Despite the importance of polyploidy and the increasing availability of new genomic data, there remain important gaps in our knowledge of polyploid population genetics. These gaps arise from the complex nature of polyploid data (e.g. multiple alleles and loci, mixed inheritance patterns, association between ploidy and mating system variation). Furthermore, many of the standard tools for population genetics that have been developed for diploids are often not feasible for polyploids. This review aims to provide an overview of the state-of-the-art in polyploid population genetics and to identify the main areas where further development of molecular techniques and statistical theory is required. We review commonly used molecular tools (amplified fragment length polymorphism, microsatellites, Sanger sequencing, next-generation sequencing and derived technologies) and their challenges associated with their use in polyploid populations: that is, allele dosage determination, null alleles, difficulty of distinguishing orthologues from paralogues and copy number variation. In addition, we review the approaches that have been used for population genetic analysis in polyploids and their specific problems. These problems are in most cases directly associated with dosage uncertainty and the problem of inferring allele frequencies and assumptions regarding inheritance. This leads us to conclude that for advancing the field of polyploid population genetics, most priority should be given to development of new molecular approaches that allow efficient dosage determination, and to further development of analytical approaches to circumvent dosage uncertainty and to accommodate 'flexible' modes of inheritance. In addition, there is a need for more simulation-based studies that test what kinds of biases could result from both existing and novel approaches.
Whole genome duplication (leading to polyploidy) is widely accepted as an important evolutionary force in plants, but it is less recognized as a driver of animal diversification. Nevertheless, it occurs across a wide range of animals; this review investigates why it is particularly common in fish and amphibians, while rare among other vertebrates. We review the current geographic, ecological and phylogenetic distributions of sexually reproducing polyploid taxa before focusing more specifically on what factors drive polyploid formation and establishment. In summary, (1) polyploidy is phylogenetically restricted in both amphibians and fishes, although entire fish, but not amphibian, lineages are derived from polyploid ancestors. (2) Although mechanisms such as polyspermy are feasible, polyploid formation appears to occur principally through unreduced gamete formation, which can be experimentally induced by temperature or pressure shock in both groups. (3) External reproduction and fertilization in primarily temperate freshwater environments potentially exposes zygotes to temperature stress, which can promote increased production of unreduced gametes. (4) Large numbers of gametes and group breeding in relatively confined areas could increase the probability of compatible gamete combinations in both groups. (5) Both fish and amphibians have a propensity to form reproductively successful hybrids; although the relative frequency of autopolyploidy versus allopolyploidy is difficult to ascertain, multiple origins involving hybridization have been confirmed for a number of species in both groups. (6) Problems with establishment of polyploid lineages associated with minority cytotype exclusion could be overcome in amphibians via assortative mating by acoustic recognition of the same ploidy level, but less attention has been given to chemical or acoustic mechanisms that might operate in fish. (7) There is no strong evidence that polyploid fish or amphibians currently exist in more extreme environments than their diploid progenitors or have broader ecological ranges. (8) Although pathogens could play a role in the relative fitness of polyploid species, particularly given duplication of genes involved in immunity, this remains an understudied field in both fish and amphibians. (9) As in plants, many duplicate copies of genes are retained for long periods of time, indicative of selective maintenance of the duplicate copies, but we find no physiological or other reasons that could explain an advantage for allelic or genetic complexity. (10) Extant polyploid species do not appear to be more or less prone to extinction than related diploids in either group. We conclude that, while polyploid fish and amphibians share a number of attributes facilitating polyploidy, clear drivers of genome duplication do not emerge from the comparison. The lack of a clear association of sexually reproducing polyploids with range expansion, harsh environments, or risk of extinction could suggest that stronger correlations in plants may be driven by s...
Although polyploidy has been involved in speciation in both animals and plants, the general perception is often that it is too rare to have been a significant factor in animal evolution and its role in plant diversification has been questioned. These views have resulted in a bias towards explanations for what deters polyploidy, rather than the somewhat more interesting question of the mechanisms by which polyploidy arises and becomes established in both plants and animals. The evidence for and against some of the traditional views on polyploidy is reviewed, with an attempt to synthesize factors promoting evolution through genome duplication in both groups. It is predicted that polyploidy should be more common in temperate than in tropical breeders because environmental fluctuations may promote unreduced gamete formation, it should be most common in organisms with sufficient numbers of gametes that random meiotic problems can be overcome, and it should be more frequent when mechanisms to promote assortative mating are a direct byproduct of genome duplication.
Theoretical and empirical comparisons of molecular diversity in selfing and outcrossing plants have primarily focused on long-term consequences of differences in mating system (between species). However, improving our understanding of the causes of mating system evolution requires ecological and genetic studies of the early stages of mating system transition. Here, we examine nuclear and chloroplast DNA sequences and microsatellite variation in a large sample of populations of Arabidopsis lyrata from the Great Lakes region of Eastern North American that show intra-and interpopulation variation in the degree of self-incompatibility and realized outcrossing rates. Populations show strong geographic clustering irrespective of mating system, suggesting that selfing either evolved multiple times or has spread to multiple genetic backgrounds. Diversity is reduced in selfing populations, but not to the extent of the severe loss of variation expected if selfing evolved due to selection for reproductive assurance in connection with strong founder events. The spread of self-compatibility in this region may have been favored as colonization bottlenecks following glaciation or migration from Europe reduced standing levels of inbreeding depression. However, our results do not suggest a single transition to selfing in this system, as has been suggested for some other species in the Brassicaceae.Arabidopsis, bottlenecks, breakdown of self-incompatibility, demography, effective population size, inbreeding depression, mating system evolution, population genetics.
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Sexual eukaryotic organisms are characterized by an alternation between haploid and diploid phases. In vascular plants and animals, somatic growth and development occur primarily in the diploid phase, with the haploid phase reduced to the gametic cells. In many other eukaryotes, however, growth and development occur in both phases, with substantial variability among organisms in the length of each phase of the life cycle. A number of theoretical models and experimental studies have shed light on factors that may influence life cycle evolution, yet we remain far from a complete understanding of the diversity of life cycles observed in nature. In this paper we review the current state of knowledge in this field, and touch upon the many questions that remain unanswered.
Abstract. Mating systems in plants are known to be highly labile traits, with frequent transitions from outcrossing to selfing. The genetic basis for breakdown in self-incompatibility (SI) systems has been studied, but data on variation in selfing rates in species for which the molecular basis of SI is known are rare. This study surveyed such variation in Arabidopsis lyrata (Brassicaceae), which is often considered an obligately outcrossing species, to examine the causes and genetic consequences of changes in its breeding system. Based on controlled self-pollinations in the greenhouse, three populations from the Great Lakes region of North America included a minority of self-compatible (SC) individuals, while two showed larger proportions of SC individuals and all populations contained some individuals capable of setting selfed seeds. Loss of SI was not associated with particular haplotypes at the S-locus (as estimated by alleles amplified at the SRK locus, the gene controlling female specificity) and all populations contained similar numbers of SRK alleles, suggesting that some other genetic factor is responsible for modifying the SI reaction. The loss of SI has resulted in an effective shift in the mating system, as the two populations with a high frequency of SC individuals showed significantly lower microsatellite-based multilocus outcrossing rates and higher inbreeding coefficients than the other populations. Based on microsatellites, observed heterozygosities and genetic diversity were also significantly depressed in these populations. These findings provide the unique opportunity to examine in detail the consequences of mating system changes within a species with a well-characterized SI system. Key words. Arabidopsis lyrata, genetic diversity, heterozygosity, mating system variation, microsatellites, self-incompatibility breakdown, SRK. The evolutionary dynamics of flowering plant mating systems has been the subject of much interest for many years, but numerous questions remain about the forces that influence changes in levels of inbreeding and the consequences of such changes. Loss of self-incompatibility (SI) is a frequent evolutionary transition at the level of species (Weller and Sakai 1999) but intermediate levels of self-fertilization may also be maintained within species (Baker 1959;Lloyd 1979;Schemske and Lande 1985;Eckert and Barrett 1994). Even in plants with genetically controlled mechanisms to prevent inbreeding (i.e., SI systems), variation in the strength of SI has long been noted (Jones 1963;Watts 1963;Levin 1996;Good-Avila and Stephenson 2002, 2003). The genetic consequences of variation in mating systems (i.e., quantifying the expected loss of genetic diversity with increased levels of inbreeding) has been assessed within and between species for some groups with known SI systems (e.g., Lloyd 1967; Ockendon and Currah 1979; Mulcahy and Mulcahy 1983; Lyons and Antonovics 1991; Charlesworth and Yang 1998; Liu et al. 1998;Liu et al. 1999;Wright et al. 2002Wright et al. , 2003Busch 2005), but ...
Arabidopsis lyrata is normally considered an obligately outcrossing species with a strong self-incompatibility system, but a shift in mating system towards inbreeding has been found in some North American populations (subspecies A. lyrata ssp. lyrata). This study provides a survey of the Great Lakes region of Canada to determine the extent of this mating system variation and how outcrossing rates are related to current population density, geographical distribution, and genetic diversity. Based on variation at microsatellite markers (progeny arrays to estimate multilocus outcrossing rates and population samples to estimate diversity measures) and controlled greenhouse pollinations, populations can be divided into two groups: (i) group A, consisting of individuals capable of setting selfed seed (including autogamous fruit set in the absence of pollinators), showing depressed outcrossing rates (T(m) = 0.2-0.6), heterozygosity (H(O) = 0.02-0.06) and genetic diversity (H(E) = 0.08-0.10); and (ii) group B, consisting of individuals that are predominantly self-incompatible (T(m) > 0.8), require pollinators for seeds set, and showing higher levels of heterozygosity (H(O) = 0.13-0.31) and diversity (H(E) = 0.19-0.410). Current population density is not related to the shift in mating system but does vary with latitude. Restricted gene flow among populations was evident among all but two populations (F(ST) = 0.11-0.8). Group A populations were more differentiated from one another (F(ST) = 0.78) than they were from group B populations (F(ST) = 0.59), with 41% of the variation partitioned within populations, 47% between populations, and 12% between groups. No significant relationship was found between genetic and geographical distance. Results are discussed in the context of possible postglacial expansion scenarios in relation to loss of self-incompatibility.
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