Comparison of sexual compatibility in crosses between the southern and northern populations of the cabbage beetle Colaphellus bowringi

It is widely accepted that the genetic divergence and reproductive incompat- ibility between closely related species and/or populations is often viewed as an important step toward speciation. In this study, sexual compatibility in crosses between the southern XS population and the northern TA population of the polyandrous cabbage beetle Co- laphellus bowringi was investigated by testing their mating preferences, mating latency, copulation duration, and reproductive performances of post-mating. In choice mating ex- periments, the percentages ofmatings were significantly higher in intra-population crosses than in inter-population crosses. Both isolation index （/） and index of pair sexual isolation （/PSi） indicated partial mating incompatibility or assortative mating in crosses between the two different geographical populations. In single pair mating experiments, XS females in inter-population crosses mated significantly later and copulated significantly shorter than those in intra-population crosses. However, TA females in inter-population crosses mated significantly earlier and copulated longer than those in intra-population crosses, suggesting that larger XS males may enhance heterotypic mating. The lifetime fecundity was highest in XS homotypic matings, lowest in TA homotypic matings, and intermedi- ate in heterotypic rnatings between their parents. The inter-population crosses resulted in significantly lower egg hatching rate and shorter female longevity than intra-population crosses. These results demonstrated that there exist some incompatibilities in premating, postmating-prezygotic, and postzygotic stages between the southern XS population and northern TA population of the cabbage beetle Colaphellus bowringi.     

Inbreeding depression is high in a self‐incompatible perennial herb population but absent in a self‐compatible population showing mixed mating

High inbreeding depression is thought to be one of the major factors preventing evolutionary transitions in hermaphroditic plants from self‐incompatibility (SI) and outcrossing toward self‐compatibility (SC) and selfing. However, when selfing does evolve, inbreeding depression can be quickly purged, allowing the evolution of complete self‐fertilization. In contrast, populations that show intermediate selfing rates (a mixed‐mating system) typically show levels of inbreeding depression similar to those in outcrossing species, suggesting that selection against inbreeding might be responsible for preventing the transition toward complete self‐fertilization. By implication, crosses among populations should reveal patterns of heterosis for mixed‐mating populations that are similar to those expected for outcrossing populations. Using hand‐pollination crosses, we compared levels of inbreeding depression and heterosis between populations of Linaria cavanillesii (Plantaginaceae), a perennial herb showing contrasting mating systems. The SI population showed high inbreeding depression, whereas the SC population displaying mixed mating showed no inbreeding depression. In contrast, we found that heterosis based on between‐population crosses was similar for SI and SC populations. Our results are consistent with the rapid purging of inbreeding depression in the derived SC population, despite the persistence of mixed mating. However, the maintenance of outcrossing after a transition to SC is inconsistent with the prediction that populations that have purged their inbreeding depression should evolve toward complete selfing, suggesting that the transition to SC in L. cavanillesii has been recent. SC in L. cavanillesii thus exemplifies a situation in which the mating system is likely not at an equilibrium with inbreeding depression.     

Evolution of sociality in spiders leads to depleted genomic diversity at both population and species levels

Across several animal taxa, the evolution of sociality involves a suite of characteristics, a “social syndrome,” that includes cooperative breeding, reproductive skew, primary female‐biased sex ratio, and the transition from outcrossing to inbreeding mating system, factors that are expected to reduce effective population size (Ne). This social syndrome may be favoured by short‐term benefits but come with long‐term costs, because the reduction in Ne amplifies loss of genetic diversity by genetic drift, ultimately restricting the potential of populations to respond to environmental change. To investigate the consequences of this social life form on genetic diversity, we used a comparative RAD‐sequencing approach to estimate genomewide diversity in spider species that differ in level of sociality, reproductive skew and mating system. We analysed multiple populations of three independent sister‐species pairs of social inbreeding and subsocial outcrossing Stegodyphus spiders, and a subsocial outgroup. Heterozygosity and within‐population diversity were sixfold to 10‐fold lower in social compared to subsocial species, and demographic modelling revealed a tenfold reduction in Ne of social populations. Species‐wide genetic diversity depends on population divergence and the viability of genetic lineages. Population genomic patterns were consistent with high lineage turnover, which homogenizes the genetic structure that builds up between inbreeding populations, ultimately depleting genetic diversity at the species level. Indeed, species‐wide genetic diversity of social species was 5–8 times lower than that of subsocial species. The repeated evolution of species with this social syndrome is associated with severe loss of genomewide diversity, likely to limit their evolutionary potential.     

MUTATIONAL MELTDOWN IN SELFING ARABIDOPSIS LYRATA

The majority of plant species and many animals are hermaphrodites, with individuals expressing both female and male function. Although hermaphrodites can potentially reproduce by self‐fertilization, they have a high prevalence of outcrossing. The genetic advantages of outcrossing are described by two hypotheses: avoidance of inbreeding depression because selfing leads to immediate expression of recessive deleterious mutations, and release from drift load because self‐fertilization leads to long‐term accumulation of deleterious mutations due to genetic drift and, eventually, to extinction. I tested both hypotheses by experimentally crossing Arabidopsis lyrata plants (self‐pollinated, cross‐pollinated within the population, or cross‐pollinated between populations) and measuring offspring performance over 3 years. There were 18 source populations, each of which was either predominantly outcrossing, mixed mating, or predominantly selfing. Contrary to predictions, outcrossing populations had low inbreeding depression, which equaled that of selfing populations, challenging the central role of inbreeding depression in mating system shifts. However, plants from selfing populations showed the greatest increase in fitness when crossed with plants from other populations, reflecting higher drift load. The results support the hypothesis that extinction by mutational meltdown is why selfing hermaphroditic taxa are rare, despite their frequent appearance over evolutionary time.     

Postglacial ecotype formation under outcrossing and self‐fertilization in Arabidopsis lyrata

The formation of ecotypes has been invoked as an important driver of postglacial biodiversity, because many species colonized heterogeneous habitats and experienced divergent selection. Ecotype formation has been predominantly studied in outcrossing taxa, while far less attention has been paid to the implications of mating system shifts. Here, we addressed whether substrate‐related ecotypes exist in selfing and outcrossing populations of Arabidopsis lyrata subsp. lyrata and whether the genomic footprint differs between mating systems. The North American subspecies colonized both rocky and sandy habitats during postglacial range expansion and shifted the mating system from predominantly outcrossing to predominantly selfing in a number of regions. We performed an association study on pooled whole‐genome sequence data of 20 selfing or outcrossing populations, which suggested genes involved in adaptation to substrate. Motivated by enriched gene ontology terms, we compared root growth between plants from the two substrates in a common environment and found that plants originating from sand grew roots faster and produced more side roots, independent of mating system. Furthermore, single nucleotide polymorphisms associated with substrate‐related ecotypes were more clustered among selfing populations. Our study provides evidence for substrate‐related ecotypes in A. lyrata and divergence in the genomic footprint between mating systems. The latter is the likely result of selfing populations having experienced divergent selection on larger genomic regions due to higher genome‐wide linkage disequilibrium.     

Mating system and the evolution of quantitative traits: an experimental study of Mimulus guttatus

Abstract The mating system of a population profoundly influences its evolution. Inbreeding alters the balance of evolutionary forces that determine the amount of genetic variation within a population. It redistributes that variation among individuals, altering heritabilities and genetic correlations. Inbreeding even changes the basic relationships between these genetic statistics and response to selection. If populations differing only in mating system are exposed to the same selection pressures, will they respond in qualitatively different ways? Here, we address this question by imposing selection on an index of two negatively correlated traits (flower size and development rate) within experimental populations that reproduce entirely by outcrossing, entirely by self‐fertilizing, or by a mixture of outcrossing and selfing. Entirely selfing populations responded mainly by evolving larger flowers whereas outcrossing populations also evolved more rapid development. Divergence occurred despite an equivalent selection regime and no direct effect of mating system on fitness. The study provides an experimental demonstration of how the interaction of selection, genetic drift, and mating system can produce dramatic short‐term changes in trait means, variances, and covariances.     

Limiting inbreeding in disjunct and isolated populations of a woody shrub

Pollen movements and mating patterns are key features that influence population genetic structure. When gene flow is low, small populations are prone to increased genetic drift and inbreeding, but naturally disjunct species may have features that reduce inbreeding and contribute to their persistence despite genetic isolation. Using microsatellite loci, we investigated outcrossing levels, family mating parameters, pollen dispersal, and spatial genetic structure in three populations of Hakea oldfieldii, a fire‐sensitive shrub with naturally disjunct, isolated populations prone to reduction in size and extinction following fires. We mapped and genotyped a sample of 102 plants from a large population, and all plants from two smaller populations (28 and 20 individuals), and genotyped 158–210 progeny from each population. We found high outcrossing despite the possibility of geitonogamous pollination, small amounts of biparental inbreeding, a limited number of successful pollen parents within populations, and significant correlated paternity. The number of pollen parents for each seed parent was moderate. There was low but significant spatial genetic structure up to 10 m around plants, but the majority of successful pollen came from outside this area including substantial proportions from distant plants within populations. Seed production varied among seven populations investigated but was not correlated with census population size. We suggest there may be a mechanism to prevent self‐pollination in H. oldfieldii and that high outcrossing and pollen dispersal within populations would promote genetic diversity among the relatively small amount of seed stored in the canopy. These features of the mating system would contribute to the persistence of genetically isolated populations prone to fluctuations in size.     

How relatedness between mates influences reproductive success: An experimental analysis of self‐fertilization and biparental inbreeding in a marine bryozoan

Kin associations increase the potential for inbreeding. The potential for inbreeding does not, however, make inbreeding inevitable. Numerous factors influence whether inbreeding preference, avoidance, or tolerance evolves, and, in hermaphrodites where both self‐fertilization and biparental inbreeding are possible, it remains particularly difficult to predict how selection acts on the overall inbreeding strategy, and to distinguish the type of inbreeding when making inferences from genetic markers. Therefore, we undertook an empirical analysis on an understudied type of mating system (spermcast mating in the marine bryozoan, Bugula neritina) that provides numerous opportunities for inbreeding preference, avoidance, and tolerance. We created experimental crosses, containing three generations from two populations to estimate how parental reproductive success varies across parental relatedness, ranging from self, siblings, and nonsiblings from within the same population. We found that the production of viable selfed offspring was extremely rare (only one colony produced three selfed offspring) and biparental inbreeding more common. Paternity analysis using 16 microsatellite markers confirmed outcrossing. The production of juveniles was lower for sib mating compared with nonsib mating. We found little evidence for consistent inbreeding, in terms of nonrandom mating, in adult samples collected from three populations, using multiple population genetic inferences. Our results suggest several testable hypotheses that potentially explain the overall mating and dispersal strategy in this species, including early inbreeding depression, inbreeding avoidance through cryptic mate choice, and differential dispersal distances of sperm and larvae.     

Genetic divergence is more tightly related to call variation than landscape features in the Amazonian frogs Physalaemus petersi and P. freibergi

Behavioural isolation from divergence in male advertisement calls and female preferences is hypothesized to cause genetic divergence and speciation in the Amazonian frogs Physalaemus petersi and P. freibergi, yet the importance of call variation and landscape features in genetic divergence is unresolved. We tested for correlations between genetic divergence at microsatellite loci and (1) call variables; and (2) landscape variables among 10 populations of these frogs. Genetic divergence was not correlated with geographical distance, rivers or elevation. There was a strong positive relationship, however, between genetic divergence and inter‐population differences in one call variable, whine dominant frequency. Effective population sizes varied among sites (range = 15–846) and were often small, suggesting that genetic drift could influence call evolution. Evidence for fine‐scale genetic structure within sites was also found. Our results support the hypothesis that behavioural isolation from divergence in male calls and female preferences causes genetic divergence and speciation.     

An unusual barrier to gene flow: perpetually immature larvae from inter-population crosses in the flour beetle, Tribolium castaneum

We genetically characterize an unusual hybrid incompatibility phenotype manifest in F₁ offspring of crosses between two populations of Tribolium castaneum. Hybrid larvae cease development at the third larval instar, persisting as ‘perpetually immature larvae’ thereafter. Although unable to produce viable adult hybrid offspring with one another, each population produces abundant, fertile hybrids with other populations, indicating a recent origin of the incompatibility and facilitating genetic studies. We mapped the paternal component of the hybrid phenotype to a single region, which exhibits two characteristics common to hybrid incompatibility: marker transmission ratio distortion within crosses and elevated genetic divergence between populations. The incompatible variation and an elevation in between‐population genetic divergence is associated with a region containing the T. castaneum ecdysone receptor homologue, a major regulatory switch, controlling larval moults, pupation and metamorphosis. This contributes to understanding the genetics of speciation in the Coleoptera, one of the most speciose of all arthropod taxa.     

The relative importance of factors determining genetic drift: mating system, spatial genetic structure, habitat and census size in Arabidopsis lyrata

? The mating system, dispersal and census size are predicted to determine the magnitude of genetic drift, but little is known about their relative importance in nature. ? We estimated the contributions of several population-level features to genetic drift in 18 populations of Arabidopsis lyrata. The factors were outcrossing rate, within-population spatial genetic structure, census size and substrate type. The expected heterozygosity (H(E)) at 10 microsatellite loci was taken to reflect the effective population size (N(e)) and the strength of genetic drift. ? The mating system explained most of the variation in H(E) (60%), followed by substrate (10%), genetic structure (9%) and census size (6%). The most outcrossing population had a +0.32 higher predicted H(E) than the most selfing population; the estimated N(e) of selfing populations was less than half that of outcrossing populations. Rocky outcrops supported populations with a +0.14 higher H(E) than did sandy substrates. The most structured population had a +0.24 higher H(E) than the least structured population, and the largest population had a +0.18 higher H(E) than the smallest population. ? This study illustrates the importance of outcrossing, genetic structure and the physical environment--together with census size--in maintaining H(E), and suggests that multiple population-level characteristics influence N(e) and the action of genetic drift.     

Heterosis is common and inbreeding depression absent in natural populations of Arabidopsis thaliana

The importance of genetic drift in shaping patterns of adaptive genetic variation in nature is poorly known. Genetic drift should drive partially recessive deleterious mutations to high frequency, and inter‐population crosses may therefore exhibit heterosis (increased fitness relative to intra‐population crosses). Low genetic diversity and greater genetic distance between populations should increase the magnitude of heterosis. Moreover, drift and selection should remove strongly deleterious recessive alleles from individual populations, resulting in reduced inbreeding depression. To estimate heterosis, we crossed 90 independent line pairs of Arabidopsis thaliana from 15 pairs of natural populations sampled across Fennoscandia and crossed an additional 41 line pairs from a subset of four of these populations to estimate inbreeding depression. We measured lifetime fitness of crosses relative to parents in a large outdoor common garden (8,448 plants in total) in central Sweden. To examine the effects of genetic diversity and genetic distance on heterosis, we genotyped parental lines for 869 SNPs. Overall, genetic variation within populations was low (median expected heterozygosity = 0.02), and genetic differentiation was high (median F_ST = 0.82). Crosses between 10 of 15 population pairs exhibited significant heterosis, with magnitudes of heterosis as high as 117%. We found no significant inbreeding depression, suggesting that the observed heterosis is due to fixation of mildly deleterious alleles within populations. Widespread and substantial heterosis indicates an important role for drift in shaping genetic variation, but there was no significant relationship between fitness of crosses relative to parents and genetic diversity or genetic distance between populations.     

Low population genetic differentiation in the Orchidaceae: implications for the diversification of the family

A leading hypothesis for the immense diversity of the Orchidaceae is that skewed mating success and small, disjunct populations lead to strong genetic drift and switches between adaptive peaks. This mechanism is only possible under conditions of low gene flow that lead to high genetic differentiation among populations. We tested whether orchids typically exhibit high levels of population genetic differentiation by conducting a meta‐analysis to compare mean levels of population genetic differentiation (F_ST) between orchids and other diverse families and between rare and common orchids. Compared with other families, the Orchidaceae is typically characterized by relatively low genetic differentiation among populations (mean F_ST = 0.146) at allozyme loci. Rare terrestrial orchids showed higher population genetic differentiation than common orchids, although this value was still lower than the mean for most plant families. All lines of evidence suggest that orchids are typically characterized by low levels of population genetic differentiation, even in species with naturally disjunct populations. As such, we found no strong evidence that genetic drift in isolated populations has played a major role in the diversification of the Orchidaceae. Further research into the diversification of the family needs to unravel the relative roles of biotic and environmental selective pressures in the speciation of orchids.     

Low reproductive isolation and highly variable levels of gene flow reveal limited progress towards speciation between European river and brook lampreys

Ecologically based divergent selection is a factor that could drive reproductive isolation even in the presence of gene flow. Population pairs arrayed along a continuum of divergence provide a good opportunity to address this issue. Here, we used a combination of mating trials, experimental crosses and population genetic analyses to investigate the evolution of reproductive isolation between two closely related species of lampreys with distinct life histories. We used microsatellite markers to genotype over 1000 individuals of the migratory parasitic river lamprey (Lampetra fluviatilis) and freshwater‐resident nonparasitic brook lamprey (Lampetra planeri) distributed in 10 sympatric and parapatric population pairs in France. Mating trials, parentage analyses and artificial fertilizations demonstrated a low level of reproductive isolation between species even though size‐assortative mating may contribute to isolation. Most parapatric population pairs were strongly differentiated due to the joint effects of geographic distance and barriers to migration. In contrast, we found variable levels of gene flow between sympatric populations ranging from panmixia to moderate differentiation, which indicates a gradient of divergence with some population pairs that may correspond to alternative morphs or ecotypes of a single species and others that remain partially isolated. Ecologically based divergent selection may explain these variable levels of divergence among sympatric population pairs, but incomplete genome swamping following secondary contact could have also played a role. Overall, this study illustrates how highly differentiated phenotypes can be maintained despite high levels of gene flow that limit the progress towards speciation.     

Gene flow does not prevent personality and morphological differentiation between two blue tit populations

Understanding the causes and consequences of population phenotypic divergence is a central goal in ecology and evolution. Phenotypic divergence among populations can result from genetic divergence, phenotypic plasticity or a combination of the two. However, few studies have deciphered these mechanisms for populations geographically close and connected by gene flow, especially in the case of personality traits. In this study, we used a common garden experiment to explore the genetic basis of the phenotypic divergence observed between two blue tit (Cyanistes caeruleus) populations inhabiting contrasting habitats separated by 25 km, for two personality traits (exploration speed and handling aggression), one physiological trait (heart rate during restraint) and two morphological traits (tarsus length and body mass). Blue tit nestlings were removed from their population and raised in a common garden for up to 5 years. We then compared adult phenotypes between the two populations, as well as trait‐specific Q_st and F_st. Our results revealed differences between populations similar to those found in the wild, suggesting a genetic divergence for all traits. Q_st–F_st comparisons revealed that the trait divergences likely result from dissimilar selection patterns rather than from genetic drift. Our study is one of the first to report a Q_st–F_st comparison for personality traits and adds to the growing body of evidence that population genetic divergence is possible at a small scale for a variety of traits including behavioural traits.     

gesp: A computer program for modelling genetic effective population size,inbreeding and divergence in substructured populations

The genetically effective population size (N_e) is of key importance for quantifying rates of inbreeding and genetic drift and is often used in conservation management to set targets for genetic viability. The concept was developed for single, isolated populations and the mathematical means for analysing the expected N_e in complex, subdivided populations have previously not been available. We recently developed such analytical theory and central parts of that work have now been incorporated into a freely available software tool presented here. gesp (Genetic Effective population size, inbreeding and divergence in Substructured Populations) is R‐based and designed to model short‐ and long‐term patterns of genetic differentiation and effective population size of subdivided populations. The algorithms performed by gesp allow exact computation of global and local inbreeding and eigenvalue effective population size, predictions of genetic divergence among populations (G_ST) as well as departures from random mating (F_IS, F_IT) while varying (i) subpopulation census and effective size, separately or including trend of the global population size, (ii) rate and direction of migration between all pairs of subpopulations, (iii) degree of relatedness and divergence among subpopulations, (iv) ploidy (haploid or diploid) and (v) degree of selfing. Here, we describe gesp and exemplify its use in conservation genetics modelling.     

Microevolutionary patterns and processes of the Native Hawaiian colonizing fern Odontosoria chinensis (Lindsaeaceae)

Abstract.— The vascular‐plant flora of the Hawaiian Islands is characterized by one of the highest rates of species endemism in the world. Among flowering plants, approximately 89% of species are endemic, and among pteridophytes, about 76% are endemic. At the single‐island level, however, rates of species endemism vary dramatically between these two groups with 80% of angiosperms and only 6% of pteridophytes being single‐island endemics. Thus, in many groups of Hawaiian angiosperms, it is possible to link studies of phylogeny, evolution, and biogeographic history at the interspecific and interisland levels. In contrast, the low level of single‐island species endemism among Hawaiian pteridophytes makes similar interspecific and interisland studies nearly impossible. Higher levels of interisland gene flow may account for the different levels of single‐island endemism in Hawaiian pteridophytes relative to angiosperms. The primary question we addressed in the present study was: Can we infer microevolutionary patterns and processes among populations within widespread species of Hawaiian pteridophytes wherein gene flow is probably common? To address this broad question, we conducted a population genetic study of the native Hawaiian colonizing species Odontosoria chinensis. Data from allozyme analyses allowed us to infer: (1) significant genetic differentiation among populations from different islands; (2) historical patterns of dispersal between particular pairs of islands; (3) archipelago‐level patterns of dispersal and colonization; (4) founder effects among populations on the youngest island of Hawaii; and, (5) that this species primarily reproduces via outcrossing, but may possess a mixed‐mating system.     

Evolutionarily stable oviposition and sex ratio in parasitoid wasps with single‐sex broods

Abstract 1. The flexibility of hymenopteran sex ratios is well documented, particularly in structured populations featuring sib mating. 2. Using game theoretic models, the present study examines species producing single‐sex broods in which sib mating is unlikely, and focuses on the role of population density in determining evolutionarily stable oviposition strategies. 3. Since only mated females can produce offspring of both sexes while unmated females produce only male offspring, mated females are under selection to produce more females overall to balance the primary sex ratio. 4. As the proportion of all females that are mated should increase with density, offspring sex ratio of mated females is strongly linked to density at low to moderate densities. The present study shows that when density becomes low enough for fewer than half of all females to have mated, then female offspring generate higher fitness. 5. In this low density situation, females may gain a fitness benefit from waiting at their emergence site or from using other costly means to find and mate with males before ovipositing. 6. The predicted correspondence between females waiting at the emergence site and fewer than half of females in the population containing sperm, can be tested empirically, as can the somewhat counter‐intuitive prediction that greater access to males should yield a more male‐biased sex ratio in the offspring of mated females. 7. The present study also indicates how measuring the variance in giving up times by females waiting for males at low density, can provide insight into mechanisms determining waiting times.     

Patterns of mating call preferences in túngara frogs, Physalaemus pustulosus

We examine acoustic mating preferences of a focal population at four different scales of divergence: within the population, between populations in the same genetic group, between populations in different genetic groups and between different species. At all scales there is substantial genetic divergence, variation in mating signals and preferences are influenced by signal variation. There is, however, no support for the hypothesis that mating preferences accumulate predictably with genetic distance. Females preferred the local conspecific call to the foreign conspecific call in about one-third of the experiments, and preferred the local call to all of the heterospecific calls tested. But there was no significant relationship between the variation in the strength of preference and genetic distance either among conspecific populations, or among heterospecific species. Thus, in this study macroevolutionary patterns are not apparent at the microevolutionary scale.