploidy, this primarily occurs through the fusion of unreduced (2n) gametes, which can take place before or after hybridization. In the former case, unreduced gametes from each diploid taxa – or reduced gametes from two autotetraploid taxa – combine to form allopolyploid offspring. In the latter case, one or more diploid F1 hybrids produce unreduced gametes that fuse to form allopolyploid progeny. [27] Hybridization followed by genome duplication may be a more common path to allopolyploidy because F1 hybrids between taxa often have relatively high rates of unreduced gamete formation – divergence between the genomes of the two taxa result in abnormal pairing between homoeologous chromosomes or nondisjunction during meiosis. [27] In this case, allopolyploidy can actually restore normal, bivalent meiotic pairing by providing each homoeologous chromosome with its own homologue. If divergence between homoeologous chromosomes is even across the two subgenomes, this can theoretically result in rapid restoration of bivalent pairing and disomic inheritance following allopolyploidization. However multivalent pairing is common in many recently formed allopolyploids, so it is likely that the majority of meiotic stabilization occurs gradually through selection. [19] [21]

Because pairing between homoeologous chromosomes is rare in established allopolyploids, they may benefit from fixed heterozygosity of homoeologous alleles. [28] In certain cases, such heterozygosity can have beneficial heterotic effects, either in terms of fitness in natural contexts or desirable traits in agricultural contexts. This could partially explain the prevalence of allopolyploidy among crop species. Both bread wheat and Triticale are examples of an allopolyploids with six chromosome sets. Cotton, peanut, or quinoa are allotetraploids with multiple origins. In Brassicaceous crops, the Triangle of U describes the relationships between the three common diploid Brassicas (B. oleracea, B. rapa, and B. nigra) and three allotetraploids (B. napus, B. juncea, and B. carinata) derived from hybridization among the diploid species. A similar relationship exists between three diploid species of Tragopogon (T. dubius, T. pratensis, and T. porrifolius) and two allotetraploid species (T. mirus and T. miscellus). [29] Complex patterns of allopolyploid evolution have also been observed in animals, as in the frog genus Xenopus. [30]

Aneuploid Edit

Organisms in which a particular chromosome, or chromosome segment, is under- or over-represented are said to be aneuploid (from the Greek words meaning "not", "good", and "fold"). Aneuploidy refers to a numerical change in part of the chromosome set, whereas polyploidy refers to a numerical change in the whole set of chromosomes. [31]

Endopolyploidy Edit

Polyploidy occurs in some tissues of animals that are otherwise diploid, such as human muscle tissues. [32] This is known as endopolyploidy. Species whose cells do not have nuclei, that is, prokaryotes, may be polyploid, as seen in the large bacterium Epulopiscium fishelsoni. [33] Hence ploidy is defined with respect to a cell.

Monoploid Edit

A monoploid has only one set of chromosomes and the term is usually only applied to cells or organisms that are normally diploid. The more general term for such organisms is haploid.

Temporal terms Edit

Neopolyploidy Edit

A polyploid that is newly formed.

Mesopolyploidy Edit

That has become polyploid in more recent history it is not as new as a neopolyploid and not as old as a paleopolyploid. It is a middle aged polyploid. Often this refers to whole genome duplication followed by intermediate levels of diploidization.

Paleopolyploidy Edit

Ancient genome duplications probably occurred in the evolutionary history of all life. Duplication events that occurred long ago in the history of various evolutionary lineages can be difficult to detect because of subsequent diploidization (such that a polyploid starts to behave cytogenetically as a diploid over time) as mutations and gene translations gradually make one copy of each chromosome unlike the other copy. Over time, it is also common for duplicated copies of genes to accumulate mutations and become inactive pseudogenes. [34]

In many cases, these events can be inferred only through comparing sequenced genomes. Examples of unexpected but recently confirmed ancient genome duplications include baker's yeast (Saccharomyces cerevisiae), mustard weed/thale cress (Arabidopsis thaliana), rice (Oryza sativa), and an early evolutionary ancestor of the vertebrates (which includes the human lineage) and another near the origin of the teleost fishes. [35] Angiosperms (flowering plants) have paleopolyploidy in their ancestry. All eukaryotes probably have experienced a polyploidy event at some point in their evolutionary history.

Other similar terms Edit

Karyotype Edit

A karyotype is the characteristic chromosome complement of a eukaryote species. [36] [37] The preparation and study of karyotypes is part of cytology and, more specifically, cytogenetics.

Although the replication and transcription of DNA is highly standardized in eukaryotes, the same cannot be said for their karyotypes, which are highly variable between species in chromosome number and in detailed organization despite being constructed out of the same macromolecules. In some cases, there is even significant variation within species. This variation provides the basis for a range of studies in what might be called evolutionary cytology.

Homoeologous chromosomes Edit

Homoeologous chromosomes are those brought together following inter-species hybridization and allopolyploidization, and whose relationship was completely homologous in an ancestral species. For example, durum wheat is the result of the inter-species hybridization of two diploid grass species Triticum urartu and Aegilops speltoides. Both diploid ancestors had two sets of 7 chromosomes, which were similar in terms of size and genes contained on them. Durum wheat contains a hybrid genome with two sets of chromosomes derived from Triticum urartu and two sets of chromosomes derived from Aegilops speltoides. Each chromosome pair derived from the Triticum urartu parent is homoeologous to the opposite chromosome pair derived from the Aegilops speltoides parent, though each chromosome pair unto itself is homologous.

Animals Edit

Examples in animals are more common in non-vertebrates [38] such as flatworms, leeches, and brine shrimp. Within vertebrates, examples of stable polyploidy include the salmonids and many cyprinids (i.e. carp). [39] Some fish have as many as 400 chromosomes. [39] Polyploidy also occurs commonly in amphibians for example the biomedically-important genus Xenopus contains many different species with as many as 12 sets of chromosomes (dodecaploid). [40] Polyploid lizards are also quite common, but are sterile and must reproduce by parthenogenesis. [ citation needed ] Polyploid mole salamanders (mostly triploids) are all female and reproduce by kleptogenesis, [41] "stealing" spermatophores from diploid males of related species to trigger egg development but not incorporating the males' DNA into the offspring. While mammalian liver cells are polyploid, rare instances of polyploid mammals are known, but most often result in prenatal death.

An octodontid rodent of Argentina's harsh desert regions, known as the plains viscacha rat (Tympanoctomys barrerae) has been reported as an exception to this 'rule'. [42] However, careful analysis using chromosome paints shows that there are only two copies of each chromosome in T. barrerae, not the four expected if it were truly a tetraploid. [43] This rodent is not a rat, but kin to guinea pigs and chinchillas. Its "new" diploid (2n) number is 102 and so its cells are roughly twice normal size. Its closest living relation is Octomys mimax, the Andean Viscacha-Rat of the same family, whose 2n = 56. It was therefore surmised that an Octomys-like ancestor produced tetraploid (i.e., 2n = 4x = 112) offspring that were, by virtue of their doubled chromosomes, reproductively isolated from their parents.

Polyploidy was induced in fish by Har Swarup (1956) using a cold-shock treatment of the eggs close to the time of fertilization, which produced triploid embryos that successfully matured. [44] [45] Cold or heat shock has also been shown to result in unreduced amphibian gametes, though this occurs more commonly in eggs than in sperm. [46] John Gurdon (1958) transplanted intact nuclei from somatic cells to produce diploid eggs in the frog, Xenopus (an extension of the work of Briggs and King in 1952) that were able to develop to the tadpole stage. [47] The British scientist J. B. S. Haldane hailed the work for its potential medical applications and, in describing the results, became one of the first to use the word "clone" in reference to animals. Later work by Shinya Yamanaka showed how mature cells can be reprogrammed to become pluripotent, extending the possibilities to non-stem cells. Gurdon and Yamanaka were jointly awarded the Nobel Prize in 2012 for this work. [47]

Humans Edit

True polyploidy rarely occurs in humans, although polyploid cells occur in highly differentiated tissue, such as liver parenchyma, heart muscle, placenta and in bone marrow. [1] [48] Aneuploidy is more common.

Polyploidy occurs in humans in the form of triploidy, with 69 chromosomes (sometimes called 69, XXX), and tetraploidy with 92 chromosomes (sometimes called 92, XXXX). Triploidy, usually due to polyspermy, occurs in about 2–3% of all human pregnancies and

15% of miscarriages. [ citation needed ] The vast majority of triploid conceptions end as a miscarriage those that do survive to term typically die shortly after birth. In some cases, survival past birth may be extended if there is mixoploidy with both a diploid and a triploid cell population present. There has been one report of a child surviving to the age of seven months with complete triploidy syndrome. He failed to exhibit normal mental or physical neonatal development, and died from a Pneumocystis carinii infection, which indicates a weak immune system. [49]

Triploidy may be the result of either digyny (the extra haploid set is from the mother) or diandry (the extra haploid set is from the father). Diandry is mostly caused by reduplication of the paternal haploid set from a single sperm, but may also be the consequence of dispermic (two sperm) fertilization of the egg. [50] Digyny is most commonly caused by either failure of one meiotic division during oogenesis leading to a diploid oocyte or failure to extrude one polar body from the oocyte. Diandry appears to predominate among early miscarriages, while digyny predominates among triploid zygotes that survive into the fetal period. [51] However, among early miscarriages, digyny is also more common in those cases less than 8 + 1 ⁄ 2 weeks gestational age or those in which an embryo is present. There are also two distinct phenotypes in triploid placentas and fetuses that are dependent on the origin of the extra haploid set. In digyny, there is typically an asymmetric poorly grown fetus, with marked adrenal hypoplasia and a very small placenta. [ citation needed ] In diandry, a partial hydatidiform mole develops. [50] These parent-of-origin effects reflect the effects of genomic imprinting. [ citation needed ]

Complete tetraploidy is more rarely diagnosed than triploidy, but is observed in 1–2% of early miscarriages. However, some tetraploid cells are commonly found in chromosome analysis at prenatal diagnosis and these are generally considered 'harmless'. It is not clear whether these tetraploid cells simply tend to arise during in vitro cell culture or whether they are also present in placental cells in vivo. There are, at any rate, very few clinical reports of fetuses/infants diagnosed with tetraploidy mosaicism.

Mixoploidy is quite commonly observed in human preimplantation embryos and includes haploid/diploid as well as diploid/tetraploid mixed cell populations. It is unknown whether these embryos fail to implant and are therefore rarely detected in ongoing pregnancies or if there is simply a selective process favoring the diploid cells.

Fishes Edit

A polyploidy event occurred within the stem lineage of the teleost fishes. [35]

Plants Edit

Polyploidy is frequent in plants, some estimates suggesting that 30–80% of living plant species are polyploid, and many lineages show evidence of ancient polyploidy (paleopolyploidy) in their genomes. [52] [53] [54] [55] Huge explosions in angiosperm species diversity appear to have coincided with the timing of ancient genome duplications shared by many species. [56] It has been established that 15% of angiosperm and 31% of fern speciation events are accompanied by ploidy increase. [57]

Polyploid plants can arise spontaneously in nature by several mechanisms, including meiotic or mitotic failures, and fusion of unreduced (2n) gametes. [58] Both autopolyploids (e.g. potato [59] ) and allopolyploids (such as canola, wheat and cotton) can be found among both wild and domesticated plant species.

Most polyploids display novel variation or morphologies relative to their parental species, that may contribute to the processes of speciation and eco-niche exploitation. [53] [58] The mechanisms leading to novel variation in newly formed allopolyploids may include gene dosage effects (resulting from more numerous copies of genome content), the reunion of divergent gene regulatory hierarchies, chromosomal rearrangements, and epigenetic remodeling, all of which affect gene content and/or expression levels. [60] [61] [62] [63] Many of these rapid changes may contribute to reproductive isolation and speciation. However seed generated from interploidy crosses, such as between polyploids and their parent species, usually suffer from aberrant endosperm development which impairs their viability, [64] [65] thus contributing to polyploid speciation.

Some plants are triploid. As meiosis is disturbed, these plants are sterile, with all plants having the same genetic constitution: Among them, the exclusively vegetatively propagated saffron crocus (Crocus sativus). Also, the extremely rare Tasmanian shrub Lomatia tasmanica is a triploid sterile species.

There are few naturally occurring polyploid conifers. One example is the Coast Redwood Sequoia sempervirens, which is a hexaploid (6x) with 66 chromosomes (2n = 6x = 66), although the origin is unclear. [66]

Aquatic plants, especially the Monocotyledons, include a large number of polyploids. [67]

Crops Edit

The induction of polyploidy is a common technique to overcome the sterility of a hybrid species during plant breeding. For example, triticale is the hybrid of wheat (Triticum turgidum) and rye (Secale cereale). It combines sought-after characteristics of the parents, but the initial hybrids are sterile. After polyploidization, the hybrid becomes fertile and can thus be further propagated to become triticale.

In some situations, polyploid crops are preferred because they are sterile. For example, many seedless fruit varieties are seedless as a result of polyploidy. Such crops are propagated using asexual techniques, such as grafting.

Polyploidy in crop plants is most commonly induced by treating seeds with the chemical colchicine.

Examples Edit
  • Triploid crops: some apple varieties (such as Belle de Boskoop, Jonagold, Mutsu, Ribston Pippin), banana, citrus, ginger, watermelon, [68]saffron crocus, white pulp of coconut
  • Tetraploid crops: very few apple varieties, durum or macaroniwheat, cotton, potato, canola/rapeseed, leek, tobacco, peanut, kinnow, Pelargonium
  • Hexaploid crops: chrysanthemum, bread wheat, triticale, oat, kiwifruit[8]
  • Octaploid crops: strawberry, dahlia, pansies, sugar cane, oca (Oxalis tuberosa) [69]
  • Dodecaploid crops: some sugar cane hybrids [70]

Some crops are found in a variety of ploidies: tulips and lilies are commonly found as both diploid and triploid daylilies (Hemerocallis cultivars) are available as either diploid or tetraploid apples and kinnow mandarins can be diploid, triploid, or tetraploid.

Fungi Edit

Besides plants and animals, the evolutionary history of various fungal species is dotted by past and recent whole-genome duplication events (see Albertin and Marullo 2012 [71] for review). Several examples of polyploids are known:

  • autopolyploid: the aquatic fungi of genus Allomyces, [72] some Saccharomyces cerevisiae strains used in bakery, [73] etc.
  • allopolyploid: the widespread Cyathus stercoreus, [74] the allotetraploid lager yeast Saccharomyces pastorianus, [75] the allotriploid wine spoilage yeast Dekkera bruxellensis, [76] etc.
  • paleopolyploid: the human pathogen Rhizopus oryzae, [77] the genus Saccharomyces, [78] etc.

In addition, polyploidy is frequently associated with hybridization and reticulate evolution that appear to be highly prevalent in several fungal taxa. Indeed, homoploid speciation (hybrid speciation without a change in chromosome number) has been evidenced for some fungal species (such as the basidiomycota Microbotryum violaceum [79] ).

As for plants and animals, fungal hybrids and polyploids display structural and functional modifications compared to their progenitors and diploid counterparts. In particular, the structural and functional outcomes of polyploid Saccharomyces genomes strikingly reflect the evolutionary fate of plant polyploid ones. Large chromosomal rearrangements [80] leading to chimeric chromosomes [81] have been described, as well as more punctual genetic modifications such as gene loss. [82] The homoealleles of the allotetraploid yeast S. pastorianus show unequal contribution to the transcriptome. [83] Phenotypic diversification is also observed following polyploidization and/or hybridization in fungi, [84] producing the fuel for natural selection and subsequent adaptation and speciation.

Chromalveolata Edit

Other eukaryotic taxa have experienced one or more polyploidization events during their evolutionary history (see Albertin and Marullo, 2012 [71] for review). The oomycetes, which are non-true fungi members, contain several examples of paleopolyploid and polyploid species, such as within the genus Phytophthora. [85] Some species of brown algae (Fucales, Laminariales [86] and diatoms [87] ) contain apparent polyploid genomes. In the Alveolata group, the remarkable species Paramecium tetraurelia underwent three successive rounds of whole-genome duplication [88] and established itself as a major model for paleopolyploid studies.

Bacteria Edit

Each Deinococcus radiodurans bacterium contains 4-8 copies of its chromosome. [89] Exposure of D. radiodurans to X-ray irradiation or desiccation can shatter its genomes into hundred of short random fragments. Nevertheless, D. radiodurans is highly resistant to such exposures. The mechanism by which the genome is accurately restored involves RecA-mediated homologous recombination and a process referred to as extended synthesis-dependent strand annealing (SDSA). [90]

Azotobacter vinelandii can contain up to 80 chromosome copies per cell. [91] However this is only observed in fast growing cultures, whereas cultures grown in synthetic minimal media are not polyploid. [92]

Archaea Edit

The archaeon Halobacterium salinarium is polyploid [93] and, like Deinococcus radiodurans, is highly resistant to X-ray irradiation and desiccation, conditions that induce DNA double-strand breaks. [94] Although chromosomes are shattered into many fragments, complete chromosomes can be regenerated by making use of overlapping fragments. The mechanism employs single-stranded DNA binding protein and is likely homologous recombinational repair. [95]


Conclusions

Animal polyploidy seems significantly less well-documented and common than plant polyploidy however, its existence is not evidence for evolution. In fact, since polyploid speciation is nearly instantaneous by definition, polyploidy is actually more consistent with a Genesis account of post-flood speciation, though primarily in plants. Polyploidy would have created new species rapidly, even in the evolutionary paradigm. Though possibly providing more potential for variation within a kind, it does not provide novel specified genetic information. To use a book analogy, extra copies of old chapters (polyploidy) do not create new chapters (new specified genetic information). Regardless of whether it is ultimately classified as deleterious, neutral, beneficial, or all the above depending on the species, polyploid speciation is consistent with the creationist worldview.


For Plants, Polyploidy Is Not a Four-Letter Word

The sacred Asian water lotus, Nelumbo nucifera -- the pedestal of choice for a variety of Egyptian and Indian deities. It's easy to see why. Public Domain. Click image for link.

Creative Commons ehamburg. Click image for license and source.

For animals, inheriting more than the usual two copies of DNA is usually a very bad thing. It can happen when two sperm fertilize one egg, or when sexual cell division errs, leaving a sperm or an egg with double the approved payload. But for animal embryos, the result is usually the same: death.

This is particularly true in mammals and birds, where more than two copies -- a condition termed polyploidy -- produces something euphemistically termed "general developmental disruption". Practically speaking, this means system meltdown, and it happens very quickly. In humans, three or more whole genome copies occurs in about 5% of human miscarriages.

Only two cases of successful polyploidy are known among birds, and only one among mammals: the South American red viscacha rat (which is much cuter than it sounds). It has four copies of its genome, which makes it tetraploid.

Polyploidy is slightly more common among other animals. A few hundred cases of polyploidy are known in insects, reptiles, amphibians, crustaceans, fish, and other "lower" animals. Polyploidy can often be induced in these creatures something called "triploid trout" is making waves among anglers in the Pacific Northwest. The fish's three sets of chromosomes can't pair properly during sexual cell division, rendering them sterile but thereby enabling them to grow bigger than their diploid kin, since they don't waste energy on such frivolities as eggs, sperm, and hooking up. You know how fishermen feel about big fish, so "triploids" have already inspired the requisite epic fishing videos.

Though polyploidy is not common in animals, it is suspected that it might have played a role in the evolution, eons ago, of vertebrates, ray-finned fish, and the salmon family (of which trout are members). But on the whole, polyploidy is a dicey and often dangerous affair for animals.

Not so for plants, who seem to have a more laissez-faire attitude toward the whole business.

In my post earlier this week about a mutant diploid moss, I mentioned that it was capable of making functional eggs and sperm with two copies of the genome instead of the usual one. In other words, the offspring of this mutant would be tetraploid. The fact these plants seem to be capable of producing viable polyploid offspring suggests polyploidy can be an instrument of evolution in mosses, as it is for many other plants, suggested the authors of the paper that I wrote about.

For in plants, unlike animals, polyploidy is common, seemingly innocuous, and often acted upon by natural selection as an instrument of speciation. Perhaps plants tolerate genome duplication better than animals because they have inherently more flexible body plans than animals, and can more easily cope with any gross anatomical changes that might accompany it.

Whatever the reason, plant polyploidy is rampant. Scientists have estimated that half to two-thirds of flowering plants are polyploid, including more than 99% of ferns and 80% of the species in the grass family -- the source of rice, wheat, barley, oats, and corn. So are a huge proportion of our other crops, including sugarcane, potatoes, sweet potatoes, bananas, strawberries, and apples. We may well have artificially selected for this. In plants, genome duplication often seems to help make more stuff, which is good if you're looking to eat the stuff.

Though genome duplication can happen on its own in plants through the same mechanisms I mentioned above for animals, that is not the most common way. It more frequently follows accidental interbreeding of two closely related species. This usually produces sterile offspring, since the the mismatched chromosomes have nothing to pair with during sexual cell division. But if, by chance, this chimera duplicates its genome, fertility is restored by pairing the assorted lot. Simultaneously, a tetraploid organism and a new species have been created.

For example, two of the major varieties of wheat grown today are the result of sequential hybrid doubling and quadrupling of the genomes of its wild grass ancestors. The original ancestral species had 14 chromosomes. Today, farmers plant both tetraploid 28-chromosome durum wheat and hexaploid 42-chromosome bread wheat. Durum wheat makes more toothsome pasta, while the gluten-y hexaploid flour forms protein networks that stretch into loftier, lighter bread.

Two other polyploid plants made waves last week: the carnivorous bladderwort and the sacred lotus. The bladderwort's time in the spotlight was thanks to the discovery that it is nearly free of non-protein coding "junk" DNA, a material nearly every other complex organism is awash in, including you.

But the tiny, insect-eating plant has managed to achieve this parsimony in spite of three rounds of genome duplication. In theory, it's got eight copies of each gene, with respect to the two-copy ancestor of nearly all true or "eudicots", a massive group of flowering plants. That makes it octoploid. (It may be even ploidier than that when you take into account that the eudicots seem to have tripled their genomes shortly after evolving.) But in practice, and for reasons scientists don't entirely understand, the bladderwort has somehow deleted all but one copy of most of its duplicated genes, along with the vast majority of its non-protein coding DNA. Now *that's* efficiency.

The sacred lotus's full genetic sequence was published May 10. Lotus seems be the first plant to have split off from the rest of the eudicots, even prior to the early genome triplication I alluded to above. But it separately doubled its own genome sometime after. Suspiciously, the authors of the paper revealing its sequence report, the doubling seems to have taken place about 65 million years ago.

That is notable, of course, because it's right around the time our planet got the snot knocked out of it by the asteroid that bid sayonara to the dinosaurs -- but also to about 60% of plant species. During times of environmental stress, the authors note, plants that have duplicated their genomes seem to adapt and survive better. One might speculate that is thanks to the raw material that a second, superfluous set of genes provides natural selection for creating proteins with new functions.

Many other plant species seem to have doubled their genomes around the time of the K-T asteroid impact, the authors write, suggesting that whatever the conditions at the time were, polyploidy seems to have been a good survival strategy for plants. It was also an option far less available to animals, who, for this and probably many other reasons (they lack some plants' ability to make fortified resting structures and go dormant, for instance) suffered heavier losses. It's thought that perhaps 80% of Earth's animal species went extinct in the catastrophic aftermath of the impact.

Otto S. & Whitton J. (2000). Polyploid Incidence and Evolution, Annual Review of Genetics, 34 401-437. DOI: 10.1146/annurev.genet.34.1.401

Ming R., VanBuren R., Liu Y., Yang M., Han Y., Li L.T., Zhang Q., Kim M.J., Schatz M.C. & Campbell M. & (2013). Genome of the long-living sacred lotus (Nelumbo nucifera Gaertn.), Genome Biology, 14 (5) R41. DOI: 10.1186/gb-2013-14-5-r41

Ibarra-Laclette E., Lyons E., Hernández-Guzmán G., Pérez-Torres C.A., Carretero-Paulet L., Chang T.H., Lan T., Welch A.J., Juárez M.J.A. & Simpson J. & (2013). Architecture and evolution of a minute plant genome, Nature, DOI: 10.1038/nature12132

The views expressed are those of the author(s) and are not necessarily those of Scientific American.

ABOUT THE AUTHOR(S)

Jennifer Frazer, an AAAS Science Journalism Award–winning science writer, authored The Artful Amoeba blog for Scientific American. She has degrees in biology, plant pathology and science writing.


Speciation

The biological definition of species, which works for sexually reproducing organisms, is a group of actually or potentially interbreeding individuals. According to this definition, one species is distinguished from another by the possibility of matings between individuals from each species to produce fertile offspring. There are exceptions to this rule. Many species are similar enough that hybrid offspring are possible and may often occur in nature, but for the majority of species this rule generally holds. In fact, the presence of hybrids between similar species suggests that they may have descended from a single interbreeding species and that the speciation process may not yet be completed.

Given the extraordinary diversity of life on the planet there must be mechanisms for speciation: the formation of two species from one original species. Darwin envisioned this process as a branching event and diagrammed the process in the only illustration found in On the Origin of Species ([link]a). For speciation to occur, two new populations must be formed from one original population, and they must evolve in such a way that it becomes impossible for individuals from the two new populations to interbreed. Biologists have proposed mechanisms by which this could occur that fall into two broad categories. Allopatric speciation, meaning speciation in “other homelands,” involves a geographic separation of populations from a parent species and subsequent evolution. Sympatric speciation, meaning speciation in the “same homeland,” involves speciation occurring within a parent species while remaining in one location.

Biologists think of speciation events as the splitting of one ancestral species into two descendant species. There is no reason why there might not be more than two species formed at one time except that it is less likely and such multiple events can also be conceptualized as single splits occurring close in time.

Speciation through Geographic Separation

A geographically continuous population has a gene pool that is relatively homogeneous. Gene flow, the movement of alleles across the range of the species, is relatively free because individuals can move and then mate with individuals in their new location. Thus, the frequency of an allele at one end of a distribution will be similar to the frequency of the allele at the other end. When populations become geographically discontinuous that free-flow of alleles is prevented. When that separation lasts for a period of time, the two populations are able to evolve along different trajectories. Thus, their allele frequencies at numerous genetic loci gradually become more and more different as new alleles independently arise by mutation in each population. Typically, environmental conditions, such as climate, resources, predators, and competitors, for the two populations will differ causing natural selection to favor divergent adaptations in each group. Different histories of genetic drift, enhanced because the populations are smaller than the parent population, will also lead to divergence.

Given enough time, the genetic and phenotypic divergence between populations will likely affect characters that influence reproduction enough that were individuals of the two populations brought together, mating would be less likely, or if a mating occurred, offspring would be non-viable or infertile. Many types of diverging characters may affect the reproductive isolation (inability to interbreed) of the two populations. These mechanisms of reproductive isolation can be divided into prezygotic mechanisms (those that operate before fertilization) and postzygotic mechanisms (those that operate after fertilization). Prezygotic mechanisms include traits that allow the individuals to find each other, such as the timing of mating, sensitivity to pheromones, or choice of mating sites. If individuals are able to encounter each other, character divergence may prevent courtship rituals from leading to a mating either because female preferences have changed or male behaviors have changed. Physiological changes may interfere with successful fertilization if mating is able to occur. Postzygotic mechanisms include genetic incompatibilities that prevent proper development of the offspring, or if the offspring live, they may be unable to produce viable gametes themselves as in the example of the mule, the infertile offspring of a female horse and a male donkey.

If the two isolated populations are brought back together and the hybrid offspring that formed from matings between individuals of the two populations have lower survivorship or reduced fertility, then selection will favor individuals that are able to discriminate between potential mates of their own population and the other population. This selection will enhance the reproductive isolation.

Isolation of populations leading to allopatric speciation can occur in a variety of ways: from a river forming a new branch, erosion forming a new valley, or a group of organisms traveling to a new location without the ability to return, such as seeds floating over the ocean to an island. The nature of the geographic separation necessary to isolate populations depends entirely on the biology of the organism and its potential for dispersal. If two flying insect populations took up residence in separate nearby valleys, chances are that individuals from each population would fly back and forth, continuing gene flow. However, if two rodent populations became divided by the formation of a new lake, continued gene flow would be unlikely therefore, speciation would be more likely.

Biologists group allopatric processes into two categories. If a few members of a species move to a new geographical area, this is called dispersal. If a natural situation arises to physically divide organisms, this is called vicariance.

Scientists have documented numerous cases of allopatric speciation taking place. For example, along the west coast of the United States, two separate subspecies of spotted owls exist. The northern spotted owl has genetic and phenotypic differences from its close relative, the Mexican spotted owl, which lives in the south ([link]). The cause of their initial separation is not clear, but it may have been caused by the glaciers of the ice age dividing an initial population into two. 1

Additionally, scientists have found that the further the distance between two groups that once were the same species, the more likely for speciation to take place. This seems logical because as the distance increases, the various environmental factors would likely have less in common than locations in close proximity. Consider the two owls in the north, the climate is cooler than in the south the other types of organisms in each ecosystem differ, as do their behaviors and habits also, the hunting habits and prey choices of the owls in the south vary from the northern ones. These variances can lead to evolved differences in the owls, and over time speciation will likely occur unless gene flow between the populations is restored.

In some cases, a population of one species disperses throughout an area, and each finds a distinct niche or isolated habitat. Over time, the varied demands of their new lifestyles lead to multiple speciation events originating from a single species, which is called adaptive radiation. From one point of origin, many adaptations evolve causing the species to radiate into several new ones. Island archipelagos like the Hawaiian Islands provide an ideal context for adaptive radiation events because water surrounds each island, which leads to geographical isolation for many organisms ([link]). The Hawaiian honeycreeper illustrates one example of adaptive radiation. From a single species, called the founder species, numerous species have evolved, including the eight shown in [link].

Notice the differences in the species’ beaks in [link]. Change in the genetic variation for beaks in response to natural selection based on specific food sources in each new habitat led to evolution of a different beak suited to the specific food source. The fruit and seed-eating birds have thicker, stronger beaks which are suited to break hard nuts. The nectar-eating birds have long beaks to dip into flowers to reach their nectar. The insect-eating birds have beaks like swords, appropriate for stabbing and impaling insects. Darwin’s finches are another well-studied example of adaptive radiation in an archipelago.

Click through this interactive site to see how island birds evolved click to see images of each species in evolutionary increments from five million years ago to today.

Speciation without Geographic Separation

Can divergence occur if no physical barriers are in place to separate individuals who continue to live and reproduce in the same habitat? A number of mechanisms for sympatric speciation have been proposed and studied.

One form of sympatric speciation can begin with a chromosomal error during meiosis or the formation of a hybrid individual with too many chromosomes. Polyploidy is a condition in which a cell, or organism, has an extra set, or sets, of chromosomes. Scientists have identified two main types of polyploidy that can lead to reproductive isolation of an individual in the polyploid state. In some cases a polyploid individual will have two or more complete sets of chromosomes from its own species in a condition called autopolyploidy ([link]). The prefix “auto” means self, so the term means multiple chromosomes from one’s own species. Polyploidy results from an error in meiosis in which all of the chromosomes move into one cell instead of separating.

For example, if a plant species with 2n = 6 produces autopolyploid gametes that are also diploid (2n = 6, when they should be n = 3), the gametes now have twice as many chromosomes as they should have. These new gametes will be incompatible with the normal gametes produced by this plant species. But they could either self-pollinate or reproduce with other autopolyploid plants with gametes having the same diploid number. In this way, sympatric speciation can occur quickly by forming offspring with 4n called a tetraploid. These individuals would immediately be able to reproduce only with those of this new kind and not those of the ancestral species. The other form of polyploidy occurs when individuals of two different species reproduce to form a viable offspring called an allopolyploid. The prefix “allo” means “other” (recall from allopatric) therefore, an allopolyploid occurs when gametes from two different species combine. [link] illustrates one possible way an allopolyploidy can form. Notice how it takes two generations, or two reproductive acts, before the viable fertile hybrid results.

The cultivated forms of wheat, cotton, and tobacco plants are all allopolyploids. Although polyploidy occurs occasionally in animals, most chromosomal abnormalities in animals are lethal it takes place most commonly in plants. Scientists have discovered more than 1/2 of all plant species studied relate back to a species evolved through polyploidy.

Sympatric speciation may also take place in ways other than polyploidy. For example, imagine a species of fish that lived in a lake. As the population grew, competition for food also grew. Under pressure to find food, suppose that a group of these fish had the genetic flexibility to discover and feed off another resource that was unused by the other fish. What if this new food source was found at a different depth of the lake? Over time, those feeding on the second food source would interact more with each other than the other fish therefore they would breed together as well. Offspring of these fish would likely behave as their parents and feed and live in the same area, keeping them separate from the original population. If this group of fish continued to remain separate from the first population, eventually sympatric speciation might occur as more genetic differences accumulated between them.

This scenario does play out in nature, as do others that lead to reproductive isolation. One such place is Lake Victoria in Africa, famous for its sympatric speciation of cichlid fish. Researchers have found hundreds of sympatric speciation events in these fish, which have not only happened in great number, but also over a short period of time. [link] shows this type of speciation among a cichlid fish population in Nicaragua. In this locale, two types of cichlids live in the same geographic location however, they have come to have different morphologies that allow them to eat various food sources.

Finally, a well-documented example of ongoing sympatric speciation occurred in the apple maggot fly, Rhagoletis pomonella, which arose as an isolated population sometime after the introduction of the apple into North America. The native population of flies fed on hawthorn species and is host-specific: it only infests hawthorn trees. Importantly, it also uses the trees as a location to meet for mating. It is hypothesized that either through mutation or a behavioral mistake, flies jumped hosts and met and mated in apple trees, subsequently laying their eggs in apple fruit. The offspring matured and kept their preference for the apple trees effectively dividing the original population into two new populations separated by host species, not by geography. The host jump took place in the nineteenth century, but there are now measureable differences between the two populations of fly. It seems likely that host specificity of parasites in general is a common cause of sympatric speciation.

Section Summary

Speciation occurs along two main pathways: geographic separation (allopatric speciation) and through mechanisms that occur within a shared habitat (sympatric speciation). Both pathways force reproductive isolation between populations. Sympatric speciation can occur through errors in meiosis that form gametes with extra chromosomes, called polyploidy. Autopolyploidy occurs within a single species, whereas allopolyploidy occurs because of a mating between closely related species. Once the populations are isolated, evolutionary divergence can take place leading to the evolution of reproductive isolating traits that prevent interbreeding should the two populations come together again. The reduced viability of hybrid offspring after a period of isolation is expected to select for stronger inherent isolating mechanisms.


Discussion

With the purpose of investigating whether WGDs may confer an adaptive advantage in the face of drastic environmental changes or extinction events, such as abrupt reductions in available food resources, we have implemented here an improved version of our previously designed bio-inspired and agent-based computational framework for simulating biological evolution [24, 25]. Two different environmental scenarios of food reduction were set: either food was removed dynamically every time the total population reached 1000 individuals, or at a fixed time step during the simulation. From our simulations, we learned that under stable environments, non-polyploids in general do better than polyploids, as reflected by the low or null fraction of polyploids surviving at the end of the different experiments performed under low or null food reduction. Under both scenarios, the relative fraction of polyploid DOs surviving at the end of the experiment increased with increasing levels of food reduction, overcoming the population of non-polyploid DOs when the environmental challenge introduced was strong enough. Taken as whole, these results suggest that WGDs are usually maladaptive under stable environments, but may actually confer an adaptive advantage under certain environmental constraints, which seems in agreement with recent ‘real-life’ observations [6, 31–33].

Although the substitution rate was the same for all genomes and is not supposed to change after WGD, contrary to our initial expectations, we observed lower STGD among polyploid DOs, suggesting that duplicated genomes are under stronger purifying selection, at least on the short-term. Once fixed and inherited though, mutations might have more chance to be retained for longer times in duplicated genomes, as suggested by the higher LTGD values for polyploids, possibly because of redundancy in the genome, although this needs to be confirmed and further investigated.

We have also shown that DOs with non-duplicated genomes need to accumulate many more mutations than polyploid genomes to reach adaptation (using homeostasis as measured by ED and the energy level as proxies). We interpret this as follows: under stable environments, and in ‘well-adapted’ organisms with (relatively) stable GRNs, there is always a certain chance that a random mutation renders the GRN (and consequently, its host) less well adapted to that environment. This phenomenon is exacerbated in more complex GRNs. With an increasing number of edges and connections in the network, the probability increases that a random mutation in a regulator affects a larger number of genes, in turn increasing the chance of causing major disturbances to the underlying GRN [34–37]. In this respect, WGDs increase the number of edges in the network exponentially (Fig 7). For instance, in our simulations, while the average GRN for the total population consisted of 272 instances or agents at the start, this increased to about 1,700 for DOs with a duplicated genome at the end of the simulations.

Simple network motif (feed forward loop) before (A) and after (B) genome wide duplication. After duplication, network complexity has increased and random mutations may affect (many) more genes, in turn increasing the chance of causing major disturbances to the GRN and underlying phenotype.

From previous theoretical and experimental work, it has been shown that gene duplication and divergence may be at the origin of specific properties of biological networks such as GRNs, including increased complexity and, also, modularity, i.e. the occurrence of multiple functional subnetworks or modules formed by highly connected genes that are co-expressed and/or co-regulated by the same set of key regulators, while establishing sparser connections with nodes from different modules [1, 38–46]. As a consequence, single substitutions in duplicated genomes have the potential to affect many more key regulators, in turn having a greater impact on the underlying GRN and the resulting phenotypes. Again, whereas this may be disadvantageous in stable environments, under drastic environmental changes, DOs with duplicated genomes may actually have a better chance to acquire the drastic genomic–and consequently phenotypic—changes necessary to survive major changes in the fitness landscape (Fig 8). In addition, the duplication of genomes and their encoded GRNs may result in redundancy, contributing to the genetic or mutational robustness at the GRN level. This facilitates the rewiring of novel functional modules while maintaining the ancestral one, a feature that is expected to be especially advantageous under unstable, recurring, and/or challenging environments [23, 41]. In this respect, our observations are compatible with previous claims that increased complexity and modularity results in increased evolvability [36, 47–52]. For a population that is already well adapted to a certain environment, the increased complexity and modularity of the duplicated GRNs could be maladaptive or detrimental because the GRNs are more vulnerable to random mutations and the potential for increased evolvability may have little value or direct benefits. On the other hand, the complex and modular structure of duplicated GRNs might allow polyploids to explore a wider evolutionary landscape (Fig 8), providing short-term increased opportunity to adapt to novel, different, or rapidly changing environments, while redundancy facilitates the gradual evolution of duplicated networks for adapting in the longer term. In partial summary, increased complexity, modularity and functional redundancy following WGD would help to explain the different behavior of polyploids and non-polyploids under stable or challenging environments [6].

Top panels, 3D surface representation of the phenotype space accessible for every combination of two hypothetical phenotypic traits, which ultimately correspond to an organism’s specific genotypic configuration. Each coordinate in the XY plane conformed by phenotype 1 and phenotype 2 has a relative fitness value associated on the Z axis. The resulting fitness landscape is formed by a range of hills, each corresponding to the total phenotype space accessible to a specific organism or group of organisms, i.e, their ecological niche, with a local maximum or adaptive peak located at the top. Hills are surrounded by valleys or depressions, colored in dark blue, corresponding to regions of the phenotype space inaccessible to any organism. Bottom panels show the 2D colored image plots corresponding to the fitness landscapes above. Black dots, white dots and red crosses represent organisms occupying the fitness landscape. Concentric circles around organisms represent the areas of the phenotype space accessible by non-polyploid organisms (inner circle) or their polyploid relatives (outer circle). Arrows indicate the trajectories followed by every organism to reach their adaptive peak. Black dots represent organisms that have reached their local maxima and are thus located at their adaptive peaks white dots represent organisms that survived after a change in the environmental conditions and subsequent shifts of their adaptive peaks red crosses represent organisms that perish because of big shifts or extinction of their niches. From left to right, three different environmental scenarios are shown. In the left two panels, organisms evolving under a stable environment for a certain time are expected to have reached their local adaptive peaks. In the middle two panels, a small change in environmental conditions (e.g., a small drop in the total food available) may result in small shifts of the peaks or their relative fitness contribution, or eventually in the extinction or emergence of specific ecological niches. In most cases, the new location of the peaks fall within the phenotype area (still) accessible to non-polyploid organisms (inner circles). Under this scenario, non-polyploid organisms are expected to quickly reach the new peaks, rapidly outcompeting their polyploid relatives, which are more likely to fall farther away (outer circles) and have well-known detrimental effects. Finally, in the right panels, a cataclysmic or extinction event (e.g., a big drop in the total food available) is represented, resulting in a reduction in the number of available ecological niches, and big shifts in their relative locations. Under these conditions, although most organisms are expected to perish, polyploids organisms, featured by wider accessible phenotype space (as a result of the potential higher impact of mutations in more complex genomes, see text for details), have better chances to fall near the peak of a newly formed adaptive hill and to develop the necessary evolutionary innovations to colonize empty niches.

Although many other factors may be at play as well, which, for simplicity, are not considered here (but will be addressed elsewhere), the effect of WGD on network complexity and redundancy could be part of the explanation why also in natural environments, floras in stable environments might have lower proportions of polyploids than highly, recently disturbed floras. In a recent study, Oberlander et al. [53] suggested that the hyper diverse South African Cape flora, which has anomalously low proportions of polyploids compared to global levels, might be due to long-term climatic and geological stability, supporting the hypothesis that WGD may be rare in stable environments. On the contrary, there is considerable evidence that polyploidy is much more common in disturbed habitats, or habitats that (have) show(n) environmental turmoil [6, 31, 54]. Previously, we have also wondered about the discrepancy between the existence of many polyploids of fairly recent origin and the scant evidence of ancient polyploidy events, certainly within the same evolutionary lineage [6]. The paucity of polyploidy events that ‘survive’ and are established in the long term would suggest that polyploidy is usually an evolutionary dead end. Again, this fits with our observation that the increased complexity and modularity of the underlying networks may be detrimental (or at least sub-optimal) for species that are well-adapted to their environment, when accumulating (too) many changes (Fig 8). In this respect, it is also noteworthy to mention that during our simulations, rarely two or three WGDs were observed, and never more. Also in real-life organisms, very few examples are known of consecutively established WGDs that have occurred in a short period of time. Some of these presumed exceptions are Musa acuminata, Spirodela polyrhiza, and Arabidopsis thaliana [6]. However, at least for Arabidopsis [55] and Spirodela [56], the number of genes is low compared to what would be expected following several rounds of WGD, suggesting huge gene loss and fractionation following WGD. In line with our observations made in the current study, quickly losing a large amount of the extra genetic material created through a WGD, thereby potentially reducing the complexity of the active GRNs, might have facilitated surviving these major events.

Finally, our observations might also have some broader implications and might help to understand the origin of complex phenotypes and discontinuities in biological evolution. Traditionally, evolution is regarded as progressing at a more or less constant rate, which is linked to the gradual accumulation of small genetic changes over time. This model successfully explains, for instance, the variation between (closely) related species but often fails to explain bigger ‘leaps’ in evolution. However, there is ample recording of ‘novel’ or highly divergent species that seem to have emerged in a relatively short evolutionary time frame and sometimes even representing important evolutionary transitions. Such observations often seem difficult to reconcile with an evolutionary model that is based on the gradual accumulation of small changes, and a huge body of literature has been devoted to this seemingly contradictory phenomenon [57, 58].

As supported by our simulations, and in previous research [24, 25], in a stable environment, gradual evolution can successfully explain the divergence and optimization of evolutionary processes. In contrast, when the environment drastically changes, in a short geological time frame, gradual evolution has difficulty to keep up, while new species or life forms, if different enough from the original ones, can successfully occupy the ‘new’ niches that have become available. When the environment is rapidly changing, existing species may not have enough time to adapt and will disappear. WGD might provide a way out and might be one way reconciling a model of gradual evolution with adaptation to a rapidly changing environment [3]. Gene and genome duplication has been suggested before as a way to explain ‘saltational’ jumps in evolution [59–61]. Indeed, the duplication of genes and particularly the duplication of entire genomes immediately creates redundant informational ‘entities’ or ‘modules’ in the genome, offering possibilities for a more drastic change and a wider exploration of genotypic and phenotypic space (Fig 8). While in a constant environment, in which organisms are already fairly well-adapted, we only could observe the further slow optimization of biological systems, a WGD creates more drastic changes in certain individual species. These individuals often remain hidden in the population–and usually have a hard time competing with their non-polyploid progenitors, for reasons explained higher and elsewhere [6, 7, 31], but could ‘grab their chance’ upon different conditions or under different contexts. Increased gene pleiotropy evoked by WGD thus forms a fertile substrate allowing evolution to explore more diverse options possibly explaining those bigger jumps in evolution observed. Again, such evolvability might only be successful when the existing environmental conditions have been (seriously) disrupted (Fig 8). When a new environmental ‘equilibrium’ has been reached and the new environmental conditions have stabilized again, the increased evolvability through WGD will become less important in further optimizing the system and on the contrary selection on a more complex system (due to WGD, see higher) might be constrained again. Considering polyploidy in the evolutionary history of organisms might thus indeed be one additional way of possibly explaining bigger leaps or major transitions in evolution, as already suggested by Susumu Ohno in 1970 [62], but certainly needs further investigation.


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2.8: Gene Balance

  • Contributed by Todd Nickle and Isabelle Barrette-Ng
  • Professors (Biology) at Mount Royal University & University of Calgary

Why do trisomies, duplications, and other chromosomal abnormalities that alter gene copy number often have a negative effect on the normal development or physiology of an organism? This is particularly intriguing because in many species, aneuploidy is detrimental or lethal, while polyploidy is tolerated or even beneficial. The answer probably differs in each case, but is probably related to the concept of gene balance, which can be summarized as follows: genes, and the proteins they produce, have evolved to function in complex metabolic and regulatory networks. Some of these networks function best when certain enzymes and regulators are present in specific ratios to each other. Increasing or decreasing the gene copy number for just one part of the network may throw the whole network out of balance, leading to increases or decreases of certain metabolites, which may be toxic in high concentrations or which may be limiting in other important processes in the cell. The activity of genes and metabolic networks is regulated in many different ways besides changes in gene copy number, so duplication of just a few genes will usually not be harmful. However, trisomy and large segmental duplications of chromosomes affect the dosage of so many genes that cellular networks are unable to compensate for the changes and an abnormal or lethal phenotype results.