Insight into the roles of selection in speciation from genomic patterns of divergence and introgression in secondary contact in venomous rattlesnakes

Investigating secondary contact of historically isolated lineages can provide insight into how selection and drift influence genomic divergence and admixture. Here, we studied the genomic landscape of divergence and introgression following secondary contact between lineages of the Western Diamondback Rattlesnake (Crotalus atrox) to determine whether genomic regions under selection in allopatry also contribute to reproductive isolation during introgression. We used thousands of nuclear loci to study genomic differentiation between two lineages that have experienced recent secondary contact following isolation, and incorporated sampling from a zone of secondary contact to identify loci that are resistant to gene flow in hybrids. Comparisons of patterns of divergence and introgression revealed a positive relationship between allelic differentiation and resistance to introgression across the genome, and greater‐than‐expected overlap between genes linked to lineage‐specific divergence and loci that resist introgression. Genes linked to putatively selected markers were related to prominent aspects of rattlesnake biology that differ between populations of Western Diamondback rattlesnakes (i.e., venom and reproductive phenotypes). We also found evidence for selection against introgression of genes that may contribute to cytonuclear incompatibility, consistent with previously observed biased patterns of nuclear and mitochondrial alleles suggestive of partial reproductive isolation due to cytonuclear incompatibilities. Our results provide a genome‐scale perspective on the relationships between divergence and introgression in secondary contact that is relevant for understanding the roles of selection in maintaining partial isolation of lineages, causing admixing lineages to not completely homogenize.     

Discordant divergence times among Z-chromosome regions between two ecologically distinct swallowtail butterfly species

We investigate multilocus patterns of differentiation between parental populations of two swallowtail butterfly species that differ at a number of ecologically important sex-linked traits. Using a new coalescent-based approach, we show that there is significant heterogeneity in estimated divergence times among five Z-linked markers, rejecting a purely allopatric speciation model. We infer that the Z chromosome is a mosaic of regions that differ in the extent of historical gene flow, potentially due to isolating barriers that prevent the introgression of species-specific traits that result in hybrid incompatibilities. Surprisingly, a candidate region for a strong barrier to introgression, Ldh, does not show a significantly deeper divergence time than other markers on the Z chromosome. Our approach can be used to test alternative models of speciation and can potentially assign chronological order to the appearance of factors contributing to reproductive isolation between species.     

Multiple forms of selection shape reproductive isolation in a primate hybrid zone

Speciation occurs when populations diverge and become reproductively isolated from each other. Natural selection is commonly accepted to play a large role in this process, and it has been widely assumed that reproductive isolation often results as a by‐product of divergence driven by adaptation in allopatry. When such populations come into secondary contact, reinforcement can act to strengthen reproductive isolation, but the frequency and importance of this process are still unknown. Here, we explored genomic signatures of selection in allopatry and sympatry for loci associated with reproductive isolation using a natural primate hybrid zone. By analysing reduced‐representation sequencing data, we quantified admixture and population structure across a howler monkey hybrid zone and examined the relationship between locus‐specific differentiation and introgression. We detected extensive admixture that was mostly limited to the narrow contact zone. Loci with reduced introgression into the heterospecific genomic background (the pattern expected for loci associated with reproductive isolation due to selection against hybrids) were significantly more differentiated between allopatric parental populations than loci with neutral and increased introgression, supporting the hypothesis that reproductive isolation is a by‐product of divergence in allopatry. Further, loci with reduced introgression showed greater differentiation in sympatry than in allopatry, suggesting a role for reinforcement. Thus, our results reflect multiple forms of selection that have shaped reproductive isolation in this system. We conclude that reproductive isolation may have initially been driven by divergence in allopatry, but later reinforced by divergent selection in sympatry.     

When the Rule Becomes the Exception. No Evidence of Gene Flow between Two Zerynthia Cryptic Butterflies Suggests the Emergence of a New Model Group

There is increasing evidence that most parapatric cryptic/sister taxa are reproductively compatible across their areas of contact. Consequently, the biological species concept, which assumes absence of interbreeding, is becoming a not so effective criterion in evolutionary ecology. Nevertheless, the few parapatric sister taxa showing complete reproductive barriers represent interesting models to study speciation processes and the evolution of reproductive isolation. In this study, we examined contact populations in northwestern Italy of two butterfly species, Zerynthia polyxena and Z. cassandra, characterized by different genitalic morphotypes. We studied levels of divergence among 21 populations distributed from Sicily to France using three genetic markers (the mitochondrial COI and ND1 genes and the nuclear wingless gene) and genitalic geometric morphometrics. Moreover, we performed species distribution modelling to estimate different climatic requirements of Z. polyxena and Z. cassandra. We projected climatic data into glacial maximum scenarios in order to verify if and to which extent glacial cycles could have contributed to speciation processes. Genetic and morphometric analyses identified two main groups. All specimens showed a concordant pattern of diversification, including those individuals sampled in the contact area. Haplotype distribution and climatic models showed that during glacial maxima both species experienced a strong range contraction and presumably remained separated into different microrefugia in southern France, in the Italian Peninsula and on the islands of Elba and Sicily. Long term separation was probably favoured by reduced dispersal ability and high phylopatry, while genitalic diversification probably favoured interbreeding avoidance. Conversely, the aposematic wing pattern remained almost identical. We compared our results with those obtained in other species and concluded that Z. polyxena and Z. cassandra represent a valuable model in the study of speciation.     

Sperm performance in conspecific and heterospecific female fluid

Divergent sexual selection within allopatric populations may result in divergent sexual phenotypes, which can act as reproductive barriers between populations upon secondary contact. This hypothesis has been most tested on traits involved in precopulatory sexual selection, with less work focusing on traits that act after copulation and before fertilization (i.e., postcopulatory prezygotic traits), particularly in internally fertilizing vertebrates. However, postcopulatory sexual selection within species can also drive trait divergence, resulting in reduced performance of heterospecific sperm within the female reproductive tract. Such incompatibilities, arising as a by‐product of divergent postcopulatory sexual selection in allopatry, can represent reproductive barriers, analogous to species‐assortative mating preferences. Here, we tested for postcopulatory prezygotic reproductive barriers between three pairs of taxa with diverged sperm phenotypes and moderate‐to‐high opportunity for postcopulatory sexual selection (barn swallows Hirundo rustica versus sand martins Riparia riparia, two subspecies of bluethroats, Luscinia svecica svecica versus L. s. namnetum, and great tits Parus major versus blue tits Cyanistes caeruleus). We tested sperm swimming performance in fluid from the outer reproductive tract of females, because the greatest reduction in sperm number in birds occurs as sperm swim across the vagina. Contrary to our expectations, sperm swam equally well in fluid from conspecific and heterospecific females, suggesting that postcopulatory prezygotic barriers do not act between these taxon pairs, at this stage between copulation and fertilization. We therefore suggest that divergence in sperm phenotypes in allopatry is insufficient to cause widespread postcopulatory prezygotic barriers in the form of impaired sperm swimming performance in passerine birds.     

Contrasting patterns of polymorphism and divergence on the Z chromosome and autosomes in two Ficedula flycatcher species

In geographic areas where pied and collared flycatchers (Ficedula hypoleuca and F. albicollis) breed in sympatry, hybridization occurs, leading to gene flow (introgression) between the two recently diverged species. Notably, while such introgression is observable at autosomal loci it is apparently absent at the Z chromosome, suggesting an important role for genes on the Z chromosome in creating reproductive isolation during speciation. To further understand the role of Z-linked loci in the formation of new species, we studied genetic variation of the two species from regions where they live in allopatry. We analyzed patterns of polymorphism and divergence in introns from 9 Z-linked and 23 autosomal genes in pied and collared flycatcher males. Average variation on the Z chromosome is greatly reduced compared to neutral expectations based on autosomal diversity in both species. We also observe significant heterogeneity between patterns of polymorphism and divergence at Z-linked loci and a relative absence of polymorphisms that are shared by the two species on the Z chromosome compared to the autosomes. We suggest that these observations may indicate the action of recurrent selective sweeps on the Z chromosome during the evolution of the two species, which may be caused by sexual selection acting on Z-linked genes. Alternatively, reduced variation on the Z chromosome could result from substantially higher levels of introgression at autosomal than at Z-linked loci or from a complex demographic history, such as a population bottleneck.     

Adaptive introgression of the beta-globin cluster in two Andean waterfowl

Introgression of beneficial alleles has emerged as an important avenue for genetic adaptation in both plant and animal populations. In vertebrates, adaptation to hypoxic high-altitude environments involves the coordination of multiple molecular and cellular mechanisms, including selection on the hypoxia-inducible factor (HIF) pathway and the blood-O₂ transport protein hemoglobin (Hb). In two Andean duck species, a striking DNA sequence similarity reflecting identity by descent is present across the ~20 kb β-globin cluster including both embryonic (HBE) and adult (HBB) paralogs, though it was yet untested whether this is due to independent parallel evolution or adaptive introgression. In this study, we find that identical amino acid substitutions in the β-globin cluster that increase Hb-O₂ affinity have likely resulted from historical interbreeding between high-altitude populations of two different distantly-related species. We examined the direction of introgression and discovered that the species with a deeper mtDNA divergence that colonized high altitude earlier in history (Anas flavirostris) transferred adaptive genetic variation to the species with a shallower divergence (A. georgica) that likely colonized high altitude more recently possibly following a range shift into a novel environment. As a consequence, the species that received these β-globin variants through hybridization might have adapted to hypoxic conditions in the high-altitude environment more quickly through acquiring beneficial alleles from the standing, hybrid-origin variation, leading to faster evolution.Subject terms: Evolutionary genetics, Evolutionary biology     

Evidence for spatial clines and mixed geographic modes of speciation for North American cherry‐infesting Rhagoletis (Diptera: Tephritidae) flies

An important criterion for understanding speciation is the geographic context of population divergence. Three major modes of allopatric, parapatric, and sympatric speciation define the extent of spatial overlap and gene flow between diverging populations. However, mixed modes of speciation are also possible, whereby populations experience periods of allopatry, parapatry, and/or sympatry at different times as they diverge. Here, we report clinal patterns of variation for 21 nuclear‐encoded microsatellites and a wing spot phenotype for cherry‐infesting Rhagoletis (Diptera: Tephritidae) across North America consistent with these flies having initially diverged in parapatry followed by a period of allopatric differentiation in the early Holocene. However, mitochondrial DNA (mtDNA) displays a different pattern; cherry flies at the ends of the clines in the eastern USA and Pacific Northwest share identical haplotypes, while centrally located populations in the southwestern USA and Mexico possess a different haplotype. We hypothesize that the mitochondrial difference could be due to lineage sorting but more likely reflects a selective sweep of a favorable mtDNA variant or the spread of an endosymbiont. The estimated divergence time for mtDNA suggests possible past allopatry, secondary contact, and subsequent isolation between USA and Mexican fly populations initiated before the Wisconsin glaciation. Thus, the current genetics of cherry flies may involve different mixed modes of divergence occurring in different portions of the fly''s range. We discuss the need for additional DNA sequencing and quantification of prezygotic and postzygotic reproductive isolation to verify the multiple mixed‐mode hypothesis for cherry flies and draw parallels from other systems to assess the generality that speciation may commonly involve complex biogeographies of varying combinations of allopatric, parapatric, and sympatric divergence.     

Hybrid speciation in sparrows II: a role for sex chromosomes?

Homoploid hybrid speciation in animals is poorly understood, mainly because of the scarcity of well‐documented cases. Here, we present the results of a multilocus sequence analysis on the house sparrow (Passer domesticus), Spanish sparrow (P. hispaniolensis) and their proposed hybrid descendant, the Italian sparrow (P. italiae). The Italian sparrow is shown to be genetically intermediate between the house sparrow and Spanish sparrow, exhibiting genealogical discordance and a mosaic pattern of alleles derived from either of the putative parental species. The average variation on the Z chromosome was significantly reduced compared with autosomal variation in the putative parental species, the house sparrow and Spanish sparrow. Additionally, divergence between the two species was elevated on the Z chromosome relative to the autosomes. This pattern of variation and divergence is consistent with reduced introgression of Z‐linked genes and/or a faster‐Z effect (increased rate of adaptive divergence on the Z). F_ST‐outlier tests were consistent with the faster‐Z hypothesis: two of five Z‐linked loci (CHD1Z and PLAA) were identified as candidates for being subject to positive, divergent selection in the putative parental species. Interestingly, the two latter genes showed a mosaic pattern in the (hybrid) Italian sparrow; that is, the Italian sparrow was found to be fixed for Spanish sparrow alleles at CHD1Z and to mainly have house sparrow alleles at PLAA. Preliminary evidence presented in this study thus suggests that sex chromosomes may play a significant role in this case of homoploid hybrid speciation.     

Inference for epidemic models with time‐varying infection rates: Tracking the dynamics of oak processionary moth in the UK

1. Invasive pests pose a great threat to forest, woodland, and urban tree ecosystems. The oak processionary moth (OPM) is a destructive pest of oak trees, first reported in the UK in 2006. Despite great efforts to contain the outbreak within the original infested area of South‐East England, OPM continues to spread.
2. Here, we analyze data consisting of the numbers of OPM nests removed each year from two parks in London between 2013 and 2020. Using a state‐of‐the‐art Bayesian inference scheme, we estimate the parameters for a stochastic compartmental SIR (susceptible, infested, and removed) model with a time‐varying infestation rate to describe the spread of OPM.
3. We find that the infestation rate and subsequent basic reproduction number have remained constant since 2013 (with R0 between one and two). This shows further controls must be taken to reduce R0 below one and stop the advance of OPM into other areas of England.
4. Synthesis. Our findings demonstrate the applicability of the SIR model to describing OPM spread and show that further controls are needed to reduce the infestation rate. The proposed statistical methodology is a powerful tool to explore the nature of a time‐varying infestation rate, applicable to other partially observed time series epidemic data.

     

A genetic legacy from archaic Homo

The roles of fossil human populations in the origin of modern humans have been enigmatic. Earlier (archaic) human populations were biologically similar and were in recurrent temporal and geographic contact, making interbreeding between ancient populations likely. Regardless of the taxonomic status of these populations, adaptive alleles may have introgressed from archaic populations into modern humans. When an introgressed archaic allele has a selective advantage, even rare interbreeding can lead to its spread or fixation in later human populations. Several genetic loci are candidates for such introgression, including microcephalin, a gene influencing brain development. This example may suggest that the evolution of human cognition depended in part on the genetic legacy of archaic groups such as the Neanderthals.     

Strong isolation by distance among local populations of an endangered butterfly species (Euphydryas aurinia)

The marsh fritillary (Euphydryas aurinia) is a critically endangered butterfly species in Denmark known to be particularly vulnerable to habitat fragmentation due to its poor dispersal capacity. We identified and genotyped 318 novel SNP loci across 273 individuals obtained from 10 small and fragmented populations in Denmark using a genotyping‐by‐sequencing (GBS) approach to investigate its population genetic structure. Our results showed clear genetic substructuring and highly significant population differentiation based on genetic divergence (F _ST) among the 10 populations. The populations clustered in three overall clusters, and due to further substructuring among these, it was possible to clearly distinguish six clusters in total. We found highly significant deviations from Hardy–Weinberg equilibrium due to heterozygote deficiency within every population investigated, which indicates substructuring and/or inbreeding (due to mating among closely related individuals). The stringent filtering procedure that we have applied to our genotype quality could have overestimated the heterozygote deficiency and the degree of substructuring of our clusters but is allowing relative comparisons of the genetic parameters among clusters. Genetic divergence increased significantly with geographic distance, suggesting limited gene flow at spatial scales comparable to the dispersal distance of individual butterflies and strong isolation by distance. Altogether, our results clearly indicate that the marsh fritillary populations are genetically isolated. Further, our results highlight that the relevant spatial scale for conservation of rare, low mobile species may be smaller than previously anticipated.     

Patch utilization and flower visitations by wild bees in a honey bee‐dominated,grassland landscape

Understanding habitat needs and patch utilization of wild and managed bees has been identified as a national research priority in the United States. We used occupancy models to investigate patterns of bee use across 1030 transects spanning a gradient of floral resource abundance and richness and distance from apiaries in the Prairie Pothole Region (PPR) of the United States. Estimates of transect use by honey bees were nearly 1.0 during our 3.5‐month sampling period, suggesting honey bees were nearly ubiquitous across transects. Wild bees more frequently used transects with higher flower richness and more abundant flowers; however, the effect size of the native flower abundance covariate (β^native = 3.90 ± 0.65 [1SE]) was four times greater than the non‐native flower covariate (β^non‐native = 0.99 ± 0.17). We found some evidence that wild bee use was lower at transects near commercial apiaries, but the effect size was imprecise (β^distance = 1.4 ± 0.81). Honey bees were more frequently detected during sampling events with more non‐native flowers and higher species richness but showed an uncertain relationship with native flower abundance. Of the 4039 honey bee and flower interactions, 85% occurred on non‐native flowers, while only 43% of the 738 wild bee observations occurred on non‐native flowers. Our study suggests wild bees and honey bees routinely use the same resource patches in the PPR but often visit different flowering plants. The greatest potential for resource overlap between honey bees and wild bees appears to be for non‐native flowers in the PPR. Our results are valuable to natural resource managers tasked with supporting habitat for managed and wild pollinators in agroecosystems.     

Combining stereo‐video monitoring and physiological trials to estimate reef fish metabolic demands in the wild

Organismal metabolic rates (MRs) are the basis of energy and nutrient fluxes through ecosystems. In the marine realm, fishes are some of the most prominent consumers. However, their metabolic demand in the wild (field MR [FMR]) is poorly documented, because it is challenging to measure directly. Here, we introduce a novel approach to estimating the component of FMR associated with voluntary activity (i.e., the field active MR [AMRfield]). Our approach combines laboratory‐based respirometry, swimming speeds, and field‐based stereo‐video systems to estimate the activity of individuals. We exemplify our approach by focusing on six coral reef fish species, for which we quantified standard MR and maximum MR (SMR and MMR, respectively) in the laboratory, and body sizes and swimming speeds in the field. Based on the relationships between MR, body size, and swimming speeds, we estimate that the activity scope (i.e., the ratio between AMRfield and SMR) varies from 1.2 to 3.2 across species and body sizes. Furthermore, we illustrate that the scaling exponent for AMRfield varies across species and can substantially exceed the widely assumed value of 0.75 for SMR. Finally, by scaling organismal AMRfield estimates to the assemblage level, we show the potential effect of this variability on community metabolic demand. Our approach may improve our ability to estimate elemental fluxes mediated by a critically important group of aquatic animals through a non‐destructive, widely applicable technique.     

Zea systematics: ribosomal ITS evidence

Ribosomal internal transcribed spacer (ITS) sequences were used to evaluate the phylogenetics of Zea and Tripsacum. Maximum likelihood and polymorphism parsimony were used for phylogenetic reconstructions. Zea ITS nucleotide diversity was high compared to other plant species, but approximately equivalent to other maize loci. Coalescence of ITS alleles was rapid relative to other nuclear loci; however, there was still much diversity within populations. Zea and Tripsacum form a clade clearly differentiated from all other Poaceae. Four Zea ITS pseudogenes were identified by phylogenetic position and nucleotide composition. The phylogenetic position of Z. mays ssp. huehuetenangensis was clearly established as basal to the other Z. mays. The ITS phylogeny disfavored a Z. luxurians and Z. diploperennis clade, which conflicted with some previous studies. The introgression of Z. mays alleles into Z. perennis and Z. diploperennis was also established. The ITS data indicated a near contemporary divergence of domesticated maize and its two closest wild relatives.      

A recombination suppressor contributes to ecological speciation in OSTRINIA moths

Despite unparalleled access to species'' genomes in our post-genomic age, we often lack adequate biological explanations for a major hallmark of the speciation process—genetic divergence. In the presence of gene flow, chromosomal rearrangements such as inversions are thought to promote divergence and facilitate speciation by suppressing recombination. Using a combination of genetic crosses, phenotyping of a trait underlying ecological isolation, and population genetic analysis of wild populations, we set out to determine whether evidence supports a role for recombination suppressors during speciation between the Z and E strains of European corn borer moth (Ostrinia nubilalis). Our results are consistent with the presence of an inversion that has contributed to accumulation of ecologically adaptive alleles and genetic differentiation across roughly 20% of the Ostrinia sex chromosome (~4 Mb). Patterns in Ostrinia suggest that chromosomal divergence may involve two separate phases—one driving its transient origin through local adaptation and one determining its stable persistence through differential introgression. As the evolutionary rate of rearrangements in lepidopteran genomes appears to be one of the fastest among eukaryotes, structural mutations may have had a disproportionate role during adaptive divergence and speciation in Ostrinia and in other moths and butterflies.     

Molecular and iridescent feather reflectance data reveal recent genetic diversification and phenotypic differentiation in a cloud forest hummingbird

The present day distribution and spatial genetic diversity of Mesoamerican biota reflects a long history of responses to habitat change. The hummingbird Lampornis amethystinus is distributed in northern Mesoamerica, with geographically disjunct populations. Based on sampling across the species range using mitochondrial DNA (mtDNA) sequences and nuclear microsatellites jointly analysed with phenotypic and climatic data, we (1) test whether the fragmented distribution is correlated with main evolutionary lineages, (2) assess body size and plumage color differentiation of populations in geographic isolation, and (3) evaluate a set of divergence scenarios and demographic patterns of the hummingbird populations. Analysis of genetic variation revealed four main groups: blue‐throated populations (Sierra Madre del Sur); two groups of amethyst‐throated populations (Trans‐Mexican Volcanic Belt and Sierra Madre Oriental); and populations east of the Isthmus of Tehuantepec (IT) with males showing an amethyst throat. The most basal split is estimated to have originated in the Pleistocene, 2.39–0.57 million years ago (MYA), and corresponded to groups of populations separated by the IT. However, the estimated recent divergence time between blue‐ and amethyst‐throated populations does not correspond to the 2‐MY needed to be in isolation for substantial plumage divergence, likely because structurally iridescent colors are more malleable than others. Results of species distribution modeling and Approximate Bayesian Computation analysis fit a model of lineage divergence west of the Isthmus after the Last Glacial Maximum (LGM), and that the species’ suitable habitat was disjunct during past and current conditions. These results challenge the generality of the contraction/expansion glacial model to cloud forest‐interior species and urges management of cloud forest, a highly vulnerable ecosystem to climate change and currently facing destruction, to prevent further loss of genetic diversity or extinction.     

Differential introgression causes genealogical discordance in host races of Acrocercops transecta (Insecta: Lepidoptera)

Recently diverged populations often exhibit incomplete reproductive isolation, with a low level of gene flow continuing between populations. Previous studies have shown that, even under a low level of gene flow, genetic divergence between populations can proceed at the loci governing local adaptation and reproductive isolation but not at other neutral loci. A leaf‐mining moth, Acrocercops transecta, consists of Juglans‐ and Lyonia‐associated host races. The two host races differ in host preferences of ovipositing females and in larval adaptation to host plants but mate readily in the laboratory, producing fertile hybrids. The Juglans and Lyonia races are often sympatric in the wild, implying that gene introgression could occur in nature between the two host races. We tested this hypothesis by combining phylogenetic analyses with coalescent simulations, focusing on mitochondrial genes (COI and ND5) and the nuclear Tpi, Per and Ldh genes located on the Z‐chromosome. The mitochondrial genes clearly distinguished the Lyonia race from the Juglnas race, whereas the Tpi, Per and Ldh genealogies did not reflect the two host races. Coalescent simulations indicated gene flow at the three Z‐linked genes in both directions, whereas there was no introgression in the mitochondrial genes. The lack of introgression in mitochondrial genes suggests that female host preference is the primary force leading to the bifurcation of maternally inherited loci. Thus, the results show that a low level of gene flow coupled with the inflexible female host preference differentiates histories of divergence between maternally and biparentally inherited genes in this host race system.     

Dominance of Deleterious Alleles Controls the Response to a Population Bottleneck

Population bottlenecks followed by re-expansions have been common throughout history of many populations. The response of alleles under selection to such demographic perturbations has been a subject of great interest in population genetics. On the basis of theoretical analysis and computer simulations, we suggest that this response qualitatively depends on dominance. The number of dominant or additive deleterious alleles per haploid genome is expected to be slightly increased following the bottleneck and re-expansion. In contrast, the number of completely or partially recessive alleles should be sharply reduced. Changes of population size expose differences between recessive and additive selection, potentially providing insight into the prevalence of dominance in natural populations. Specifically, we use a simple statistic, BR≡∑xipop1/∑xjpop2, where x _i represents the derived allele frequency, to compare the number of mutations in different populations, and detail its functional dependence on the strength of selection and the intensity of the population bottleneck. We also provide empirical evidence showing that gene sets associated with autosomal recessive disease in humans may have a B _R indicative of recessive selection. Together, these theoretical predictions and empirical observations show that complex demographic history may facilitate rather than impede inference of parameters of natural selection.     

Divergence maintained by climatic selection despite recurrent gene flow: a case study of Castanopsis carlesii (Fagaceae)

Local adaptation to different environments has the potential to maintain divergence between populations despite recurrent gene flow and is an important driver for generating biological diversity. In this study, we investigate the role of adaptation in the maintenance of two parapatric varieties of a forest tree. We used sequence variation of chloroplastic DNA and restriction site‐associated DNA to investigate the genetic structure of two varieties of Castanopsis carlesii in subtropical China and relate it to climatic variation. We used niche reconstruction methods to investigate niche differentiation between the two varieties and to estimate the past distribution of this species. A deep divergence was observed between the two varieties, but evidence of introgression and genetic admixture was detected in two phenotypically and geographically intermediate populations. Niche reconstruction suggests that the distribution of the two varieties was disjunct during periods of global cooling and that the two varieties occupy significantly different niches. The genetic structure was mainly driven by environmental factors, and 13 outlier loci under divergent selection were correlated with climatic variation. These results suggest that the two varieties evolved in allopatry and came back into secondary contact after the last glacial maximum and that they are an evolutionary example of divergence maintained by climatic selection despite recurrent gene flow.