Estimating Long-Term Mating Systems Using DNA Sequences

Plant mating systems often involve a mixture of self fertilizations and outcross fertilizations. The degree of selfing has a large impact on the genetic composition of natural populations and on the evolution of the mating system itself in response to such factors as inbreeding depression. This paper describes a means of estimating the long-term rate of self-fertilization from samples of alleles taken from individuals in a population. Use is made of the genealogy of pairs of alleles at a locus within individuals and pairs between individuals. The degree of selfing is closely related to the extent to which the number of nucleotide sites differing within an individual is reduced relative to the number differing between individuals. Importantly, the estimate of long-term selfing is largely independent of population size and is not affected by historical fluctuations in population size; instead it responds directly to the mating system itself. The approach outlined here is most appropriate to evolutionary problems in which the long-term nature of the mating system is of interest, such as to determine the relationship between prior inbreeding and inbreeding depression.     

The interdependence of mating structure and inbreeding depression

The level of inbreeding depression depends on the genetic structure and composition of a population, and is not a meaningful concept in its own right. Models are presented for the dynamics of alleles governing mating strategy when viability is determined by generalized heterosis or lethal recessive alleles. It is shown that a protected polymorphism for mating strategy may ensue from generalized heterosis, while lethal recessive alleles may favor the common mating strategy. Further, neither model provides the conditions allowing spread of an allele when rare (protection) which are obtained by assuming as constant the level of inbreeding depression associated with the equilibrium genetic structure dictated by the common mating strategy.     

Mate availability contributes to maintain the mixed‐mating system in a scolytid beetle

We investigated the mating system and population genetic structure of the beetle, Coccotrypes dactyliperda, with life history characteristics that suggest the presence of a stable mixed‐mating system. We examined the genetic structure of seven populations in Israel and found significant departures from the Hardy–Weinberg equilibrium and an excess of homozygosity. Inbreeding coefficients were highly variable across populations, suggesting that low levels of outbreeding occur in nature. Experiments were conducted to determine whether the observed high inbreeding in these populations is the result of a reproductive assurance strategy. Females reared in the laboratory took longer to mate with males from the same population (inbreeding) than with males from a different population (outbreeding). These results suggest that females delayed inbreeding, and were more inclined to outbreed when possible. Thus inbreeding, which predominates in most populations, may be due to a shortage of mates for outbreeding rather than a preference for inbreeding. We conclude that C. dactyliperda has a mixed‐mating system that may be maintained by a reproductive assurance strategy.     

The effect of reproductive compensation on recessive disorders within consanguineous human populations

We investigate the effects of consanguinity and population substructure on genetic health using the UK Asian population as an example. We review and expand upon previous treatments dealing with the deleterious effects of consanguinity on recessive disorders and consider how other factors, such as population substructure, may be of equal importance. For illustration, we quantify the relative risks of recessive lethal disorders by presenting some simple calculations that demonstrate the effect 'reproductive compensation' has on the maintenance of recessive alleles. The results show how reproductive compensation can effectively counteract the purging of deleterious alleles within consanguineous populations. Whereas inbreeding does not elevate the equilibrium frequency of affected individuals, reproductive compensation does. We suggest this effect must be built into interpretations of the incidence of genetic disease within populations such as the UK Asians. Information of this nature will benefit health care workers who inform such communities.     

Population genetics of sporophytic self-incompatibility in Senecio squalidus L. (Asteraceae) II: a spatial autocorrelation approach to determining mating behaviour in the presence of low S allele diversity

We recently estimated that as few as six S alleles represent the extent of S locus diversity in a British population of the self-incompatible (SI) coloniser Senecio squalidus (Oxford Ragwort). Despite the predicted constraints to mating imposed by such a low number of S alleles, S. squalidus maintains a strong sporophytic self-incompatibility (SSI) system and there is no evidence for a breakdown of SSI or any obvious negative reproductive consequences for this highly successful coloniser. The present paper assesses mating behaviour in an Oxford S. squalidus population through observations of its effect on spatial patterns of genetic diversity and thus the extent to which it is responsible for ameliorating the potentially detrimental reproductive consequences of low S allele diversity in British S. squalidus. A spatial autocorrelation (SA) treatment of S locus and allozyme polymorphism data for four loci indicates that mating events regularly occur at all the distance classes examined from 60 to 480 m throughout the entire sample population. Less SA is observed for S locus data than for allozyme data in accordance with the hypothesis that SSI and low diversity at the S locus are driving these large-scale mating events. The limited population structure at small distances of 60 m and less observed for SA analysis of the Me-2 locus and by F-statistics for all the allozyme data, is evidence of some local relatedness due to limited seed and pollen dispersal in S. squalidus. However, the overall impression of mating dynamics in this S. squalidus population is that of ample potential mating opportunities with many individuals at large population scales, indicating that reproductive success is not seriously affected by few S alleles available for mating interactions.     

The effects of genetic screening and assortative mating on lethal recessive-allele frequencies and homozygote incidence.

The widespread use of genetic screening, along with mating and reproductive patterns reflecting that information, can significantly alter the genetic structure of populations. Both allele frequencies and mortality could be significantly reduced if carriers of lethal recessive alleles were withdrawn from the mating pool. But schemes to mask deleterious alleles in heterozygous condition could significantly increase the deleterious-allele frequencies while resulting in only a slight reduction in mortality. The immediate and equilibrium consequences of such mating strategies may be quite disparate.     

An explicit model for the inbreeding load in the evolutionary analysis of selfing

I present analytical predictions for the equilibrium inbreeding load expected in a population under mutation, selection, and a regular mating system for any population size and for any magnitude and recessivity of the deleterious effects. Using this prediction, I deduce the relative fitness of mutant alleles with small effect on selfing to explore the situations where selfing or outcrossing are expected to evolve. The results obtained are in agreement with previous literature, showing that natural selection is expected to lead to stable equilibria where populations show either complete outcrossing or complete selfing, and that selfing is promoted by large deleterious mutation rates. I find that the evolution of selfing is favored by a large recessivity of deleterious effects, while the magnitude of homozygous deleterious effects only becomes relevant in relatively small populations. This result contradicts the standard assumption that purging in large populations will only promote selfing when homozygous deleterious effects are large, and implies that previously published results obtained assuming lethal mutations in large populations can be extrapolated to nonlethal alleles of similar recessivity. This conclusion and the general approach used in this analysis can be useful in the study of the evolution of mating systems.     

Loss and gain of sexual reproduction in the same stick insect

The outcome of competition between different reproductive strategies within a single species can be used to infer selective advantage of the winning strategy. Where multiple populations have independently lost or gained sexual reproduction it is possible to investigate whether the advantage is contingent on local conditions. In the New Zealand stick insect Clitarchus hookeri, three populations are distinguished by recent change in reproductive strategy and we determine their likely origins. One parthenogenetic population has established in the United Kingdom and we provide evidence that sexual reproduction has been lost in this population. We identify the sexual population from which the parthenogenetic population was derived, but show that the UK females have a post‐mating barrier to fertilisation. We also demonstrate that two sexual populations have recently arisen in New Zealand within the natural range of the mtDNA lineage that otherwise characterizes parthenogenesis in this species. We infer independent origins of males at these two locations using microsatellite genotypes. In one population, a mixture of local and nonlocal alleles suggested males were the result of invasion. Males in another population were most probably the result of loss of an X chromosome that produced a male phenotype in situ. Two successful switches in reproductive strategy suggest local competitive advantage for outcrossing over parthenogenetic reproduction. Clitarchus hookeri provides remarkable evidence of repeated and rapid changes in reproductive strategy, with competitive outcomes dependent on local conditions.     

Plant population dynamics, pollinator foraging, and the selection of self-fertilization

Many flowering plants rely on pollinators, self-fertilization, or both for reproduction. We model the consequences of these features for plant population dynamics and mating system evolution. Our mating systems-based population dynamics model includes an Allee effect. This often leads to an extinction threshold, defined as a density below which population densities decrease. Reliance on generalist pollinators who primarily visit higher density plant species increases the extinction threshold, whereas autonomous modes of selfing decrease and can eliminate the threshold. Generalist pollinators visiting higher density plant species coupled with autonomous selfing may introduce an effect where populations decreasing in density below the extinction threshold may nonetheless persist through selfing. The extinction threshold and selfing at low density result in populations where individuals adopting a single reproductive strategy exhibit mating systems that depend on population density. The ecological and evolutionary analyses provide a mechanism where prior selfing evolves even though inbreeding depression is greater than one-half. Simultaneous consideration of ecological and evolutionary dynamics confirms unusual features (e.g., evolution into extinction or abrupt increases in population density) implicit in our separate consideration of ecological and evolutionary scenarios. Our analysis has consequences for understanding pollen limitation, reproductive assurance, and the evolution of mating systems.     

Host mating system and the prevalence of disease in a plant population

A modified susceptible-infected-recovered (SIR) host-pathogen model is used to determine the influence of plant mating system on the outcome of a host-pathogen interaction. Unlike previous models describing how interactions between mating system and pathogen infection affect individual fitness, this model considers the potential consequences of varying mating systems on the prevalence of resistance alleles and disease within the population. If a single allele for disease resistance is sufficient to confer complete resistance in an individual and if both homozygote and heterozygote resistant individuals have the same mean birth and death rates, then, for any parameter set, the selfing rate does not affect the proportions of resistant, susceptible or infected individuals at equilibrium. If homozygote and heterozygote individual birth rates differ, however, the mating system can make a difference in these proportions. In that case, depending on other parameters, increased selfing can either increase or decrease the rate of infection in the population. Results from this model also predict higher frequencies of resistance alleles in predominantly selfing compared to predominantly outcrossing populations for most model conditions. In populations that have higher selfing rates, the resistance alleles are concentrated in homozygotes, whereas in more outcrossing populations, there are more resistant heterozygotes.     

Reduced mate availability leads to evolution of self‐fertilization and purging of inbreeding depression in a hermaphrodite

Basic models of mating‐system evolution predict that hermaphroditic organisms should mostly either cross‐fertilize, or self‐fertilize, due to self‐reinforcing coevolution of inbreeding depression and outcrossing rates. However transitions between mating systems occur. A plausible scenario for such transitions assumes that a decrease in pollinator or mate availability temporarily constrains outcrossing populations to self‐fertilize as a reproductive assurance strategy. This should trigger a purge of inbreeding depression, which in turn encourages individuals to self‐fertilize more often and finally to reduce male allocation. We tested the predictions of this scenario using the freshwater snail Physa acuta, a self‐compatible hermaphrodite that preferentially outcrosses and exhibits high inbreeding depression in natural populations. From an outbred population, we built two types of experimental evolution lines, controls (outcrossing every generation) and constrained lines (in which mates were often unavailable, forcing individuals to self‐fertilize). After ca. 20 generations, individuals from constrained lines initiated self‐fertilization earlier in life and had purged most of their inbreeding depression compared to controls. However, their male allocation remained unchanged. Our study suggests that the mating system can rapidly evolve as a response to reduced mating opportunities, supporting the reproductive assurance scenario of transitions from outcrossing to selfing.     

普通野生稻小种群的交配系统与遗传多样性

小种群的遗传动态是保育遗传学关注的核心问题之一,而种群遗传动态又与交配系统密切相关.普通野生稻(Oryza rufipogon Griff.)是具有重要经济价值的濒危物种,目前其种群规模都较小,研究其小种群交配系统与遗传变异性对普通野生稻的保护具有重要意义.运用7对SSR引物,对采自江西东乡普通野生稻小种群的36份种茎和其中20个家系共计601份子代进行了分析.结果显示:该种群的表观异交率为0.318,多位点法估计(MLTR)的多位点异交率为0.481;50%以上的子代共享亲本,非随机交配明显;东乡普通野生稻种群交配系统属于混合交配类型.比较亲本和子代种群的遗传变异性显示:子代种群比亲本种群遗传变异性更丰富;子代种群的杂合子不足与种群变小自交比例上升有关;而亲本种群杂合子过剩可能与杂合基因型的选择优势有关.这些结果说明创造条件扩大种群规模对普通野生稻的原生境保护显得尤为重要.     

Workers' sons rescue genetic diversity at the sex locus in an invasive honey bee population

The hallmark of eusociality is the division of labour between reproductive (queen) and nonreproductive (worker) females. Yet in many eusocial insects, workers retain the ability to produce haploid male offspring from unfertilized eggs. The reproductive potential of workers has well‐documented consequences for the structure and function of insect colonies, but its implications at the population level are less often considered. We show that worker reproduction in honey bees can have an important role in maintaining genetic diversity at the sex locus in invasive populations. The honey bee sex locus is homozygous‐lethal, and, all else being equal, a higher allele number in the population lead to higher mean brood survival. In an invasive population of the honey bee Apis cerana in Australia, workers contribute significantly to male production: 38% of male‐producing colonies are queenless, and these contribute one‐third of all males at mating congregations. Using a model, we show that such male production by queenless workers will increase the number of sex alleles retained in nascent invasive populations following founder events, relative to a scenario in which only queens reproduce. We conclude that by rescuing sex locus diversity that would otherwise be lost, workers' sons help honey bee populations to minimize the negative effects of inbreeding after founder events and so contribute to their success as invaders.     

Color Assortative Mating in a Mainland Population of the Poison Frog Oophaga pumilio

Assortative mating is a reproductive strategy used by a diversity of animals, in which individuals choose a mate that shares similar characteristics. This mating strategy has the potential to promote the evolution of various sexual signals and has been a proposed mechanism driving and maintaining color variation in the anuran family Dendrobatidae. Most studies have examined this reproductive strategy in the polytypic poison frog, Oophaga pumilio, in the Bocas del Toro archipelago in Panama. Little attention, however, has been given to ancestral populations across this species’ mainland range, where dramatic color polytypism appears to lack. Additionally, most studies are exclusively experimental and investigate mate choice between allopatric populations, neglecting the behaviors of naturally occurring mates. This study observed natural mating pairs within a population of O. pumilio on mainland Costa Rica and tested the prediction that color phenotype of mating females and males would be correlated. Naturally occurring pairs were found to share similar coloration, suggesting that color assortative mating operates in nature, and in a mainland population. Our results indicate that coloration is an important trait in driving the natural mate choices of female O. pumilio, which provides valuable insight into realistic mate selection tactics of this dendrobatid frog.     

Reproductive compensation in the evolution of plant mating systems

Reproductive compensation, the replacement of dead embryos by potentially viable ones, is known to play a major role in the maintenance of deleterious mutations in mammalian populations. However, it has received little attention in plant evolution. Here we model the joint evolution of mating system and inbreeding depression with reproductive compensation. We used a dynamic model of inbreeding depression, allowing for partial purging of recessive lethal mutations by selfing. We showed that reproductive compensation tended to increase the mean number of lethals in a population, but favored self-fertilization by effectively decreasing early inbreeding depression. When compensation depended on the selfing rate, stable mixed mating systems can occur, with low to intermediate selfing rates. Experimental evidence of reproductive compensation is required to confirm its potential importance in the evolution of plant mating systems. We suggest experimental methods to detect reproductive compensation.     

Virus-immune dynamics determined by prey-predator interaction network and epistasis in viral fitness landscape

The emergence and persistence of polymorphism within populations generally requires specific regimes of natural or sexual selection. Here, we develop a unified theoretical framework to explore how polymorphism at targeted loci can be generated and maintained by either disassortative mating choice or balancing selection due to, for example, heterozygote advantage. To this aim, we model the dynamics of alleles at a single locus A in a population of haploid individuals, where reproductive success depends on the combination of alleles carried by the parents at locus A. Our theoretical study of the model confirms that the conditions for the persistence of a given level of allelic polymorphism depend on the relative reproductive advantages among pairs of individuals. Interestingly, equilibria with unbalanced allelic frequencies were shown to emerge from successive introduction of mutants. We then investigate the role of the function linking allelic divergence to reproductive advantage on the evolutionary fate of alleles within the population. Our results highlight the significance of the shape of this function for both the number of alleles maintained and their level of genetic divergence. Large number of alleles are maintained with substantial replacement of alleles, when disassortative advantage slowly increases with allelic differentiation . In contrast, few highly differentiated alleles are predicted to be maintained when genetic differentiation has a strong effect on disassortative advantage. These opposite effects predicted by our model explain how disassortative mate choice may lead to various levels of allelic differentiation and polymorphism, and shed light on the effect of mate preferences on the persistence of balanced and unbalanced polymorphism in natural population.

     

High genetic diversity in the remnant island population of hihi and the genetic consequences of re-introduction

The maintenance of genetic diversity is thought to be fundamental for the conservation of threatened species. It is therefore important to understand how genetic diversity is affected by the re-introduction of threatened species. We use establishment history and genetic data from the remnant and re-introduced populations of a New Zealand endemic bird, the hihi Notiomystis cincta, to understand genetic diversity loss and quantify the genetic effects of re-introduction. Our data do not support any recent bottleneck events in the remnant population. Furthermore, all genetic diversity measures indicate the remnant hihi population has retained high levels of genetic diversity relative to other New Zealand avifauna with similar histories of decline. Genetic diversity (N(A) , alleles per locus, allelic richness, F(IS) and H(S) ) did not significantly decrease in new hihi populations founded through re-introduction when compared to their source populations, except in the Kapiti Island population (allelic richness and H(S) ) which had very slow post-re-introduction population growth. The N(e) /N(c) ratio in the remnant population was high, but decreased in first-level re-introductions, which together with significant genetic differentiation between populations (F(ST) & Fisher's exact tests) suggest that extant populations are diverging as a result of founder effects and drift. Importantly, simulations of future allele loss predict that the number of alleles lost will be higher in populations with a slow population growth, fewer founding individuals and with nonrandom mating. Interestingly, this species has very high levels of extra-pair paternity which may reduce reproductive variance by allowing social and floater males to reproduce a life history trait that together with a large remnant population size may help maintain higher levels of genetic diversity than expected.     

Engineered underdominance allows efficient and economical introgression of traits into pest populations

A novel form of underdominance is suggested as a mechanism that is able to drive desired genes into pest populations through the release of transgenic individuals over one or more generations. Such a mechanism is urgently needed by those working to reduce the impact of malaria by releasing strains of Anopheles, the vector of the disease, that are not susceptible to malaria parasites. We use simple population genetics models to quantify the benefits conferred when heterozygous genotypes, arising from matings between introduced and wild individuals, are not viable. In a randomly mating population, underdominant systems accelerate introgression of desired alleles and allow the release of individuals to be discontinued once the frequency of transgenic alleles attains a threshold. A set of two constructs, which together are selectively neutral but lethal when one is carried without the other, are found to produce dynamics that are characteristic of underdominant systems. When these constructs are carried on non-homologous chromosomes, then the ratio of released to natural born individuals need only be greater than 3:100 for introgression to occur. Furthermore, the threshold for the gene frequencies over which the introduced genes are expected to become fixed upon discontinuing the release of transgenic individuals is surprisingly low. The location of the threshold suggests that the introduced genes are expected to spread in space, at least locally. For the first time, the prospect of a practical drive mechanism for the genetic manipulation of pest populations is raised.     

The effect of mating system on growth of Arabidopsis lyrata in response to inoculation with the biotrophic parasite Albugo candida

The effects of variation in host reproductive systems on response to pathogens are not well understood. We inoculated individuals from outcrossing and inbreeding populations of North American Arabidopsis lyrata with Albugo candida (white blister rust) to test the effect of mating system and heterozygosity on disease response. We observed three host infection phenotypes, classified as fully resistant, partially resistant and fully susceptible. Overall, inbreeding populations had more susceptible and fewer partially resistant individuals than outcrossing populations, but the highest proportion of resistant individuals was found in two of the inbreeding populations. Mating system did not affect relative growth rate of inoculated plants, but there were strong effects of population and infection phenotype. We conclude that mating system per se does not determine the resistance of natural A. lyrata populations to infection by Albugo, but that the increased variability in responses among inbreeding populations may be due to reduced effective population size.     

Microsatellite analysis reveals genetically distinct populations of red pine (Pinus resinosa, Pinaceae)

Red pine (Pinus resinosa Ait.) is an ecologically and economically important forest tree species of northeastern North America and is considered one of the most genetically depauperate conifer species in the region. We have isolated and characterized 13 nuclear microsatellite loci by screening a partial genomic library with di-, tri-, and tetranucleotide repeat oligonucleotide probes. In an analysis of over 500 individuals representing 17 red pine populations from Manitoba through Newfoundland, five polymorphic microsatellite loci with an average of nine alleles per locus were identified. The mean expected and observed heterozygosity values were 0.508 and 0.185, respectively. Significant departures from Hardy-Weinberg equilibrium with excess homozygosity indicating high levels of inbreeding were evident in all populations studied. The population differentiation was high with 28-35% of genetic variation partitioned among populations. The genetic distance analysis showed that three northeastern (two Newfoundland and one New Brunswick) populations are genetically distinct from the remaining populations. The coalescence-based analysis suggests that "northeastern" and "main" populations likely became isolated during the most recent Pleistocene glacial period, and severe population bottlenecks may have led to the evolution of a highly selfing mating system in red pine.