Recent rapid speciation and ecomorph divergence in Indo‐Australian sea snakes

The viviparous sea snakes (Hydrophiinae) are a young radiation of at least 62 species that display spectacular morphological diversity and high levels of local sympatry. To shed light on the mechanisms underlying sea snake diversification, we investigated recent speciation and eco‐morphological differentiation in a clade of four nominal species with overlapping ranges in Southeast Asia and Australia. Analyses of morphology and stomach contents identified the presence of two distinct ecomorphs: a ‘macrocephalic’ ecomorph that reaches >2 m in length, has a large head and feeds on crevice‐dwelling eels and gobies; and a ‘microcephalic’ ecomorph that rarely exceeds 1 m in length, has a small head and narrow fore‐body and hunts snake eels in burrows. Mitochondrial sequences show a lack of reciprocal monophyly between ecomorphs and among putative species. However, individual assignment based on newly developed microsatellites separated co‐distributed specimens into four significantly differentiated clusters corresponding to morphological species designations, indicating limited recent gene flow and progress towards speciation. A coalescent species tree (based on mitochondrial and nuclear sequences) and isolation‐migration model (mitochondrial and microsatellite markers) suggest between one and three transitions between ecomorphs within the last approximately 1.2 million to approximately 840 000 years. In particular, the macrocephalic ‘eastern’ population of Hydrophis cyanocinctus and microcephalic H. melanocephalus appear to have diverged very recently and rapidly, resulting in major phenotypic differences and restriction of gene flow in sympatry. These results highlight the viviparous sea snakes as a promising system for speciation studies in the marine environment.     

Deep mitochondrial introgression and hybridization among ecologically divergent vole species

The completion of speciation is typically difficult to ascertain in rapidly diverging taxa but the amount of hybridization and gene flow in sympatry or parapatry contains important information about the level of reproductive isolation achieved. Here, we examined the progress in speciation between the Mediterranean (Microtus duodecimcostatus) and the Lusitanian pine vole (M. lusitanicus), which are part of the most rapid radiation of species known in mammals. These two Iberian pine voles are classified as separate species because of differences in morphology and ecology, but relatively many ambiguous individuals can be found in sympatric conditions. Our phylogenetic analyses of rangewide data from the mitochondrial cytochrome b gene (mtDNA) demonstrated high levels of diversity and a basal separation in two parapatric lineages. However, mtDNA affiliation was at odds with morphological classification or geographical distribution of the taxa. In contrast, statistical analyses of microsatellites (nucDNA) showed two clear genetic clusters in allopatry and sympatry generally matching morphological classification. This cytonuclear discordance over a large geographic area suggests historical introgression of mtDNA from M. duodecimcostatus to M. lusitanicus. There was statistical evidence for at least two recent hybrids in the sympatry zone but gene flow is apparently low given clear‐cut differences in nucDNA. Our results indicate a relatively advanced speciation process in these Iberian pine voles without fully established reproductive isolation. This situation enables use of combined population genomic and experimental approaches for the separation of patterns and mechanisms in the ongoing explosive diversification of these and other Arvicoline rodents in the future.     

Genetic divergence between the sympatric queen morphs of the ant Myrmica rubra

Pairs of obligate social parasites and their hosts, where some of the parasites have recently diverged from their host through intraspecific social parasitism, provide intriguing systems for studying the modes and processes of speciation. Such speciation, probably in sympatry, has also been propounded in the ant Myrmica rubra and its intraspecific social parasite. In this species, parasitism is associated with queen size dimorphism, and the small microgyne has become a social parasite of the large macrogyne. Here, we investigated the genetic divergence of the host and the parasite queen morphs in 11 localities in southern Finland, using nuclear and mitochondrial markers of queens and workers. We formulated and tested four speciation‐related hypotheses that differed in the degree of genetic divergence between the morphs. The queen morphs were genetically distinct from each other with little hybridization. In the nuclear data, when localities were nested within queen morphs in the hierarchical amova , 39% of the genetic variation was explained by the queen morph (standardized F'_CT = 0.63, uncorrected F_CT = 0.39), whereas 18% was explained by the locality (F'_SC = 0.39, F_SC = 0.29). This result corroborated the hypothesis of advanced sympatric speciation. In contrast, the mitochondrial DNA could not settle between the hierarchical levels of locality and queen morph, thus substantiating equally the hypotheses of incipient and advanced sympatric speciation. Together, our results support the view that the microgynous parasite has genetically diverged from its macrogynous host to the level of a nascent species.     

Population structure of a vector‐borne plant parasite

Parasites are among the most diverse groups of life on Earth, yet complex natural histories often preclude studies of their speciation processes. The biology of parasitic plants facilitates in situ collection of data on both genetic structure and the mechanisms responsible for that structure. Here, we studied the role of mating, dispersal and establishment in host race formation of a parasitic plant. We investigated the population genetics of a vector‐borne desert mistletoe (Phoradendron californicum) across two legume host tree species (Senegalia greggii and Prosopis velutina) in the Sonoran desert using microsatellites. Consistent with host race formation, we found strong host‐associated genetic structure in sympatry, little genetic variation due to geographic site and weak isolation by distance. We hypothesize that genetic differentiation results from differences in the timing of mistletoe flowering by host species, as we found initial flowering date of individual mistletoes correlated with genetic ancestry. Hybrids with intermediate ancestry were detected genetically. Individuals likely resulting from recent, successful establishment events following dispersal between the host species were detected at frequencies similar to hybrids between host races. Therefore, barriers to gene flow between the host races may have been stronger at mating than at dispersal. We also found higher inbreeding and within‐host individual relatedness values for mistletoes on the more rare and isolated host species (S. greggii). Our study spanned spatial scales to address how interactions with both vectors and hosts influence parasitic plant structure with implications for parasite virulence evolution and speciation.     

Gene flow,divergent selection and resistance to introgression in two species of morning glories (Ipomoea)

Gene flow is thought to impede genetic divergence and speciation by homogenizing genomes. Recent theory and research suggest that sufficiently strong divergent selection can overpower gene flow, leading to loci that are highly differentiated compared to others. However, there are also alternative explanations for this pattern. Independent evidence that loci in highly differentiated regions are under divergent selection would allow these explanations to be distinguished, but such evidence is scarce. Here, we present multiple lines of evidence that many of the highly divergent SNPs in a pair of sister morning glory species, Ipomoea cordatotriloba and I. lacunosa, are the result of divergent selection in the face of gene flow. We analysed a SNP data set across the genome to assess the amount of gene flow, resistance to introgression and patterns of selection on loci resistant to introgression. We show that differentiation between the two species is much lower in sympatry than in allopatry, consistent with interspecific gene flow in sympatry. Gene flow appears to be substantially greater from I. lacunosa to I. cordatotriloba than in the reverse direction, resulting in sympatric and allopatric I. cordatotriloba being substantially more different than sympatric and allopatric I. lacunosa. Many SNPs highly differentiated in allopatry have experienced divergent selection, and, despite gene flow in sympatry, resist homogenization in sympatry. Finally, five out of eight floral and inflorescence characteristics measured exhibit asymmetric convergence in sympatry. Consistent with the pattern of gene flow, I. cordatotriloba traits become much more like those of I. lacunosa than the reverse. Our investigation reveals the complex interplay between selection and gene flow that can occur during the early stages of speciation.     

Spatial and host related genomic variation in partially sympatric cactophagous moth species

Surveys of patterns of genetic variation in natural sympatric and allopatric populations of recently diverged species are necessary to understand the processes driving intra- and interspecific diversification. The South American moths Cactoblastis cactorum, Cactoblastis doddi and Cactoblastis bucyrus are specialized in the use of cacti as host plants. These species have partially different geographic ranges and differ in patterns of host plant use. However, there are areas that overlap, particularly, in northwestern Argentina, where they are sympatric. Using a combination of genome-wide SNPs and mitochondrial data we assessed intra and interspecific genetic variation and investigated the relative roles of geography and host plants on genetic divergence. We also searched for genetic footprints of hybridization between species. We identified three well delimited species and detected signs of hybridization in the area of sympatry. Our results supported a hypothetical scenario of allopatric speciation in the generalist C. cactorum and genetic interchange during secondary geographic contact with the pair of specialists C. bucyrus and C. doddi that probably speciated sympatrically. In both cases, adaptation to new host plants probably played an important role in speciation. The results also suggested the interplay of geography and host plant use as drivers of divergence and limiting gene flow at intra and interspecific levels.     

Unexpected cryptic species diversity in the widespread coral Seriatopora hystrix masks spatial‐genetic patterns of connectivity

Mounting evidence of cryptic species in a wide range of taxa highlights the need for careful analyses of population genetic data sets to unravel within‐species diversity from potential interspecies relationships. Here, we use microsatellite loci and hierarchical clustering analysis to investigate cryptic diversity in sympatric and allopatric (separated by 450 km) populations of the widespread coral Seriatopora hystrix on the Great Barrier Reef. Structure analyses delimited unique genetic clusters that were confirmed by phylogenetic and extensive population‐level analyses. Each of four sympatric yet distinct genetic clusters detected within S. hystrix demonstrated greater genetic cohesion across regional scales than between genetic clusters within regions (<10 km). Moreover, the magnitude of genetic differentiation between different clusters (>0.620 G”_ST) was similar to the difference between S. hystrix clusters and the congener S. caliendrum (mean G”_ST 0.720). Multiple lines of evidence, including differences in habitat specificity, mitochondrial identity, Symbiodinium associations and morphology, corroborate the nuclear genetic evidence that these distinct clusters constitute different species. Hierarchical clustering analysis combined with more traditional population genetic methods provides a powerful approach for delimiting species and should be regularly applied to ensure that ecological and evolutionary patterns interpreted for single species are not confounded by the presence of cryptic species.     

Diploid hybrid origin of Ostryopsis intermedia (Betulaceae) in the Qinghai‐Tibet Plateau triggered by Quaternary climate change

Despite the well‐known effects that Quaternary climate oscillations had on shaping intraspecific diversity, their role in driving homoploid hybrid speciation is less clear. Here, we examine their importance in the putative homoploid hybrid origin and evolution of Ostryopsis intermedia, a diploid species occurring in the Qinghai‐Tibet Plateau (QTP), a biodiversity hotspot. We investigated interspecific relationships between this species and its only other congeners, O. davidiana and O. nobilis, based on four sets of nuclear and chloroplast population genetic data and tested alternative speciation hypotheses. All nuclear data distinguished the three species clearly and supported a close relationship between O. intermedia and the disjunctly distributed O. davidiana. Chloroplast DNA sequence variation identified two tentative lineages, which distinguished O. intermedia from O. davidiana; however, both were present in O. nobilis. Admixture analyses of genetic polymorphisms at 20 SSR loci and sequence variation at 11 nuclear loci and approximate Bayesian computation (ABC) tests supported the hypothesis that O. intermedia originated by homoploid hybrid speciation from O. davidiana and O. nobilis. We further estimated that O. davidiana and O. nobilis diverged 6–11 Ma, while O. intermedia originated 0.5–1.2 Ma when O. davidiana is believed to have migrated southward, contacted and hybridized with O. nobilis possibly during the largest Quaternary glaciation that occurred in this region. Our findings highlight the importance of Quaternary climate change in the QTP in causing hybrid speciation in this important biodiversity hotspot.     

Rapid sexual and genomic isolation in sympatric Drosophila without reproductive character displacement

The rapid evolution of sexual isolation in sympatry has long been associated with reinforcement (i.e., selection to avoid maladaptive hybridization). However, there are many species pairs in sympatry that have evolved rapid sexual isolation without known costs to hybridization. A major unresolved question is what evolutionary processes are involved in driving rapid speciation in such cases. Here, we focus on one such system; the Drosophila athabasca species complex, which is composed of three partially sympatric and interfertile semispecies: WN, EA, and EB. To study speciation in this species complex, we assayed sexual and genomic isolation within and between these semispecies in both sympatric and allopatric populations. First, we found no evidence of reproductive character displacement (RCD) in sympatric zones compared to distant allopatry. Instead, semispecies were virtually completely sexually isolated from each other across their entire ranges. Moreover, using spatial approaches and coalescent demographic simulations, we detected either zero or only weak heterospecific gene flow in sympatry. In contrast, within each semispecies we found only random mating and little population genetic structure, except between highly geographically distant populations. Finally, we determined that speciation in this system is at least an order of magnitude older than previously assumed, with WN diverging first, around 200K years ago, and EA and EB diverging 100K years ago. In total, these results suggest that these semispecies should be given full species status and we adopt new nomenclature: WN—D. athabasca, EA—D. mahican, and EB—D. lenape. While the lack of RCD in sympatry and interfertility do not support reinforcement, we discuss what additional evidence is needed to further decipher the mechanisms that caused rapid speciation in this species complex.     

High‐throughput sequencing and graph‐based cluster analysis facilitate microsatellite development from a highly complex genome

Despite recent advances in high‐throughput sequencing, difficulties are often encountered when developing microsatellites for species with large and complex genomes. This probably reflects the close association in many species of microsatellites with cryptic repetitive elements. We therefore developed a novel approach for isolating polymorphic microsatellites from the club‐legged grasshopper (Gomphocerus sibiricus), an emerging quantitative genetic and behavioral model system. Whole genome shotgun Illumina MiSeq sequencing was used to generate over three million 300 bp paired‐end reads, of which 67.75% were grouped into 40,548 clusters within RepeatExplorer. Annotations of the top 468 clusters, which represent 60.5% of the reads, revealed homology to satellite DNA and a variety of transposable elements. Evaluating 96 primer pairs in eight wild‐caught individuals, we found that primers mined from singleton reads were six times more likely to amplify a single polymorphic microsatellite locus than primers mined from clusters. Our study provides experimental evidence in support of the notion that microsatellites associated with repetitive elements are less likely to successfully amplify. It also reveals how advances in high‐throughput sequencing and graph‐based repetitive DNA analysis can be leveraged to isolate polymorphic microsatellites from complex genomes.     

Phylogeny and biogeography of the American live oaks (Quercus subsection Virentes): a genomic and population genetics approach

The nature and timing of evolution of niche differentiation among closely related species remains an important question in ecology and evolution. The American live oak clade, Virentes, which spans the unglaciated temperate and tropical regions of North America and Mesoamerica, provides an instructive system in which to examine speciation and niche evolution. We generated a fossil‐calibrated phylogeny of Virentes using RADseq data to estimate divergence times and used nuclear microsatellites, chloroplast sequences and an intron region of nitrate reductase (NIA‐i3) to examine genetic diversity within species, rates of gene flow among species and ancestral population size of disjunct sister species. Transitions in functional and morphological traits associated with ecological and climatic niche axes were examined across the phylogeny. We found the Virentes to be monophyletic with three subclades, including a southwest clade, a southeastern US clade and a Central American/Cuban clade. Despite high leaf morphological variation within species and transpecific chloroplast haplotypes, RADseq and nuclear SSR data showed genetic coherence of species. We estimated a crown date for Virentes of 11 Ma and implicated the formation of the Sea of Cortés in a speciation event ~5 Ma. Tree height at maturity, associated with fire tolerance, differs among the sympatric species, while freezing tolerance appears to have diverged repeatedly across the tropical–temperate divide. Sympatric species thus show evidence of ecological niche differentiation but share climatic niches, while allopatric and parapatric species conserve ecological niches, but diverge in climatic niches. The mode of speciation and/or degree of co‐occurrence may thus influence which niche axis plants diverge along.     

Microsatellite allele sizes alone are insufficient to delineate species boundaries in Symbiodinium

Symbiodinium are a diverse group of unicellular dinoflagellates that are important nutritional symbionts of reef‐building corals. Symbiodinium putative species (‘types’) are commonly identified with genetic markers, mostly nuclear and chloroplast encoded ribosomal DNA regions. Population genetic analyses using microsatellite loci have provided insights into Symbiodinium biogeography, connectivity and phenotypic plasticity, but are complicated by: (i) a lack of consensus criteria used to delineate inter‐ vs. intragenomic variation within species; and (ii) the high density of Symbiodinium in host tissues, which results in single samples comprising thousands of individuals. To address this problem, Wham & LaJeunesse (2016) present a method for identifying cryptic Symbiodinium species from microsatellite data based on correlations between allele size distributions and nongeographic genetic structure. Multilocus genotypes that potentially do not recombine in sympatry are interpreted as secondary ‘species’ to be discarded from downstream population genetic analyses. However, Symbiodinium species delineations should ideally incorporate multiple physiological, ecological and molecular criteria. This is because recombination tests may be a poor indicator of species boundaries in Symbiodinium due to their predominantly asexual mode of reproduction. Furthermore, discontinuous microsatellite allele sizes in sympatry may be explained by secondary contact between previously isolated populations and by mutations that occur in a nonstepwise manner. Limitations of using microsatellites alone to delineate species are highlighted in earlier studies that demonstrate occasional bimodal distributions of allele sizes within Symbiodinium species and considerable allele size sharing among Symbiodinium species. We outline these issues and discuss the validity of reinterpretations of our previously published microsatellite data from Symbiodinium populations on the Great Barrier Reef (Howells et al. 2013).     

A three‐way contact zone between forms of Patella rustica (Mollusca: Patellidae) in the central Mediterranean Sea

Previous studies have reported the occurrence of three differentiated mtDNA lineages within Patella rustica in the Mediterranean Sea. Two hypotheses have been proposed to explain these observations: (1) the maintenance of ancestral polymorphism within a single species; (2) the occurrence of cryptic species not identified previously. To distinguish between these hypotheses, we screened the genetic variability at nine allozyme loci, an intron from the α‐amylase gene and a mitochondrial gene for 187 individuals of P. rustica sampled from seven Mediterranean localities. Eight additional localities were screened for the last two markers to place the differentiated lineages in a clear geographic context. Our results demonstrate that the three mtDNA lineages correspond to three distinct nuclear genotype clusters and provide further details on their distribution: the cluster corresponding to the mtDNA lineage from the Atlantic and western Mediterranean extends as far as the south coast of Italy, whereas the remaining two clusters occur in sympatry in the eastern Mediterranean. One of the eastern Mediterranean clusters is highly differentiated and seems to be reproductively isolated from the codistributed form; we therefore suggest that it corresponds to a new species. The remaining two clusters are less differentiated and form a contact zone across south Italian shores. This three‐way contact zone constitutes an interesting model for the study of speciation in the marine realm. © 2010 The Linnean Society of London, Biological Journal of the Linnean Society, 2010, 100 , 154–169.     

Population genetic structure,genetic diversity,and natural history of the South American species of Nothofagus subgenus Lophozonia (Nothofagaceae) inferred from nuclear microsatellite data

The effect of glaciation on the levels and patterns of genetic variation has been well studied in the Northern Hemisphere. However, although glaciation has undoubtedly shaped the genetic structure of plants in the Southern Hemisphere, fewer studies have characterized the effect, and almost none of them using microsatellites. Particularly, complex patterns of genetic structure might be expected in areas such as the Andes, where both latitudinal and altitudinal glacial advance and retreat have molded modern plant communities. We therefore studied the population genetics of three closely related, hybridizing species of Nothofagus (N. obliqua, N. alpina, and N. glauca, all of subgenus Lophozonia; Nothofagaceae) from Chile. To estimate population genetic parameters and infer the influence of the last ice age on the spatial and genetic distribution of these species, we examined and analyzed genetic variability at seven polymorphic microsatellite DNA loci in 640 individuals from 40 populations covering most of the ranges of these species in Chile. Populations showed no significant inbreeding and exhibited relatively high levels of genetic diversity (H_E = 0.502–0.662) and slight, but significant, genetic structure (R_ST = 8.7–16.0%). However, in N. obliqua, the small amount of genetic structure was spatially organized into three well‐defined latitudinal groups. Our data may also suggest some introgression of N. alpina genes into N. obliqua in the northern populations. These results allowed us to reconstruct the influence of the last ice age on the genetic structure of these species, suggesting several centers of genetic diversity for N. obliqua and N. alpina, in agreement with the multiple refugia hypothesis.     

Plio-Pleistocene sea level and temperature fluctuations in the northwestern Pacific promoted speciation in the globally-distributed flathead mullet Mugil cephalus

Background  

The study of speciation in the marine realm is challenging because of the apparent absence of physical barriers to dispersal, which are one of the main drivers of genetic diversity. Although phylogeographic studies using mitochondrial DNA (mtDNA) information often reveal significant genetic heterogeneity within marine species, the evolutionary significance of such diversity is difficult to interpret with these markers. In the northwestern (NW) Pacific, several studies have emphasised the potential importance of sea-level regression during the most recent glaciations as a driver of genetic diversity in marine species. These studies have failed, however, to determine whether the period of isolation was long enough for divergence to attain speciation. Among these marine species, the cosmopolitan estuarine-dependent fish Mugil cephalus represents an interesting case study. Several divergent allopatric mtDNA lineages have been described in this species worldwide, and three occur in sympatry in the NW Pacific.     

Cytonuclear discordance among Southeast Asian black rats (Rattus rattus complex)

Black rats are major invasive vertebrate pests with severe ecological, economic and health impacts. Remarkably, their evolutionary history has received little attention, and there is no firm agreement on how many species should be recognized within the black rat complex. This species complex is native to India and Southeast Asia. According to current taxonomic classification, there are three taxa living in sympatry in several parts of Thailand, Cambodia and Lao People's Democratic Republic, where this study was conducted: two accepted species (Rattus tanezumi, Rattus sakeratensis) and an additional mitochondrial lineage of unclear taxonomic status referred to here as ‘Rattus R3’. We used extensive sampling, morphological data and diverse genetic markers differing in rates of evolution and parental inheritance (two mitochondrial DNA genes, one nuclear gene and eight microsatellite loci) to assess the reproductive isolation of these three taxa. Two close Asian relatives, Rattus argentiventer and Rattus exulans, were also included in the genetic analyses. Genetic analyses revealed discordance between the mitochondrial and nuclear data. Mitochondrial phylogeny studies identified three reciprocally monophyletic clades in the black rat complex. However, studies of the phylogeny of the nuclear exon interphotoreceptor retinoid‐binding protein gene and clustering and assignation analyses with eight microsatellites failed to separate R. tanezumi and R3. Morphometric analyses were consistent with nuclear data. The incongruence between mitochondrial and nuclear (and morphological) data rendered R. tanezumi/R3 paraphyletic for mitochondrial lineages with respect to R. sakeratensis. Various evolutionary processes, such as shared ancestral polymorphism and incomplete lineage sorting or hybridization with massive mitochondrial introgression between species, may account for this unusual genetic pattern in mammals.     

The genomic bases of morphological divergence and reproductive isolation driven by ecological speciation in Senecio (Asteraceae)

Ecological speciation, driven by adaptation to contrasting environments, provides an attractive opportunity to study the formation of distinct species, and the role of selection and genomic divergence in this process. Here, we focus on a particularly clear‐cut case of ecological speciation to reveal the genomic bases of reproductive isolation and morphological differences between closely related Senecio species, whose recent divergence within the last ~200 000 years was likely driven by the uplift of Mt. Etna (Sicily). These species form a hybrid zone, yet remain morphologically and ecologically distinct, despite active gene exchange. Here, we report a high‐density genetic map of the Senecio genome and map hybrid breakdown to one large and several small quantitative trait loci (QTL). Loci under diversifying selection cluster in three 5 cM regions which are characterized by a significant increase in relative (F_ST), but not absolute (d_XY), interspecific differentiation. They also correspond to some of the regions of greatest marker density, possibly corresponding to ‘cold‐spots’ of recombination, such as centromeres or chromosomal inversions. Morphological QTL for leaf and floral traits overlap these clusters. We also detected three genomic regions with significant transmission ratio distortion (TRD), possibly indicating accumulation of intrinsic genetic incompatibilities between these recently diverged species. One of the TRD regions overlapped with a cluster of high species differentiation, and another overlaps the large QTL for hybrid breakdown, indicating that divergence of these species may have occurred due to a complex interplay of ecological divergence and accumulation of intrinsic genetic incompatibilities.     

Tracking the progression of speciation: variable patterns of introgression across the genome provide insights on the species delimitation between progenitor–derivative spruces (Picea mariana × P. rubens)

The genic species concept implies that while most of the genome can be exchanged somewhat freely between species through introgression, some genomic regions remain impermeable to interspecific gene flow. Hence, interspecific differences can be maintained despite ongoing gene exchange within contact zones. This study assessed the heterogeneous patterns of introgression at gene loci across the hybrid zone of an incipient progenitor–derivative species pair, Picea mariana (black spruce) and Picea rubens (red spruce). The spruce taxa likely diverged in geographic isolation during the Pleistocene and came into secondary contact during late Holocene. A total of 300 SNPs distributed across the 12 linkage groups (LG) of black spruce were genotyped for 385 individual trees from 33 populations distributed across the allopatric zone of each species and within the zone of sympatry. An integrative framework combining three population genomic approaches was used to scan the genomes, revealing heterogeneous patterns of introgression. A total of 23 SNPs scattered over 10 LG were considered impermeable to introgression and putatively under diverging selection. These loci revealed the existence of impermeable genomic regions forming the species boundary and are thus indicative of ongoing speciation between these two genetic lineages. Another 238 SNPs reflected selectively neutral diffusion across the porous species barrier. Finally, 39 highly permeable SNPs suggested ancestral polymorphism along with balancing selection. The heterogeneous patterns of introgression across the genome indicated that the speciation process between black spruce and red spruce is young and incomplete, albeit some interspecific differences are maintained, allowing ongoing species divergence even in sympatry. The approach developed in this study can be used to track the progression of ongoing speciation processes.     

Evidence for nonallopatric speciation among closely related sympatric Heliotropium species in the Atacama Desert

The genetic structure of populations of closely related, sympatric species may hold the signature of the geographical mode of the speciation process. In fully allopatric speciation, it is expected that genetic differentiation between species is homogeneously distributed across the genome. In nonallopatric speciation, the genomes may remain undifferentiated to a large extent. In this article, we analyzed the genetic structure of five sympatric species from the plant genus Heliotropium in the Atacama Desert. We used amplified fragment length polymorphisms (AFLPs) to characterize the genetic structure of these species and evaluate their genetic differentiation as well as the number of loci subject to positive selection using divergence outlier analysis (DOA). The five species form distinguishable groups in the genetic space, with zones of overlap, indicating that they are possibly not completely isolated. Among‐species differentiation accounts for 35% of the total genetic differentiation (F_ST = 0.35), and F_ST between species pairs is positively correlated with phylogenetic distance. DOA suggests that few loci are subject to positive selection, which is in line with a scenario of nonallopatric speciation. These results support the idea that sympatric species of Heliotropium sect. Cochranea are under an ongoing speciation process, characterized by a fluctuation of population ranges in response to pulses of arid and humid periods during Quaternary times.     

Climatic drivers of leaf traits and genetic divergence in the tree Annona crassiflora: a broad spatial survey in the Brazilian savannas

The Cerrado is the largest South American savanna and encompasses substantial species diversity and environmental variation. Nevertheless, little is known regarding the influence of the environment on population divergence of Cerrado species. Here, we searched for climatic drivers of genetic (nuclear microsatellites) and leaf trait divergence in Annona crassiflora, a widespread tree in the Cerrado. The sampling encompassed all phytogeographic provinces of the continuous area of the Cerrado and included 397 individuals belonging to 21 populations. Populations showed substantial genetic and leaf trait divergence across the species' range. Our data revealed three spatially defined genetic groups (eastern, western and southern) and two morphologically distinct groups (eastern and western only). The east‐west split in both the morphological and genetic data closely mirrors previously described phylogeographic patterns of Cerrado species. Generalized linear mixed effects models and multiple regression analyses revealed several climatic factors associated with both genetic and leaf trait divergence among populations of A. crassiflora. Isolation by environment (IBE) was mainly due to temperature seasonality and precipitation of the warmest quarter. Populations that experienced lower precipitation summers and hotter winters had heavier leaves and lower specific leaf area. The southwestern area of the Cerrado had the highest genetic diversity of A. crassiflora, suggesting that this region may have been climatically stable. Overall, we demonstrate that a combination of current climate and past climatic changes have shaped the population divergence and spatial structure of A. crassiflora. However, the genetic structure of A. crassiflora reflects the biogeographic history of the species more strongly than leaf traits, which are more related to current climate.