Genetic isolation in an endemic African habitat specialist

The Chestnut‐banded Plover Charadrius pallidus is a Near‐Threatened shorebird species endemic to mainland Africa. We examined levels of genetic differentiation between its two morphologically and geographically distinct subspecies, C. p. pallidus in southern Africa (population size 11 000–16 000) and C. p. venustus in eastern Africa (population size 6500). In contrast to other plover species that maintain genetic connectivity over thousands of kilometres across continental Africa, we found profound genetic differences between remote sampling sites. Phylogenetic network analysis based on four nuclear and two mitochondrial gene regions, and population genetic structure analyses based on 11 microsatellite loci, indicated strong genetic divergence, with 2.36% mitochondrial sequence divergence between individuals sampled in Namibia (southern Africa) and those of Kenya and Tanzania (eastern Africa). This distinction between southern and eastern African populations was also supported by highly distinct genetic clusters based on microsatellite markers (global F_ST = 0.309,  = 0.510, D = 0.182). Behavioural factors that may promote genetic differentiation in this species include habitat specialization, monogamous mating behaviour and sedentariness. Reliance on an extremely small number of saline lakes for breeding and limited dispersal between populations are likely to promote reproductive and genetic isolation between eastern and southern Africa. We suggest that the two Chestnut‐banded Plover subspecies may warrant elevation to full species status. To assess this distinction fully, additional sample collection will be needed, with analysis of genetic and phenotypic traits from across the species’ entire breeding range.     

What haplodiploids can teach us about hybridization and speciation

Most evolutionary theory focuses on species that reproduce through sexual reproduction where both sexes have a diploid chromosome count. Yet a substantial proportion of multicellular species display complex life cycles, with both haploid and diploid life stages. A classic example is haplodiploidy, where females develop from fertilized eggs and are diploid, while males develop from unfertilized eggs and are haploid. Although haplodiploids make up about 15% of all animals (de la Filia et al. 2015 ), this type of reproduction is rarely considered in evolutionary theory. In this issue of Molecular Ecology, Patten et al. ( 2015 ) develop a theoretical model to compare the rate of nuclear and mitochondrial introgression in haplodiploid and diploid species. They show that when two haplodiploid species hybridize, nuclear genes are much less likely to cross the species barrier than if both species were to be diploids. The reason for this is that only half of the offspring resulting from matings between haplodiploid species are true hybrids: sons from such mating only inherit their mother genes and therefore only contain genes of the maternal species. Truly, hybrid males can only occur through backcrossing of a hybrid female to a male of one of the parental species. While this twist of haplodiploid transmission genetics limits nuclear introgression, mitochondrial genes, which are maternally inherited, are unaffected by the scarcity of hybrid males. In other words, the rate of mitochondrial introgression is the same for haplodiploid and diploid species. As a result, haplodiploid species on average show a bias of mitochondrial compared to nuclear introgression.     

Testing models of speciation from genome sequences: divergence and asymmetric admixture in Island South‐East Asian Sus species during the Plio‐Pleistocene climatic fluctuations

In many temperate regions, ice ages promoted range contractions into refugia resulting in divergence (and potentially speciation), while warmer periods led to range expansions and hybridization. However, the impact these climatic oscillations had in many parts of the tropics remains elusive. Here, we investigate this issue using genome sequences of three pig (Sus) species, two of which are found on islands of the Sunda‐shelf shallow seas in Island South‐East Asia (ISEA). A previous study revealed signatures of interspecific admixture between these Sus species (Genome biology, 14 , 2013, R107). However, the timing, directionality and extent of this admixture remain unknown. Here, we use a likelihood‐based model comparison to more finely resolve this admixture history and test whether it was mediated by humans or occurred naturally. Our analyses suggest that interspecific admixture between Sunda‐shelf species was most likely asymmetric and occurred long before the arrival of humans in the region. More precisely, we show that these species diverged during the late Pliocene but around 23% of their genomes have been affected by admixture during the later Pleistocene climatic transition. In addition, we show that our method provides a significant improvement over D‐statistics which are uninformative about the direction of admixture.     

Refugial isolation and secondary contact in the dyeing poison frog Dendrobates tinctorius

Recent palaeoclimactic research suggests that fluctuating environmental conditions throughout the Pleistocene of Amazonia occurred with previously unrecognized frequency. This has resulted in a theoretical shift from glacially influenced fluctuations to those driven by precessional rhythms. This theoretical revolution has a profound impact on expectations of biotic diversity within biogeographical regions that have long been based on the idea of large-scale landscape fragmentation associated with increased aridity and glacial cycles. Generally speaking, this shifts phylogeographical expectations from that of (i) large areas of sympatry of closely related (but not sister) species whose origins lie in separate refugia, and current distributions are the results of cyclic connectivity of those two refugia (refuge hypothesis), to that of (ii) fine scale genetic structure, often associated with elevation, and divergence well below expected speciation levels [disturbance-vicariance (DV) hypothesis]. To date there have been few tests of the expectations of the DV hypothesis based on empirical studies of Neotropical floral and faunal communities. Herein we examine phylogeographical structure of Dendrobates tinctorius, an amphibian species endemic to the uplands of the eastern Guiana Shield, based on sampling of 114 individuals from 24 localities. Phylogenetic, nested clade, and dispersal-vicariance (DIVA) analyses of cytochrome b sequence data reveal the presence of two mitochondrial lineages that are associated with previously identified western and eastern uplands of this area. The geographical distribution of mitochondrial haplotypes and the results of DIVA and coalescent analyses suggest that there has been extensive secondary contact between these lineages indicating a complex history of connectivity between these western and eastern highlands, supporting the predictions of the DV hypothesis.     

Cryptic speciation along a bathymetric gradient

The deep ocean supports a highly diverse and mostly endemic fauna, yet little is known about how or where new species form in this remote ecosystem. How speciation occurs is especially intriguing in the deep sea because few obvious barriers exist that would disrupt gene flow. Geographic and bathymetric patterns of genetic variation can provide key insights into how and where new species form. We quantified the population genetic structure of a protobranch bivalve, Neilonella salicensis, along a depth gradient (2200–3800 m) in the western North Atlantic using both nuclear (28S and calmodulin intron) and mitochondrial (cytochrome c oxidase subunit I) loci. A sharp genetic break occurred for each locus between populations above 2800 m and below 3200 m, defining two distinct clades with no nuclear or mitochondrial haplotypes shared between depth regimes. Bayesian phylogenetic analyses provided strong support for two clades, separated by depth, within N. salicensis. Although no morphological divergence was apparent, we suggest that the depth‐related population genetic and phylogenetic divergence is indicative of a cryptic species. The frequent occurrence of various stages of divergence associated with species formation along bathymetric gradients suggests that depth, and the environmental gradients that attend changes in depth, probably play a fundamental role in the diversification of marine organisms, especially in deep water. © 2014 The Linnean Society of London, Biological Journal of the Linnean Society, 2014, 113 , 897–913.     

Population structure and speciation in the genus Tursiops based on microsatellite and mitochondrial DNA analyses

Bottlenose dolphins (Tursiops truncatus) have a world-wide distribution, and show morphotypic variation among regions. Distinctions between coastal and pelagic populations have been documented; however, regional patterns of differentiation had not been previously investigated in a wider geographic context. We analysed up to nine different populations from seven different areas of the world by mitochondrial DNA and microsatellite DNA markers, and found differentiation among all putative regional populations. Both mtDNA and microsatellite DNA data show significant differentiation, suggesting restricted gene flow for both males and females. Dolphins in coastal habitat showed less variability and were in most cases differentiated from a pelagic lineage, which could suggest local founder events in some cases. Two coastal populations recently classified as belonging to a new species, T. aduncus, were each highly differentiated from populations of the truncatus morphotype, and from each other, suggesting a possible third species represented by the South African aduncus type.     

Molecular tools and bumble bees: revealing hidden details of ecology and evolution in a model system

Bumble bees are a longstanding model system for studies on behaviour, ecology and evolution, due to their well‐studied social lifestyle, invaluable role as wild and managed pollinators, and ubiquity and diversity across temperate ecosystems. Yet despite their importance, many aspects of bumble bee biology have remained enigmatic until the rise of the genetic and, more recently, genomic eras. Here, we review and synthesize new insights into the ecology, evolution and behaviour of bumble bees that have been gained using modern genetic and genomic techniques. Special emphasis is placed on four areas of bumble bee biology: the evolution of eusociality in this group, population‐level processes, large‐scale evolutionary relationships and patterns, and immunity and resistance to pesticides. We close with a prospective on the future of bumble bee genomics research, as this rapidly advancing field has the potential to further revolutionize our understanding of bumble bees, particularly in regard to adaptation and resilience. Worldwide, many bumble bee populations are in decline. As such, throughout the review, connections are drawn between new molecular insights into bumble bees and our understanding of the causal factors involved in their decline. Ongoing and potential applications to bumble bee management and conservation are also included to demonstrate how genetics‐ and genomics‐enabled research aids in the preservation of this threatened group.     

The expression and impact of antifungal grooming in ants

Parasites can cause extensive damage to animal societies in which many related individuals frequently interact. In response, social animals have evolved diverse individual and collective defences. Here, we measured the expression and efficiency of self-grooming and allo-grooming when workers of the ant Formica selysi were contaminated with spores of the fungal entomopathogen Metarhizium anisopliae. The amount of self-grooming increased in the presence of fungal spores, which shows that the ants are able to detect the risk of infection. In contrast, the amount of allo-grooming did not depend on fungal contamination. Workers groomed all nestmate workers that were re-introduced into their groups. The amount of allo-grooming towards noncontaminated individuals was higher when the group had been previously exposed to the pathogen. Allo-grooming decreased the number of fungal spores on the surface of contaminated workers, but did not prevent infection in the conditions tested (high dose of spores and late allo-grooming). The rate of disease transmission to groomers and other nestmates was extremely low. The systematic allo-grooming of all individuals returning to the colony, be they contaminated or not, is probably a simple but robust prophylactic defence preventing the spread of fungal diseases in insect societies.     

Re-examination of a proposed case of stasipatric speciation: phylogeography of the Australian morabine grasshoppers (Vandiemenella viatica species group)

Karyotypic differences have been used for delimiting populations or species, although whether these mutations provide strong barriers to gene flow between populations and promote speciation remains contentious. In this study, we assessed whether 11 chromosomal races of Australian morabine grasshoppers ( Vandiemenella viatica species group) represent genetically distinct populations by analyses of cytological and allozyme (35 loci) data and DNA sequences of the elongation factor-1 alpha ( EF -1α), anonymous Mvia11 , and mitochondrial cytochrome c oxidase subunit I ( COI ) loci. While the Vandiemenella chromosomal taxa generally represent genetically distinct units, a substantial portion of the total genetic variation in our samples was not explained by the chromosomal variation. Mantel tests indicated that Vandiemenella populations were spatially structured and have maintained gene flow at a local scale within each of the taxa. The group was subdivided into 13 genetic clusters; four chromosomal taxa comprised single exclusive clusters, while others comprised more than one cluster or clusters shared with other taxa. Boundaries of these cryptic population subdivisions correspond with several biogeographical barriers, such as straits, gulfs, the Murray River, and an ancient mega-lake, Lake Bungunnia. The viatica species group was previously proposed to have diversified without major geographical separation based on the stasipatric speciation model; however, the present study suggests the involvement of allopatric fragmentation. Given extensive nonmonophyly of chromosomal taxa and incomplete barriers to gene flow among taxa, all Vandiemenella chromosomal taxa and genetically distinct populations within chromosomal taxa, except Vandiemenella pichirichi , should be regarded as populations of one species: Vandiemenella viatica .     

Positive selection on sociobiological traits in invasive fire ants

The fire ant Solenopsis invicta and its close relatives are highly invasive. Enhanced social cooperation may facilitate invasiveness in these and other invasive ant species. We investigated whether invasiveness in Solenopsis fire ants was accompanied by positive selection on sociobiological traits by applying a phylogenomics approach to infer ancient selection, and a population genomics approach to infer recent and ongoing selection in both native and introduced S. invicta populations. A combination of whole‐genome sequencing of 40 haploid males and reduced‐representation genomic sequencing of 112 diploid workers identified 1,758,116 and 169,682 polymorphic markers, respectively. The resulting high‐resolution maps of genomic polymorphism provide high inference power to test for positive selection. Our analyses provide evidence of positive selection on putative ion channel genes, which are implicated in neurological functions, and on vitellogenin, which is a key regulator of development and caste determination. Furthermore, molecular functions implicated in pheromonal signalling have experienced recent positive selection. Genes with signatures of positive selection were significantly more often those overexpressed in workers compared with queens and males, suggesting that worker traits are under stronger selection than queen and male traits. These results provide insights into selection pressures and ongoing adaptation in an invasive social insect and support the hypothesis that sociobiological traits are under more positive selection than nonsocial traits in such invasive species.     

Hybrid zones and the speciation continuum in Heliconius butterflies

Tropical butterflies in the genus Heliconius have long been models in the study of the stages of speciation. Heliconius are unpalatable to predators, and many species are notable for multiple geographic populations with striking warning colour pattern differences associated with Müllerian mimicry. A speciation continuum is evident in Heliconius hybrid zones. Examples range from hybrid zones across which (a) there is little genetic differentiation other than at mimicry loci, but where hybrids are common, (b) to ‘bimodal‘ hybrid zones with strong genetic divergence and few hybrids, (c) through to ‘good’ sympatric species, with hybridization extremely rare or absent. Now, in this issue of Molecular Ecology, Arias et al. ( 2012 ) have found an intermediate case in Colombian Heliconius cydno showing evidence for assortative mating and molecular differences, but where hybrids are abundant.     

Ecological speciation in phytophagous insects

Divergent natural selection has been shown to promote speciation in a wide range of taxa. For example, adaptation to different ecological environments, via divergent selection, can result in the evolution of reproductive incompatibility between populations. Phytophagous insects have been at the forefront of these investigations of 'ecological speciation' and it is clear that adaptation to different host plants can promote insect speciation. However, much remains unknown. For example, there is abundant variability in the extent to which divergent selection promotes speciation, the sources of divergent selection, the types of reproductive barriers involved, and the genetic basis of divergent adaptation. We review these factors here. Several findings emerge, including the observation that although numerous different sources of divergent selection and reproductive isolation can be involved in insect speciation, their order of evolution and relative importance are poorly understood. Another finding is that the genetic basis of host preference and performance can involve loci of major effect and opposing dominance, factors which might facilitate speciation in the face of gene flow. In addition, we raise a number of other recent issues relating to phytophagous insect speciation, such as alternatives to ecological speciation, the geography of speciation, and the molecular signatures of speciation. Throughout, we aim to both synthesize what is known, as well as highlight areas where future work is especially needed.     

The genetic basis of evolution, adaptation and speciation

A primary question in biology concerns the genetic basis of the evolution of novel traits, often in response to environmental changes, and how this can subsequently cause species isolation. This topic was the focus of the symposium on the Genetics of Speciation and Evolution at the annual meeting of the Canadian Society for Ecology and Evolution, held in Banff in May 2011. The presentations revealed some of the rapid advances being made in understanding the genetic basis of adaptation and speciation, as well as the elegant interplay between an organism's genetic complement and the environment that organism experiences.     

Individual-based analysis opens new insights into understanding population structure and animal behaviour

Studying the movement of individuals in the wild has always been a challenge in ecology. However, estimating such movement is essential in life sciences as it is the base-line for evaluating connectivity, a major component in developing management and conservation plans. Furthermore, movement, or migration, is an essential parameter in population genetics, as it directly affects genetic differentiation. The development of highly variable markers has allowed genetic discrimination between individuals within populations and at larger scales, and the availability of high-throughput technologies means that many samples and hence many individuals can be screened. These advances mean that we can now use genetic identification for tracking individuals, and hence follow both survival and reproductive output through the life cycle. The paper by Morrissey & Ferguson (2011, this issue) is a demonstration of this new capability, as authors were able to infer the movement of salmonid fish initially captured as juveniles, and later as reproductively mature adults.     

Evolution of hybridogenetic lineages in Cataglyphis ants

In most social Hymenoptera, a diploid egg develops into either a queen or a worker depending on environmental conditions. Hybridogenetic Cataglyphis ants display a bizarre genetic system, where queen‐worker caste determination is primarily determined by genetic factors. In hybridogenetic populations, all workers are F1 hybrids of two distinct lineages, whereas new queens are nearly always pure‐lineage individuals produced by clonal reproduction. The distribution and evolutionary history of these hybridogenetic populations have not yet been thoroughly analysed. Here, we studied the phylogeographic distribution of hybridogenetic populations in two closely related Spanish species: Cataglyphis humeya and Cataglyphis velox. Hybridogenesis has been previously documented in a locality of C. velox, but whether this system occurs elsewhere within the range of the two species was yet unknown. Queens and workers from 66 localities sampled across the range of the species were genotyped at 18 microsatellite markers to determine whether queens were produced by parthenogenesis and whether workers were hybrids of divergent lineages. Populations with F1 hybrid workers were identified by combining genetic, geographical and mating assortments data. In most populations of C. velox, workers were found to be hybrids of two divergent lineages. Workers were however produced via random mating in two marginal populations of C. velox, and in all populations studied of its sister species C. humeya. High‐throughput sequencing data were obtained to confirm inferences based on microsatellites and to characterize relationships between populations. Our results revealed a complicated history of reticulate evolution that may account for the origin of hybridogenetic lineages in Cataglyphis.     

No reversion to single mating in a socially parasitic ant

Social Hymenoptera are ideal biological models for the study of the selective forces affecting the evolution of multiple mating (polyandry), because sister species can evolve different lifestyles and mating strategies. Single mating is predicted in workerless social parasites, because the key benefit of multiple mating in social insects, that is, the increase in genetic diversity among worker offspring, does not hold for workerless species. We compared the queen mating frequency between the ant Plagiolepis pygmaea and its derived social parasite P. xene. Previous studies showed that queens of the host P. pygmaea are obligately polyandrous. Here, pedigree analyses of mother–offspring combinations indicate that queens of the parasite P. xene did not revert to single mating; more than 50% of queens mated multiply, with 2–4 males. This result shows that reversal from multiple to single mating may be not selected in polyandrous social insect workerless parasites. We propose that such reversion does not occur when multiple mating is virtually cost free.     

Phylogeography of speciation: allopatric divergence and secondary contact between outcrossing and selfing Clarkia

The origins of hybrid zones between parapatric taxa have been of particular interest for understanding the evolution of reproductive isolation and the geographic context of species divergence. One challenge has been to distinguish between allopatric divergence (followed by secondary contact) versus primary intergradation (parapatric speciation) as alternative divergence histories. Here, we use complementary phylogeographic and population genetic analyses to investigate the recent divergence of two subspecies of Clarkia xantiana and the formation of a hybrid zone within the narrow region of sympatry. We tested alternative phylogeographic models of divergence using approximate Bayesian computation (ABC) and found strong support for a secondary contact model and little support for a model allowing for gene flow throughout the divergence process (i.e. primary intergradation). Two independent methods for inferring the ancestral geography of each subspecies, one based on probabilistic character state reconstructions and the other on palaeo-distribution modelling, also support a model of divergence in allopatry and range expansion leading to secondary contact. The membership of individuals to genetic clusters suggests geographic substructure within each taxon where allopatric and sympatric samples are primarily found in separate clusters. We also observed coincidence and concordance of genetic clines across three types of molecular markers, which suggests that there is a strong barrier to gene flow. Taken together, our results provide evidence for allopatric divergence followed by range expansion leading to secondary contact. The location of refugial populations and the directionality of range expansion are consistent with expectations based on climate change since the last glacial maximum. Our approach also illustrates the utility of combining phylogeographic hypothesis testing with species distribution modelling and fine-scale population genetic analyses for inferring the geography of the divergence process.     

The genomics of adaptation,divergence and speciation: a congealing theory

In this issue, Flaxman et al. ( 2014 ) report the results of sophisticated whole‐genome simulations of speciation with gene flow, enhancing our understanding of the process by building on previous single‐locus, multilocus and analytical works. Their findings provide us with new insights about how genomes can diverge and the importance of statistical and chromosomal linkage in facilitating reproductive isolation. The authors characterize the conditions under which, even with high gene flow and weak divergent selection, reproductive isolation between populations can occur due to the emergent stochastic process of genomewide congealing, where numerous statistically or physically linked loci of small effect allow selection to limit effective migration rates. The initial congealing event can occur within a broad range conditions, and once initiated, the self‐reinforcing process leads to rapid divergence and ultimately two reproductively isolated populations. Flaxman et al.'s ( 2014 ) work is a valuable contribution to our understanding of speciation with gene flow and in making a more predictive field of evolutionary genomics and speciation.     

Dobzhansky–Muller incompatibilities,dominance drive,and sex‐chromosome introgression at secondary contact zones: A simulation study

Dobzhansky–Muller (DM) incompatibilities involving sex chromosomes have been proposed to account for Haldane's rule (lowered fitness among hybrid offspring of the heterogametic sex) as well as Darwin's corollary (asymmetric fitness costs with respect to the direction of the cross). We performed simulation studies of a hybrid zone to investigate the effects of different types of DM incompatibilities on cline widths and positions of sex‐linked markers. From our simulations, X‐Y incompatibilities generate steep clines for both X‐linked and Y‐linked markers; random effects may produce strong noise in cline center positions when migration is high relative to fitness costs, but X‐ and Y‐centers always coincide strictly. X‐autosome and Y‐autosome incompatibilities also generate steep clines, but systematic shifts in cline centers occur when migration is high relative to selection, as a result of a dominance drive linked to Darwin's corollary. Interestingly, sex‐linked genes always show farther introgression than the associated autosomal genes. We discuss ways of disentangling the potentially confounding effects of sex biases in migration, we compare our results to those of a few documented contact zones, and we stress the need to study independent replicates of the same contact zone.