The effects of historical fragmentation on major histocompatibility complex class II β and microsatellite variation in the Aegean island reptile,Podarcis erhardii

The major histocompatibility complex (MHC) plays a key role in disease resistance and is the most polymorphic gene region in vertebrates. Although habitat fragmentation is predicted to lead to a loss in MHC variation through drift, the impact of other evolutionary forces may counter this effect. Here we assess the impact of selection, drift, migration, and recombination on MHC class II and microsatellite variability in 14 island populations of the Aegean wall lizard Podarcis erhardii. Lizards were sampled from islands within the Cyclades (Greece) formed by rising sea levels as the last glacial maximum approximately 20,000 before present. Bathymetric data were used to determine the area and age of each island, allowing us to infer the corresponding magnitude and timing of genetic bottlenecks associated with island formation. Both MHC and microsatellite variation were positively associated with island area, supporting the hypothesis that drift governs neutral and adaptive variation in this system. However, MHC but not microsatellite variability declined significantly with island age. This discrepancy is likely due to the fact that microsatellites attain mutation‐drift equilibrium more rapidly than MHC. Although we detected signals of balancing selection, recombination and migration, the effects of these evolutionary processes appeared negligible relative to drift. This study demonstrates how land bridge islands can provide novel insights into the impact of historical fragmentation on genetic diversity as well as help disentangle the effects of different evolutionary forces on neutral and adaptive diversity.     

Balancing selection, random genetic drift, and genetic variation at the major histocompatibility complex in two wild populations of guppies (Poecilia reticulata)

Our understanding of the evolution of genes of the major histocompatibility complex (MHC) is rapidly increasing, but there are still enigmatic questions remaining, particularly regarding the maintenance of high levels of MHC polymorphisms in small, isolated populations. Here, we analyze the genetic variation at eight microsatellite loci and sequence variation at exon 2 of the MHC class IIB (DAB) genes in two wild populations of the Trinidadian guppy, Poecilia reticulata. We compare the genetic variation of a small (Ne, 100) and relatively isolated upland population to that of its much larger (Ne approximately 2400) downstream counterpart. As predicted, microsatellite diversity in the upland population is significantly lower and highly differentiated from the population further downstream. Surprisingly, however, these guppy populations are not differentiated by MHC genetic variation and show very similar levels of allelic richness. Computer simulations indicate that the observed level of genetic variation can be maintained with overdominant selection acting at three DAB loci. The selection coefficients differ dramatically between the upland (s > or = 0.2) and lowland (s < or = 0.01) populations. Parasitological analysis on wild-caught fish shows that parasite load is significantly higher on upland than on lowland fish, which suggests that large differences in selection intensity may indeed exist between populations. Based on the infection intensity, a substantial proportion of the upland fish would have suffered direct or indirect fitness consequences as a result of their high parasite loads. Selection by parasites plays a particularly important role in the evolution of guppies in the upland habitat, which has resulted in high levels of MHC diversity being maintained in this population despite considerable genetic drift.     

Disentangling the role of MHC‐dependent ‘good genes' and ‘compatible genes' in mate‐choice decisions of three‐spined sticklebacks Gasterosteus aculeatus under semi‐natural conditions

To investigate and disentangle the role of major histocompatibility complex (MHC)‐based ‘good genes' and ‘compatible genes' in mate choice, three‐spined sticklebacks Gasterosteus aculeatus with specific MHC IIB genotypes were allowed to reproduce in an outdoor enclosure system. Here, fish were protected from predators but encountered their natural parasites. Mate choice for an intermediate genetic distance between parental MHC genotypes was observed, which would result in intermediate diversity in the offspring, but no mate choice based on good genes was found under the current semi‐natural conditions. Investigation of immunological variables revealed that the less‐specific innate immune system was more active in individuals with a genetically more divergent MHC allele repertoire. This suggests the need to compensate for an MHC‐diminished T‐cell repertoire and potentially explains the observed mate choice for intermediate MHC genetic distance. The present findings support a general pattern of mate choice for intermediate MHC diversity (i.e. compatible genes). In addition, the potentially dynamic role of MHC good genes in mate choice under different parasite pressures is discussed in the light of present and previous results.     

The impact of translocations on neutral and functional genetic diversity within and among populations of the Seychelles warbler

Translocations are an increasingly common tool in conservation. The maintenance of genetic diversity through translocation is critical for both the short‐ and long‐term persistence of populations and species. However, the relative spatio‐temporal impacts of translocations on neutral and functional genetic diversity, and how this affects genetic structure among the conserved populations overall, have received little investigation. We compared the impact of translocating different numbers of founders on both microsatellite and major histocompatibility complex (MHC) class I diversity over a 23‐year period in the Seychelles warbler (Acrocephalus sechellensis). We found low and stable microsatellite and MHC diversity in the source population and evidence for only a limited loss of either type of diversity in the four new populations. However, we found evidence of significant, but low to moderate, genetic differentiation between populations, with those populations established with fewer founders clustering separately. Stochastic genetic capture (as opposed to subsequent drift) was the main determinant of translocated population diversity. Furthermore, a strong correlation between microsatellite and MHC differentiation suggested that neutral processes outweighed selection in shaping MHC diversity in the new populations. These data provide important insights into how to optimize the use of translocation as a conservation tool.     

The hidden benefits of sex: Evidence for MHC‐associated mate choice in primate societies

Major histocompatibility complex (MHC)‐associated mate choice is thought to give offspring a fitness advantage through disease resistance. Primates offer a unique opportunity to understand MHC‐associated mate choice within our own zoological order, while their social diversity provides an exceptional setting to examine the genetic determinants and consequences of mate choice in animal societies. Although mate choice is constrained by social context, increasing evidence shows that MHC‐dependent mate choice occurs across the order in a variety of socio‐sexual systems and favours mates with dissimilar, diverse or specific genotypes non‐exclusively. Recent research has also identified phenotypic indicators of MHC quality. Moreover, novel findings rehabilitate the importance of olfactory cues in signalling MHC genes and influencing primate mating decisions. These findings underline the importance to females of selecting a sexual partner of high genetic quality, as well as the generality of the role of MHC genes in sexual selection.     

Limited polymorphism of the functional MHC class II B gene in the black‐spotted frog (Pelophylax nigromaculatus) identified by locus‐specific genotyping

Amphibians can be more vulnerable to environmental changes and diseases than other species because of their complex life cycle and physiological requirements. Therefore, understanding the adaptation of amphibians to environmental changes is crucial for their conservation. Major histocompatibility complex (MHC) presents an excellent tool for the investigation of adaptive variations and the assessment of adaptive potential because it can be under strong diversifying selection. Here, we isolated the MHC class II B (MHCIIB) gene from cDNA sequences of the black‐spotted frog (Pelophylax nigromaculatus), a widespread amphibian species in China, and designed locus‐specific primers to characterize adaptive variability of this amphibian. Ten alleles were identified from 67 individual frogs of three populations and no more than two alleles were present in each individual animal. Furthermore, none of the sequences had indels or/and stop codons, which is in good agreement with locus‐specific amplification of a functional gene. However, we found low polymorphism at both nucleotide and amino acid levels, even in the antigen‐binding region. Purifying selection acting at this locus was supported by the findings that the d_N/d_S ratio across all alleles was below 1 and that negatively selected sites were detected by different methods. Allele frequency distributions were significantly different among geographic populations, indicating that physiographic factors may have strong effect on the genetic structure of the black‐spotted frog. This study revealed limited polymorphism of three adjacent black‐spotted frog populations at the functional MHCIIB locus, which may be attributed to region‐specific differences. The locus‐specific genotyping technique developed in this study would provide a foundation for future studies on adaptive divergence among different frog populations.     

Contrasting patterns of selection and drift between two categories of immune genes in prairie‐chickens

Immune‐receptor genes of the adaptive immune system, such as the major histocompatibility complex (MHC), are involved in recognizing specific pathogens and are known to have high rates of adaptive evolution, presumably as a consequence of rapid co‐evolution between hosts and pathogens. In contrast, many ‘mediating’ genes of the immune system do not interact directly with specific pathogens and are involved in signalling (e.g. cytokines) or controlling immune cell growth. As a consequence, we might expect stronger selection at immune‐receptor than mediating genes, but these two types of genes have not been compared directly in wild populations. Here, we tested the hypothesis that selection differs between MHC (class I and II) and mediating genes by comparing levels of population differentiation across the range of greater prairie‐chickens (Tympanuchus cupido). As predicted, there was stronger population differentiation and isolation by distance at immune receptor (MHC) than at either mediating genes or neutral microsatellites, suggesting a stronger role of local adaptation at the MHC. In contrast, mediating genes displayed weaker differentiation between populations than neutral microsatellites, consistent with selection favouring similar alleles across populations for mediating genes. In addition to selection, drift also had a stronger effect on immune receptor (MHC) than mediating genes as indicated by the stronger decline of MHC variation in relation to population size. This is the first study in the wild to show that the effects of selection and drift on immune genes vary across populations depending on their functional role.     

No postcopulatory selection against MHC‐homozygous offspring: Evidence from a pedigreed captive rhesus macaque colony

The heterozygosity status of polymorphic elements of the immune system, such as the major histocompatibility complex (MHC), is known to increase the potential to cope with a wider variety of pathogens. Pre‐ and postcopulatory processes may regulate MHC heterozygosity. In a population where mating occurs among individuals that share identical MHC haplotypes, postcopulatory selection may disfavour homozygous offspring or ones with two MHC haplotypes identical to its mother. We tested these ideas by determining the incidence of MHC‐heterozygous and MHC‐homozygous individuals in a pedigreed, partially consanguineous captive rhesus monkey colony. Bayesian statistics showed that when parents share MHC haplotypes, the distribution of MHC‐heterozygous and MHC‐homozygous individuals significantly fitted the expected Mendelian distribution, both for the complete MHC haplotypes, and for MHC class I or II genes separately. Altogether, we found in this captive colony no evidence for postcopulatory selection against MHC‐homozygous individuals. However, the distribution of paternally and maternally inherited MHC haplotypes tended to differ significantly from expected. Individuals with two MHC haplotypes identical to their mother were underrepresented and offspring with MHC haplotypes identical to their father tended to be overrepresented. This suggests that postcopulatory processes affect MHC haplotype combination in offspring, but do not prevent low MHC heterozygosity.     

Immunogenetic heterogeneity in a widespread ungulate: the European roe deer (Capreolus capreolus)

Understanding how immune genetic variation is shaped by selective and neutral processes in wild populations is of prime importance in both evolutionary biology and epidemiology. The European roe deer (Capreolus capreolus) has considerably expanded its distribution range these last decades, notably by colonizing agricultural landscapes. This range shift is likely to have led to bottlenecks and increased roe deer exposure to a new range of pathogens that until recently predominantly infected humans and domestic fauna. We therefore investigated the historical and contemporary forces that have shaped variability in a panel of genes involved in innate and acquired immunity in roe deer, including Mhc‐Drb and genes encoding cytokines or toll‐like receptors (TLRs). Together, our results suggest that genetic drift is the main contemporary evolutionary force shaping immunogenetic variation within populations. However, in contrast to the classical view, we found that some innate immune genes involved in micropathogen recognition (e.g. Tlrs) continue to evolve dynamically in roe deer in response to pathogen‐mediated positive selection. Most studied Tlrs (Tlr2, Tlr4 and Tlr5) had similarly high levels of amino acid diversity in the three studied populations including one recently established in southwestern France that showed a clear signature of genetic bottleneck. Tlr2 implicated in the recognition of Gram‐positive bacteria in domestic ungulates, showed strong evidence of balancing selection. The high immunogenetic variation revealed here implies that roe deer are able to cope with a wide spectrum of pathogens and to respond rapidly to emerging infectious diseases.     

The Park Grass Experiment and next‐generation approaches: local adaptation of sweet vernal grass revisited

Long‐term ecological experiments provide unique opportunities to observe the effects of natural selection. The Park Grass Experiment at Rothamsted Experiment Station in Hertfordshire, UK, is the longest running ecological experiment that incorporates fertilization treatments and has been ongoing since 1856. In the 1970s, local adaptation was observed in the grass Anthoxanthum odoratum to the elevated soil aluminium levels of the fertilized plots. Gould et al. ( 2014 ) have utilized this system to reevaluate the extent of local adaptation, first documented nearly 45 years ago (Snaydon 1970 ), and to use emerging molecular approaches to identify candidate genes for the adaptation. From their work, they identify several plausible candidate loci for aluminium tolerance. This work shows the power of long‐term field‐based trials in a scientific age concentrated on rapidly emerging molecular techniques often utilized in short, narrowly focused laboratory or controlled environment experiments. The current study clearly illustrates the benefits gained by combining these molecular approaches within long‐term monitoring experiments that can be regularly revisited in a changing world and used to address questions on evolutionary scales.     

Family‐assisted inference of the genetic architecture of major histocompatibility complex variation

With their direct link to individual fitness, genes of the major histocompatibility complex (MHC) are a popular system to study the evolution of adaptive genetic diversity. However, owing to the highly dynamic evolution of the MHC region, the isolation, characterization and genotyping of MHC genes remain a major challenge. While high‐throughput sequencing technologies now provide unprecedented resolution of the high allelic diversity observed at the MHC, in many species, it remains unclear (i) how alleles are distributed among MHC loci, (ii) whether MHC loci are linked or segregate independently and (iii) how much copy number variation (CNV) can be observed for MHC genes in natural populations. Here, we show that the study of allele segregation patterns within families can provide significant insights in this context. We sequenced two MHC class I (MHC‐I) loci in 1267 European barn owls (Tyto alba), including 590 offspring from 130 families using Illumina MiSeq technology. Coupled with a high per‐individual sequencing coverage (~3000×), the study of allele segregation patterns within families provided information on three aspects of the architecture of MHC‐I variation in barn owls: (i) extensive sharing of alleles among loci, (ii) strong linkage of MHC‐I loci indicating tandem architecture and (iii) the presence of CNV in the barn owl MHC‐I. We conclude that the additional information that can be gained from high‐coverage amplicon sequencing by investigating allele segregation patterns in families not only helps improving the accuracy of MHC genotyping, but also contributes towards enhanced analyses in the context of MHC evolutionary ecology.     

Rapid loss of MHC class II variation in a bottlenecked population is explained by drift and loss of copy number variation

Population bottlenecks may reduce genetic variation and potentially increase the risk of extinction. Here, we present the first study to use historic samples to analyse loss of variation at the major histocompatibility complex (MHC), which plays a central role in vertebrate disease resistance. Balancing selection acts on the MHC and could moderate the loss of variation expected from drift; however, in a Wisconsin population of greater prairie-chickens (Tympanuchus cupido), the number of MHC class II B alleles per individual declined by 44% following a population bottleneck, compared to a loss of only 8% at microsatellites. Simulations indicate that drift likely reduced MHC variation at the population level, as well as within individuals by reducing the number of gene copies per individual or by fixing the same alleles across multiple loci. These multiple effects of genetic drift on MHC variation could have important implications for immunity and fitness.     

Coalescence 2.0: a multiple branching of recent theoretical developments and their applications

Population genetics theory has laid the foundations for genomic analyses including the recent burst in genome scans for selection and statistical inference of past demographic events in many prokaryote, animal and plant species. Identifying SNPs under natural selection and underpinning species adaptation relies on disentangling the respective contribution of random processes (mutation, drift, migration) from that of selection on nucleotide variability. Most theory and statistical tests have been developed using the Kingman coalescent theory based on the Wright‐Fisher population model. However, these theoretical models rely on biological and life history assumptions which may be violated in many prokaryote, fungal, animal or plant species. Recent theoretical developments of the so‐called multiple merger coalescent models are reviewed here (Λ‐coalescent, beta‐coalescent, Bolthausen‐Sznitman, Ξ‐coalescent). We explain how these new models take into account various pervasive ecological and biological characteristics, life history traits or life cycles which were not accounted in previous theories such as (i) the skew in offspring production typical of marine species, (ii) fast adapting microparasites (virus, bacteria and fungi) exhibiting large variation in population sizes during epidemics, (iii) the peculiar life cycles of fungi and bacteria alternating sexual and asexual cycles and (iv) the high rates of extinction‐recolonization in spatially structured populations. We finally discuss the relevance of multiple merger models for the detection of SNPs under selection in these species, for population genomics of very large sample size and advocate to potentially examine the conclusion of previous population genetics studies.     

Ecology can inform genetics: Disassortative mating contributes to MHC polymorphism in Leach’s storm‐petrels (Oceanodroma leucorhoa)

Studies of MHC‐based mate choice in wild populations often test hypotheses on species exhibiting female choice and male–male competition, which reflects the general prevalence of females as the choosy sex in natural systems. Here, we examined mutual mate‐choice patterns in a small burrow‐nesting seabird, the Leach’s storm‐petrel (Oceanodroma leucorhoa), using the major histocompatibility complex (MHC). The life history and ecology of this species are extreme: both partners work together to fledge a single chick during the breeding season, a task that requires regularly travelling hundreds of kilometres to and from foraging grounds over a 6‐ to 8‐week provisioning period. Using a 5‐year data set unprecedented for this species (n = 1078 adults and 925 chicks), we found a positive relationship between variation in the likelihood of female reproductive success and heterozygosity at Ocle‐DAB2, a MHC class IIB locus. Contrary to previous reports rejecting disassortative mating as a mechanism for maintaining genetic polymorphism in this species, here we show that males make significant disassortative mate‐choice decisions. Variability in female reproductive success suggests that the most common homozygous females (Ocle‐DAB2*01/Ocle‐DAB2*01) may be physiologically disadvantaged and, therefore, less preferred as lifelong partners for choosy males. The results from this study support the role of mate choice in maintaining high levels of MHC variability in a wild seabird species and highlight the need to incorporate a broader ecological framework and sufficient sample sizes into studies of MHC‐based mating patterns in wild populations in general.     

The Genetic Paradox of Invasions revisited: the potential role of inbreeding × environment interactions in invasion success

Invasive species that successfully establish, persist, and expand within an area of introduction, in spite of demographic bottlenecks that reduce their genetic diversity, represent a paradox. Bottlenecks should inhibit population growth and invasive expansion, as a decrease in genetic diversity should result in inbreeding depression, increased fixation of deleterious mutations by genetic drift (drift load), and reduced evolutionary potential to respond to novel selection pressures. Here, we focus on the problems of inbreeding depression and drift load in introduced populations as key components of the Genetic Paradox of Invasions (GPI). We briefly review published explanations for the GPI, which are based on various mechanisms (invasion history events, reproductive traits, genetic characteristics) that mediate the avoidance of inbreeding depression and drift load. We find that there is still a substantial lack of explanation and empirical evidence for explaining the GPI for strongly bottlenecked invasions, or for during critical invasion phases (e.g. initial colonization, leading edges of range expansion) where strong genetic depletion, inbreeding depression and drift load occurs. Accordingly, we suggest that discussion of the GPI should be revived to find additional mechanisms applicable to explaining invasion success for such species and invasion phases. Based on a synthesis of the literature on the population genetics of invaders and the ecology of invaded habitats, we propose that inbreeding × environment (I × E) interactions are one such mechanism that may have strong explanatory power to address the GPI. Specifically, we suggest that a temporary or permanent release from stress in invaded habitats may alleviate the negative effects of genetic depletion on fitness via I × E interactions, and present published empirical evidence supporting this hypothesis. We additionally discuss that I × E interactions can result in rapid evolutionary changes, and may even contribute to adaptation of invaders in the absence of high genetic variation. With a view to encouraging further empirical research, we propose an experimental approach to investigate the occurrence of I × E interactions in ongoing invasions. Revived research on the GPI should provide new fundamental insights into eco‐evolutionary invasion biology, and more generally into the evolutionary consequences of the interactions between inbreeding and environment.     

Experimental manipulation of population‐level MHC diversity controls pathogen virulence evolution in Mus musculus

The virulence levels attained by serial passage of pathogens through similar host genotypes are much higher than observed in natural systems; however, it is unknown what keeps natural virulence levels below these empirically demonstrated maximum levels. One hypothesis suggests that host diversity impedes pathogen virulence, because adaptation to one host genotype carries trade‐offs in the ability to replicate and cause disease in other host genotypes. To test this hypothesis, with the simplest level of population diversity within the loci of the major histocompatibility complex (MHC), we serially passaged Friend virus complex (FVC) through two rounds, in hosts with either the same MHC genotypes (pure passage) or hosts with different MHC genotypes (alternated passage). Alternated passages showed a significant overall reduction in viral titre (31%) and virulence (54%) when compared to pure passages. Furthermore, a resistant host genotype initially dominated any effects due to MHC diversity; however, when FVC was allowed to adapt to the resistant host genotype, predicted MHC effects emerged; that is, alternated lines show reduced virulence. These data indicate serial exposure to diverse MHC genotypes is an impediment to pathogen adaptation, suggesting genetic variation at MHC loci is important for limiting virulence in a rapidly evolving pathogen and supports negative frequency‐dependent selection as a force maintaining MHC diversity in host populations.     

Patterns of MHC‐dependent mate selection in humans and nonhuman primates: a meta‐analysis

Genes of the major histocompatibility complex (MHC) in vertebrates are integral for effective adaptive immune response and are associated with sexual selection. Evidence from a range of vertebrates supports MHC‐based preference for diverse and dissimilar mating partners, but evidence from human mate choice studies has been disparate and controversial. Methodologies and sampling peculiarities specific to human studies make it difficult to know whether wide discrepancies in results among human populations are real or artefact. To better understand what processes may affect MHC‐mediated mate choice across humans and nonhuman primates, we performed phylogenetically controlled meta‐analyses using 58 effect sizes from 30 studies across seven primate species. Primates showed a general trend favouring more MHC‐diverse mates, which was statistically significant for humans. In contrast, there was no tendency for MHC‐dissimilar mate choice, and for humans, we observed effect sizes indicating selection of both MHC‐dissimilar and MHC‐similar mates. Focusing on MHC‐similar effect sizes only, we found evidence that preference for MHC similarity was an artefact of population ethnic heterogeneity in observational studies but not among experimental studies with more control over sociocultural biases. This suggests that human assortative mating biases may be responsible for some patterns of MHC‐based mate choice. Additionally, the overall effect sizes of primate MHC‐based mating preferences are relatively weak (Fisher's Z correlation coefficient for dissimilarity Zr = 0.044, diversity Zr = 0.153), calling for careful sampling design in future studies. Overall, our results indicate that preference for more MHC‐diverse mates is significant for humans and likely conserved across primates.     

Extensive polymorphism of the major histocompatibility complex DRA gene in Balkan donkeys: perspectives on selection and genealogy

The major histocompatibility complex (MHC) contains genes important for immune response in mammals, and these genes exhibit high polymorphism and diversity. The DRA gene, a member of the MHC class II family, is highly conserved across a large number of mammalian species, but it displays exceptionally rich sequence variations in Equidae members. We analyzed allelic polymorphism of the DRA locus in 248 donkeys sampled across the Balkan Peninsula (Albania, Bulgaria, Croatia, Macedonia, Greece and Montenegro). Five known alleles and two new alleles were identified. The new allele Eqas‐DRA*0601 was found to carry a synonymous mutation, and new allele Eqas‐DRA*0701, a non‐synonymous mutation. We further analyzed the historical selection and allele genealogy at the DRA locus in equids. Signals of positive selection obtained by various tests were ambiguous. A conservative conclusion is that DRA polymorphism occurred relatively recently and that positive selection has been acting on the DRA locus for a relatively brief period.     

MHC‐disassortative mate choice and inbreeding avoidance in a solitary primate

Sexual selection theory suggests that choice for partners carrying dissimilar genes at the major histocompatibility complex (MHC) may play a role in maintaining genetic variation in animal populations by limiting inbreeding or improving the immunity of future offspring. However, it is often difficult to establish whether the observed MHC dissimilarity among mates drives mate choice or represents a by‐product of inbreeding avoidance based on MHC‐independent cues. Here, we used 454‐sequencing and a 10‐year study of wild grey mouse lemurs (Microcebus murinus), small, solitary primates from western Madagascar, to compare the relative importance on the mate choice of two MHC class II genes, DRB and DQB, that are equally variable but display contrasting patterns of selection at the molecular level, with DRB under stronger diversifying selection. We further assessed the effect of the genetic relatedness and of the spatial distance among candidate mates on the detection of MHC‐dependent mate choice. Our results reveal inbreeding avoidance, along with disassortative mate choice at DRB, but not at DQB. DRB‐disassortative mate choice remains detectable after excluding all related dyads (characterized by a relatedness coefficient r > 0), but varies slightly with the spatial distance among candidate mates. These findings suggest that the observed deviations from random mate choice at MHC are driven by functionally important MHC genes (like DRB) rather than passively resulting from inbreeding avoidance and further emphasize the need for taking into account the spatial and genetic structure of the population in correlative tests of MHC‐dependent mate choice.     

The effects of genetic drift during range expansion on geographical patterns of variation: a computer simulation of the colonization of Australia by Bufo marinus

A computer simulation is performed of allele frequency changes resulting from genetic drift at eleven loci during the probable course of colonization of Australia by populations of the Giant Toad, Bufo marinus. The history of twelve populations for which allele frequency data are available is modelled. Account is taken of the likely pattern of relationship among the populations, the effective size of the populations (as indicated by the observed variance of allele frequencies) and the probable isolation of the populations from each other following their separation. In all simulations, allele frequencies at some loci show a significant association with latitude while others do not. In six of ten simulations, there is a significant association between degree of variation at a locus and the presence of a latitudinal cline of allele frequencies. There are also indications of this kind of association in simulations of a uni-directional range expansion. These results demonstrate that such associations, which were also observed in the data from the actual populations, can result from genetic drift during a range expansion, and therefore cannot be taken as evidence of the action of natural selection.