Finding the Factors of Reduced Genetic Diversity on X Chromosomes of Macaca fascicularis: Male-Driven Evolution,Demography, and Natural Selection

The ratio of genetic diversity on X chromosomes relative to autosomes in organisms with XX/XY sex chromosomes could provide fundamental insight into the process of genome evolution. Here we report this ratio for 24 cynomolgus monkeys (Macaca fascicularis) originating in Indonesia, Malaysia, and the Philippines. The average X/A diversity ratios in these samples was 0.34 and 0.20 in the Indonesian–Malaysian and Philippine populations, respectively, considerably lower than the null expectation of 0.75. A Philippine population supposed to derive from an ancestral population by founding events showed a significantly lower ratio than the parental population, suggesting a demographic effect for the reduction. Taking sex-specific mutation rate bias and demographic effect into account, expected X/A diversity ratios generated by computer simulations roughly agreed with the observed data in the intergenic regions. In contrast, silent sites in genic regions on X chromosomes showed strong reduction in genetic diversity and the observed X/A diversity ratio in the genic regions cannot be explained by mutation rate bias and demography, indicating that natural selection also reduces the level of polymorphism near genes. Whole-genome analysis of a female cynomolgus monkey also supported the notion of stronger reduction of genetic diversity near genes on the X chromosome.     

Sex ratio rather than population size affects genetic diversity in Antennaria dioica

• Habitat fragmentation and small population size can lead to genetic erosion in threatened plant populations. Classical theory implies that dioecy can counteract genetic erosion as it decreases the magnitude of inbreeding and genetic drift due to obligate outcrossing. However, in small populations, sex ratios may be strongly male‐ or female‐biased, leading to substantial reductions in effective population size. This may theoretically result in a unimodal relationship between sex ratios and genetic diversity; yet, empirical studies on this relationship are scarce.
• Using AFLP markers, we studied genetic diversity, structure and differentiation in 14 highly fragmented Antennaria dioica populations from the Central European lowlands. Our analyses focused on the relationship between sex ratio, population size and genetic diversity.
• Although most populations were small (mean: 35.5 patches), genetic diversity was moderately high. We found evidence for isolation‐by‐distance, but overall differentiation of the populations was rather weak. Females dominated 11 populations, which overall resulted in a slightly female‐biased sex ratio (61.5%). There was no significant relationship between population size and genetic diversity. The proportion of females was not unimodally but positively linearly related to genetic diversity.
• The high genetic diversity and low genetic differentiation suggest that A. dioica has been widely distributed in the Central European lowlands in the past, while fragmentation occurred only in the last decades. Sex ratio has more immediate consequences on genetic diversity than population size. An increasing proportion of females can increase genetic diversity in dioecious plants, probably due to a higher amount of sexual reproduction.

     

Population size changes reshape genomic patterns of diversity

Elucidating the forces responsible for genomic variation is critical for understanding evolution. Under standard conditions, X-linked diversity is expected to be three-quarters the level of autosomal diversity. Empirical data often deviate from this prediction, but the reasons for these departures are unclear. We demonstrate that population size changes can greatly alter relative levels of X-linked and autosomal variation: population size reductions lead to particularly low X-linked diversity, whereas growth elevates X-linked relative to autosomal diversity. Genetic variation from a diverse array of taxa supports an important role for this effect in accounting for population differences in the ratio of X-linked to autosomal diversity. Consideration of this effect may improve the inference of population history and other evolutionary processes.     

Variations in elk aggregation patterns across a range of elk population sizes at Wall Creek,Montana

In the Greater Yellowstone Ecosystem, growing concern over increasing rates of brucellosis seroprevalence in wildlife has challenged wildlife managers to develop strategies for minimizing the potential for pathogen exchange within and between wildlife populations. Recent evidence suggests that increases in elk seroprevalence may be associated with increasing elk densities and/or increasing size of elk aggregations. However, the interactions between elk population density, landscape factors, and elk aggregation patterns are not well-understood, making appropriate management responses challenging. Using a unique, long-term elk aggregation dataset collected across a wide range of elk population sizes, we investigated relationships between elk population size, landscape factors, and elk aggregation responses (group size and group density) with goals of clarifying how changes in elk population size may affect elk aggregation patterns. Overall, landscape attributes and weather had a stronger influence on elk aggregation patterns than factors such as elk population size that are within management control. We found little evidence that elk population size affected mean elk group sizes, but we did find evidence that the size and density of the largest elk aggregations increased as elk population size increased. We also found some evidence that group densities increased following the establishment of wolves. However, across the relatively wide range of elk population sizes observed in this study, only modest changes in elk group density were observed, suggesting that dramatic reductions in population sizes would be necessary to produce measureable reductions in elk group density to affect frequency-dependent transmission. Management actions designed to lower disease transmission are likely to negatively affect other objectives related to elk management and conservation. We therefore suggest that a first step in managing disease transmission risk is agreement among stakeholders interested in elk management of all objectives related to elk management, including acknowledgment that disease transmission is undesirable. © 2011 The Wildlife Society.     

Detection of reduction in population size using data from microsatellite loci

We demonstrate that the mean ratio of the number of alleles to the range in allele size, which we term M, calculated from a population sample of microsatellite loci, can be used to detect reductions in population size. Using simulations, we show that, for a general class of mutation models, the value of M decreases when a population is reduced in size. The magnitude of the decrease is positively correlated with the severity and duration of the reduction in size. We also find that the rate of recovery of M following a reduction in size is positively correlated with post-reduction population size, but that recovery occurs in both small and large populations. This indicates that M can distinguish between populations that have been recently reduced in size and those which have been small for a long time. We employ M to develop a statistical test for recent reductions in population size that can detect such changes for more than 100 generations with the post-reduction demographic scenarios we examine. We also compute M for a variety of populations and species using microsatellite data collected from the literature. We find that the value of M consistently predicts the reported demographic history for these populations. This method, and others like it, promises to be an important tool for the conservation and management of populations that are in need of intervention or recovery.     

Reduced X-linked diversity in derived populations of house mice

Contrasting patterns of X-linked vs. autosomal diversity may be indicative of the mode of selection operating in natural populations. A number of observations have shown reduced X-linked (or Z-linked) diversity relative to autosomal diversity in various organisms, suggesting a large impact of genetic hitchhiking. However, the relative contribution of other forces such as population bottlenecks, variation in reproductive success of the two sexes, and differential introgression remains unclear. Here, we survey 13 loci, 6 X-linked and 7 autosomal, in natural populations of the house mouse (Mus musculus) subspecies complex. We studied seven populations of three different subspecies, the eastern house mouse M. musculus castaneus, the central house mouse M. m. musculus, and the western house mouse M. m. domesticus, including putatively ancestral and derived populations for each. All populations display lower diversity on the X chromosomes relative to autosomes, and this effect is most pronounced in derived populations. To assess the role of demography, we fit the demographic parameters that gave the highest likelihood of the data using coalescent simulations. We find that the reduction in X-linked diversity is too large to be explained by a simple demographic model in at least two of four derived populations. These observations are also not likely to be explained by differences in reproductive success between males and females. They are consistent with a greater impact of positive selection on the X chromosome, and this is supported by the observation of an elevated K(A) and elevated K(A)/K(S) ratios on the rodent X chromosome. A second contribution may be that the X chromosome less readily introgresses across subspecies boundaries.     

Contrasting X-Linked and Autosomal Diversity across 14 Human Populations

Contrasting the genetic diversity of the human X chromosome (X) and autosomes has facilitated understanding historical differences between males and females and the influence of natural selection. Previous studies based on smaller data sets have left questions regarding how empirical patterns extend to additional populations and which forces can explain them. Here, we address these questions by analyzing the ratio of X-to-autosomal (X/A) nucleotide diversity with the complete genomes of 569 females from 14 populations. Results show that X/A diversity is similar within each continental group but notably lower in European (EUR) and East Asian (ASN) populations than in African (AFR) populations. X/A diversity increases in all populations with increasing distance from genes, highlighting the stronger impact of diversity-reducing selection on X than on the autosomes. However, relative X/A diversity (between two populations) is invariant with distance from genes, suggesting that selection does not drive the relative reduction in X/A diversity in non-Africans (0.842 ± 0.012 for EUR-to-AFR and 0.820 ± 0.032 for ASN-to-AFR comparisons). Finally, an array of models with varying population bottlenecks, expansions, and migration from the latest studies of human demographic history account for about half of the observed reduction in relative X/A diversity from the expected value of 1. They predict values between 0.91 and 0.94 for EUR-to-AFR comparisons and between 0.91 and 0.92 for ASN-to-AFR comparisons. Further reductions can be predicted by more extreme demographic events in excess of those captured by the latest studies but, in the absence of these, also by historical sex-biased demographic events or other processes.     

Reproductive Mode and the Evolution of Genome Size and Structure in Caenorhabditis Nematodes

The self-fertile nematode worms Caenorhabditis elegans, C. briggsae, and C. tropicalis evolved independently from outcrossing male-female ancestors and have genomes 20-40% smaller than closely related outcrossing relatives. This pattern of smaller genomes for selfing species and larger genomes for closely related outcrossing species is also seen in plants. We use comparative genomics, including the first high quality genome assembly for an outcrossing member of the genus (C. remanei) to test several hypotheses for the evolution of genome reduction under a change in mating system. Unlike plants, it does not appear that reductions in the number of repetitive elements, such as transposable elements, are an important contributor to the change in genome size. Instead, all functional genomic categories are lost in approximately equal proportions. Theory predicts that self-fertilization should equalize the effective population size, as well as the resulting effects of genetic drift, between the X chromosome and autosomes. Contrary to this, we find that the self-fertile C. briggsae and C. elegans have larger intergenic spaces and larger protein-coding genes on the X chromosome when compared to autosomes, while C. remanei actually has smaller introns on the X chromosome than either self-reproducing species. Rather than being driven by mutational biases and/or genetic drift caused by a reduction in effective population size under self reproduction, changes in genome size in this group of nematodes appear to be caused by genome-wide patterns of gene loss, most likely generated by genomic adaptation to self reproduction per se.     

Small population size and extremely low levels of genetic diversity in island populations of the platypus, Ornithorhynchus anatinus

Genetic diversity generally underpins population resilience and persistence. Reductions in population size and absence of gene flow can lead to reductions in genetic diversity, reproductive fitness, and a limited ability to adapt to environmental change increasing the risk of extinction. Island populations are typically small and isolated, and as a result, inbreeding and reduced genetic diversity elevate their extinction risk. Two island populations of the platypus, Ornithorhynchus anatinus, exist; a naturally occurring population on King Island in Bass Strait and a recently introduced population on Kangaroo Island off the coast of South Australia. Here we assessed the genetic diversity within these two island populations and contrasted these patterns with genetic diversity estimates in areas from which the populations are likely to have been founded. On Kangaroo Island, we also modeled live capture data to determine estimates of population size. Levels of genetic diversity in King Island platypuses are perilously low, with eight of 13 microsatellite loci fixed, likely reflecting their small population size and prolonged isolation. Estimates of heterozygosity detected by microsatellites (H(E)= 0.032) are among the lowest level of genetic diversity recorded by this method in a naturally outbreeding vertebrate population. In contrast, estimates of genetic diversity on Kangaroo Island are somewhat higher. However, estimates of small population size and the limited founders combined with genetic isolation are likely to lead to further losses of genetic diversity through time for the Kangaroo Island platypus population. Implications for the future of these and similarly isolated or genetically depauperate populations are discussed.     

Elongation of the body in eels

The shape of the body affects how organisms move, where they live, and how they feed. One body plan that has long engaged the interest of both evolutionary biologists and functional morphologists is axial elongation. There is a growing interest in the correlates and evolution of elongation within different terrestrial and aquatic vertebrate clades. At first glance, Anguilliformes may appear to exhibit a single cylindrical form but there is considerable diversity underlying this seemingly simplified body plan. Here, we explore evolution of the axial skeleton in 54 anguilliform taxa and some close relatives. We describe the diversity of axial elongation as well as investigate how characters such as head length, branchial-arch length, and shape of the pectoral fins correlate with vertebral number to possibly facilitate changes in absolute diameter of the body. Overall, we find that precaudal vertebral numbers and caudal vertebral numbers are evolving independently across elopomorph fishes. We also find that precaudal and caudal vertebral aspect ratios are evolving together across elopomorph fishes. When focusing within Anguilliformes we find striking diversity in the mechanisms of elongation of the body, including almost every trend for axial elongation known within actinopterygian fishes. The three major clades of eels we examined have slightly different mechanisms of elongation. We also find a suite of morphological characters associated with elongation in anguilliform fishes that appears to coincide with a more fossorial lifestyle such as high elongation ratios, a more posteriorly extended-branchial region, and a reduction in the size of the pectoral fins. Lastly, we point out that a diverse range of derived behaviors such as head- and tail-first burrowing, rotational feeding, and knotting around prey are only found in long cylindrical vertebrates.     

Coalescence in a metapopulation with recurrent local extinction and recolonization

Abstract Many species exist as metapopulations in balance between local population extinction and recolonization. The effect of these processes on average population differentiation, within-deme diversity, and specieswide diversity has been considered previously. In this paper, coalescent simulations of Slatkin's propagule-pool and migrant-pool models are used to characterize the distribution of neutral genetic diversity within demes (π_s), diversity in the metapopulation a whole (TT_T), the ratio F _ST= (π_t–π_S)/π_T, Tajima's D statistic, and several ratios of gene-tree branch lengths. Using these distributions, power to detect differences in key metapopulation parameter values is determined under contrasting sampling regimes. The results indicate that it will be difficult to use sequence data from a single locus to detect a history of extinctions and recolonizations in a metapopulation because of high genealogical variance, the loss of diversity due to reductions in effective population size, and the fact that a genealogy of lineages from different demes under Slatkin's model differs from a neutral coalescent only in its time scale. Genetic indices of gene-tree shape that capture the effects of extinction/recolonization on both external branches and the length of the genealogy as a whole will provide the best indication of metapopulation dynamics if several lineages are sampled from several different demes.     

Interpopulation variation in mating system and late-stage inbreeding depression in Magnolia stellata

Inbreeding has the potential to cause evolutionary changes in populations, although these changes are likely to drive populations to extinction through inbreeding depression and reductions in genetic diversity. We investigated the mating system and late-stage inbreeding depression (δ) in 10 populations of Magnolia stellata using nine microsatellite markers and evaluated the effects of population size and the degree of population isolation through inbreeding and inbreeding depression on the persistence of populations. The outcrossing rates were very similar (~0.7) among populations, but the correlations of paternity, fractions of biparental inbreeding and inbreeding coefficients at the seed stage ( F _S) varied among populations, suggesting that the level of outcrossing was similar among populations, while the quality of it was not. A significant negative correlation was detected between F _S and population size. The average value of δ was 0.709, and the values in six of the 10 populations were significant. The values of δ differed among populations, although clear relationships with population size and the degree of population isolation were not detected. However, in one population, which was very small and located in the edge of the species' range, we obtained a very low value of δ (–0.096), which may be indicative of purging or the fixation of deleterious alleles. Existing M. stellata populations that are small (and thus might be expected to have higher frequencies of inbreeding) and have large values of δ may be in danger of declining, even if the populations are located within the central region of the species' range.     

Loss and Recovery of Genetic Diversity in Adapting Populations of HIV

The evolution of drug resistance in HIV occurs by the fixation of specific, well-known, drug-resistance mutations, but the underlying population genetic processes are not well understood. By analyzing within-patient longitudinal sequence data, we make four observations that shed a light on the underlying processes and allow us to infer the short-term effective population size of the viral population in a patient. Our first observation is that the evolution of drug resistance usually occurs by the fixation of one drug-resistance mutation at a time, as opposed to several changes simultaneously. Second, we find that these fixation events are accompanied by a reduction in genetic diversity in the region surrounding the fixed drug-resistance mutation, due to the hitchhiking effect. Third, we observe that the fixation of drug-resistance mutations involves both hard and soft selective sweeps. In a hard sweep, a resistance mutation arises in a single viral particle and drives all linked mutations with it when it spreads in the viral population, which dramatically reduces genetic diversity. On the other hand, in a soft sweep, a resistance mutation occurs multiple times on different genetic backgrounds, and the reduction of diversity is weak. Using the frequency of occurrence of hard and soft sweeps we estimate the effective population size of HIV to be ( confidence interval ). This number is much lower than the actual number of infected cells, but much larger than previous population size estimates based on synonymous diversity. We propose several explanations for the observed discrepancies. Finally, our fourth observation is that genetic diversity at non-synonymous sites recovers to its pre-fixation value within 18 months, whereas diversity at synonymous sites remains depressed after this time period. These results improve our understanding of HIV evolution and have potential implications for treatment strategies.     

Ecological genetics of range size variation in Boechera spp. (Brassicaceae)

Many taxonomic groups contain both rare and widespread species, which indicates that range size can evolve quickly. Many studies have compared molecular genetic diversity, plasticity, or phenotypic traits between rare and widespread species; however, a suite of genetic attributes that unites rare species remains elusive. Here, using two rare and two widespread Boechera (Brassicaceae) species, we conduct a simultaneous comparison of quantitative trait diversity, genetic diversity, and population structure among species with highly divergent range sizes. Consistent with previous studies, we do not find strong associations between range size and within‐population genetic diversity. In contrast, we find that both the degree of phenotypic plasticity and quantitative trait structure (Q_ST) were positively correlated with range size. We also found higher F_ST: Q_ST ratios in rare species, indicative of either a greater response to stabilizing selection or a lack of additive genetic variation. While widespread species occupy more ecological and climactic space and have diverged at both traits and markers, rare species display constrained levels of population differentiation and phenotypic plasticity. Combined, our results provide evidence for a specialization–generalization trade‐off across three orders of magnitude of range size variation in the ecological model genus, Boechera.     

Invading populations of an ornamental shrub show rapid life history evolution despite genetic bottlenecks

Human-mediated species introductions offer opportunities to investigate when and how non-native species to adapt to novel environments, and whether evolution has the potential to contribute to colonization success. Many long-established introductions harbour high genetic diversity, raising the possibility that multiple introductions of genetic material catalyze adaptation and/or the evolution of invasiveness. Studies of nascent invasions are rare but crucial for understanding whether genetic diversity facilitates population expansion. We explore variation and evolution in founder populations of the invasive shrub Hypericum canariense . We find that these introductions have experienced large reductions in genetic diversity, but that increased growth and a latitudinal cline in flowering phenology have nevertheless evolved. These life history changes are consistent with predictions for invasive plants. Our results highlight the potential for even genetically depauperate founding populations to adapt and evolve invasive patters of spread.     

Indirect evidence from DNA sequence diversity for genetic degeneration of the Y-chromosome in dioecious species of the plant Silene: the SlY4/SlX4 and DD44-X/DD44-Y gene pairs

The action of natural selection is expected to reduce the effective population size of a nonrecombining chromosome, and this is thought to be the chief factor leading to genetic degeneration of Y-chromosomes, which cease recombining during their evolution from ordinary chromosomes. Low effective population size of Y chromosomes can be tested by studying DNA sequence diversity of Y-linked genes. In the dioecious plant, Silene latifolia, which has sex chromosomes, one comparison (SlX1 vs. SlY1) indeed finds lower Y diversity compared with the homologous X-linked gene, and one Y-linked gene with no X-linked homologue has lower species-wide diversity than a homologous autosomal copy (SlAp3Y vs. SlAp3A). To test whether this is a general pattern for Y-linked genes, we studied two further recently described X and Y homologous gene pairs in samples from several populations of S. latifolia and S. dioica. Diversity is reduced for both Y-linked genes, compared with their X-linked homologues. Our new data are analysed to show that the low Y effective size cannot be explained by different levels of gene flow for the X vs. the Y chromosomes, either between populations or between these closely related species. Thus, all four Y-linked genes that have now been studied in these plants (the two studied here, and two previously studied genes, have low diversity). This supports other evidence for an ongoing degeneration process in these species.     

Reduced polymorphism associated with X chromosome meiotic drive in the stalk-eyed fly Teleopsis dalmanni

Sex chromosome meiotic drive has been suggested as a cause of several evolutionary genetic phenomena, including genomic conflicts that give rise to reproductive isolation between new species. In this paper we present a population genetic analysis of X chromosome drive in the stalk-eyed fly, Teleopsis dalmanni, to determine how this natural polymorphism influences genetic diversity. We analyzed patterns of DNA sequence variation at two X-linked regions (comprising 1325 bp) approximately 50 cM apart and one autosomal region (comprising 921 bp) for 50 males, half of which were collected in the field from one of two allopatric locations and the other half were derived from lab-reared individuals with known brood sex ratios. These two populations are recently diverged but exhibit partial postzygotic reproductive isolation, i.e. crosses produce sterile hybrid males and fertile females. We find no nucleotide or microsatellite variation on the drive X chromosome, whereas the same individuals show levels of variation at autosomal regions that are similar to field-collected flies. Furthermore, one field-caught individual collected 10 years previously had a nearly identical X haplotype to the drive X, and is over 2% divergent from other haplotypes sampled from the field. These results are consistent with a selective sweep that has removed genetic variation from much of the drive X chromosome. We discuss how this finding may relate to the rapid evolution of postzygotic reproductive isolation that has been documented for these flies.     

High Genetic Diversity and Differentiation in Relict Lowland Populations of Gentianella austriaca (A. and J. Kern.) Holub (Gentianaceae)

Abstract: The biennial Gentianella austriaca (A. & J. Kern.) Holub, representing a nutrient-poor grassland taxon of low competition power, is becoming rare in the lowlands of eastern Austria due to changes in land use. To estimate effects of isolation and decreasing population sizes, as well as evolutionary relationships, we investigated variation in isozymes and morphological characters within and between seven populations from the mountains, foothills, and lowlands. Additionally, data on reproduction, habitat, germination and population sizes were collected to examine possible causes of variation and differentiation. We found highest genetic diversity (v_a, v_go) in the lowland and foothill populations, and highest genetic differentiation (D_ja, D_jgo) (i.e., lowest genetic identity: Nei's I) in the lowland populations. The low diversity of the mountain populations might indicate that they are derived from lowland populations. Surprisingly, highest genetic diversity was found in the smallest population. This indicates that in small remnant populations of taxa with a mixed mating system, genetic diversity might be maintained even after many generations after reducing population size dramatically. We found some relationship between genetic diversity and high fitness (germination success) and (inversely) with seed size. Plant size and reproductive success are negatively correlated with altitude, whereas flower size and seed size seem to be subject to other forces of selection. Combining all morphometric, reproductive and genetic traits, the lowland populations are most strongly differentiated and therefore of highest conservation priority.     

Genetic uniqueness of the Waorani tribe from the Ecuadorian Amazon

South America and especially the Amazon basin is known to be home to some of the most isolated human groups in the world. Here, we report on a study of mitochondrial DNA (mtDNA) in the Waorani from Ecuador, probably the most warlike human population known to date. Seeking to look in more depth at the characterization of the genetic diversity of this Native American tribe, molecular markers from the X and Y chromosomes were also analyzed. Only three different mtDNA haplotypes were detected among the Waorani sample. One of them, assigned to Native American haplogroup A2, accounted for more than 94% of the total diversity of the maternal gene pool. Our results for sex chromosome molecular markers failed to find close genetic kinship between individuals, further emphasizing the low genetic diversity of the mtDNA. Bearing in mind the results obtained for both the analysis of the mtDNA control region and complete mitochondrial genomes, we suggest the existence of a 'Waorani-specific' mtDNA lineage. According to current knowledge on the phylogeny of haplogroup A2, we propose that this lineage could be designated as subhaplogroup A2s. Its wide predominance among the Waorani people might have been conditioned by severe genetic drift episodes resulting from founding events, long-term isolation and a traditionally small population size most likely associated with the striking ethnography of this Amazonian community. In all, the Waorani constitute a fine example of how genetic imprint may mirror ethnopsychology and sociocultural features in human populations.     

A metapopulation perspective on genetic diversity and differentiation in partially self-fertilizing plants

Abstract.— Partial self-fertilization is common in higher plants. Mating system variation is known to have important consequences for how genetic variation is distributed within and among populations. Selfing is known to reduce effective population size, and inbreeding species are therefore expected to have lower levels of genetic variation than comparable out crossing taxa. However, several recent empirical studies have shown that reductions in genetic diversity within populations of inbreeding species are far greater than the expected reductions based on the reduced effective population size. Two different processes have been argued to cause these patterns, selective sweeps (or hitchhiking) and background selection. Both are expected to be most effective in reducing genetic variation in regions of low recombination rates. Selfing is known to reduce the effective recombination rate, and inbreeding taxa are thus thought to be particularly vulnerable to the effects of hitchhiking or background selection. Here I propose a third explanation for the lower-than-expected levels of genetic diversity within populations of selfing species; recurrent extinctions and recolonizations of local populations, also known as metapopulation dynamics. I show that selfing in a metapopulation setting can result in large reductions in genetic diversity within populations, far greater than expected based the lower effective population size inbreeding species is expected to have. The reason for this depends on an interaction between selfing and pollen migration.