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Recent simulation studies examining the performance of Bayesian species delimitation as implemented in the BPP program have suggested that BPP may detect population splits but not species divergences and that it tends to over-split when data of many loci are analyzed. Here, we confirm these results and provide the mathematical justifications. We point out that the distinction between population and species splits made in the protracted speciation model (PSM) has no influence on the generation of gene trees and sequence data, which explains why no method can use such data to distinguish between population splits and speciation. We suggest that the PSM is unrealistic as its mechanism for assigning species status assumes instantaneous speciation, contradicting prevailing taxonomic practice. We confirm the suggestion, based on simulation, that in the case of speciation with gene flow, Bayesian model selection as implemented in BPP tends to detect population splits when the amount of data (the number of loci) increases. We discuss the use of a recently proposed empirical genealogical divergence index (gdi) for species delimitation and illustrate that parameter estimates produced by a full likelihood analysis as implemented in BPP provide much more reliable inference under the gdi than the approximate method PHRAPL. We distinguish between Bayesian model selection and parameter estimation and suggest that the model selection approach is useful for identifying sympatric cryptic species, while the parameter estimation approach may be used to implement empirical criteria for determining species status among allopatric populations.

Costly interactions between species that arise as a by-product of ancestral similarities in communication signals are expected to persist only under specific evolutionary circumstances. Territorial aggression between species, for instance, is widely assumed to persist only when extrinsic barriers prevent niche divergence or selection in sympatry is too weak to overcome gene flow from allopatry. However, recent theoretical and comparative studies have challenged this view. Here we present a large-scale, phylogenetic analysis of the distribution and determinants of interspecific territoriality. We find that interspecific territoriality is widespread in birds and strongly associated with hybridization and resource overlap during the breeding season. Contrary to the view that territoriality only persists between species that rarely breed in the same areas or where niche divergence is constrained by habitat structure, we find that interspecific territoriality is positively associated with breeding habitat overlap and unrelated to habitat structure. Furthermore, our results provide compelling evidence that ancestral similarities in territorial signals are maintained and reinforced by selection when interspecific territoriality is adaptive. The territorial signals linked to interspecific territoriality in birds depend on the evolutionary age of interacting species, plumage at shallow (within-family) timescales, and song at deeper (between-family) timescales. Evidently, territorial interactions between species have persisted and shaped phenotypic diversity on a macroevolutionary timescale.

Pollinators influence patterns of plant speciation, and one intuitive hypothesis is that pollinators affect rates of plant diversification through their effects on pollen dispersal. By specifying mating events and pollen flow across the landscape, distinct types of pollinators may cause different opportunities for allopatric speciation. This pollen dispersal-dependent speciation hypothesis predicts that pollination mode has effects on the spatial context of mating events that scale up to impact population structure and rates of species formation. Here I consider recent comparative studies, including genetic analyses of plant mating events, population structure and comparative phylogenetic analyses, to examine evidence for this model. These studies suggest that highly mobile pollinators conduct greater gene flow within and among populations, compared to less mobile pollinators. These differences influence patterns of population structure across the landscape. However, the effects of pollination mode on speciation rates is less predictable. In some contexts, the predicted effects of pollen dispersal are outweighed by other factors that govern speciation rates. A multiscale approach to examine effects of pollination mode on plant mating system, population structure and rates of diversification is key to determining the role of pollen dispersal on plant speciation for model clades.

More than five decades ago, Ehrlich and Raven proposed a revolutionary idea–that the evolution of novel plant defense could spur adaptive radiation in plants. Despite motivating much work on plant–herbivore coevolution and defense theory, Ehrlich and Raven never proposed a mechanism for their “escape and radiate” model. Recent intriguing mechanisms proposed by Marquis et al. include sympatric divergence, pleiotropic effects of plant defense traits on reproductive isolation, and strong postzygotic isolation, but these may not be general features of herbivore-mediated speciation. An alternate view is that herbivores impose strong divergent selection on defenses in allopatric plant populations, with plant–herbivore coevolution driving local adaptation resulting in plant speciation. Building on these ideas, we propose three scenarios that consider the role of herbivores in plant speciation. These include (1) vicariance, subsequent coevolution within populations and adaptive divergence between geographically isolated populations, (2) colonization of a new habitat lacking effective herbivores followed by loss of defense and then re-evolution and coevolution of defense in response to novel herbivores, and (3) evolution of a new defense followed by range expansion, vicariance, and coevolution. We discuss the general role of coevolution in plant speciation and consider outstanding issues related to understanding: (1) the mechanisms behind cospeciation of plants and insects, (2) geographic variation in defense phenotypes, (3) how defensive traits and geography map onto plant phylogenies, and (4) the role of herbivores in driving character displacement in defense phenotypes of related species in sympatry.

Evidence is accumulating that gene flow commonly occurs between recently diverged species, despite the existence of barriers to gene flow in their genomes. However, we still know little about what regions of the genome become barriers to gene flow and how such barriers form. Here, we compare genetic differentiation across the genomes of bumblebee species living in sympatry and allopatry to reveal the potential impact of gene flow during species divergence and uncover genetic barrier loci. We first compared the genomes of the alpine bumblebee Bombus sylvicola and a previously unidentified sister species living in sympatry in the Rocky Mountains, revealing prominent islands of elevated genetic divergence in the genome that colocalize with centromeres and regions of low recombination. This same pattern is observed between the genomes of another pair of closely related species living in allopatry (B. bifarius and B. vancouverensis). Strikingly however, the genomic islands exhibit significantly elevated absolute divergence (dXY) in the sympatric, but not the allopatric, comparison indicating that they contain loci that have acted as barriers to historical gene flow in sympatry. Our results suggest that intrinsic barriers to gene flow between species may often accumulate in regions of low recombination and near centromeres through processes such as genetic hitchhiking, and that divergence in these regions is accentuated in the presence of gene flow.

Pleistocene climatic fluctuations (PCF) are frequently highlighted as important evolutionary engines that triggered cycles of biome expansion and contraction. Although there is ample evidence of the impact of PCF on biodiversity of continental biomes, the consequences in insular systems depend on the geology of the islands and the ecology of the taxa inhabiting them. The idiosyncratic aspects of insular systems are exemplified by the islands of the Sunda Shelf in Southeast Asia (Sundaland), where PCF-induced eustatic fluctuations had complex interactions with the geology of the region, resulting in high species diversity and endemism. Emergent land in Southeast Asia varied drastically with sea-level fluctuations during the Pleistocene. Climate-induced fluctuations in sea level caused temporary connections between insular and continental biodiversity hotspots in Southeast Asia. These exposed lands likely had freshwater drainage systems that extended between modern islands: the Paleoriver Hypothesis. Built upon the assumption that aquatic organisms are among the most suitable models to trace ancient river boundaries and fluctuations of landmass coverage, the present study aims to examine the evolutionary consequences of PCF on the dispersal of freshwater biodiversity in Southeast Asia. Time-calibrated phylogenies of DNA-delimited species were inferred for six species-rich freshwater fish genera in Southeast Asia (Clarias, Channa, Glyptothorax, Hemirhamphodon, Dermogenys, Nomorhamphus). The results highlight rampant cryptic diversity and the temporal localization of most speciation events during the Pleistocene, with 88% of speciation events occurring during this period. Diversification analyses indicate that sea-level-dependent diversification models poorly account for species proliferation patterns for all clades excepting Channa. Ancestral area estimations point to Borneo as the most likely origin for most lineages, with two waves of dispersal to Sumatra and Java during the last 5 myr. Speciation events are more frequently associated with boundaries of the paleoriver watersheds, with 60%, than islands boundaries, with 40%. In total, one-third of speciation events are inferred to have occurred within paleorivers on a single island, suggesting that habitat heterogeneity and factors other than allopatry between islands substantially affected diversification of Sundaland fishes. Our results suggest that species proliferation in Sundaland is not wholly reliant on Pleistocene sea-level fluctuations isolating populations on different islands.

A molecular survey of native and adventive psyllids in the central Macaronesian islands provides the first comprehensive phylogenetic assessment of the origins of the psyllid fauna of the Canary and Madeira archipelagos. We employ a maximum likelihood backbone constraint analysis to place the central Macaronesian taxa within the Psylloidea mitogenome phylogeny. The native psyllid fauna in these central Macaronesian islands results from an estimated 26 independent colonization events. Island host plants are predicted by host plants of continental relatives in nearly all cases and six plant genera have been colonized multiple times ( Chamaecytisus , Convolvulus , Olea , Pistacia , Rhamnus , and Spartocytisus ) from the continent. Post-colonization diversification varies from no further cladogenesis (18 events, represented by a single native taxon) to modest in situ diversification resulting in two to four native taxa and, surprisingly, given the diverse range of islands and habitats, only one substantial species radiation with more than four native species. Specificity to ancestral host plant genera or family is typically maintained during in situ diversification both within and among islands. Characterization of a recently discovered island radiation consisting of four species on Convolvulus floridus in the Canary Islands shows patterns and rates of diversification that reflect island topographic complexity and geological dynamism. Although modest in species diversity, this radiation is atypical in diversification on a single host plant species, but typical in the primary role of allopatry in the diversification process.

Batrachochytrium dendrobatidis (Bd) is a globally ubiquitous fungal infection that has emerged to become a primary driver of amphibian biodiversity loss. Despite widespread effort to understand the emergence of this panzootic, the origins of the infection, its patterns of global spread, and principle mode of evolution remain largely unknown. Using comparative population genomics, we discovered three deeply diverged lineages of Bd associated with amphibians. Two of these lineages were found in multiple continents and are associated with known introductions by the amphibian trade. We found that isolates belonging to one clade, the global panzootic lineage (BdGPL) have emerged across at least five continents during the 20th century and are associated with the onset of epizootics in North America, Central America, the Caribbean, Australia, and Europe. The two newly identified divergent lineages, Cape lineage (BdCAPE) and Swiss lineage (BdCH), were found to differ in morphological traits when compared against one another and BdGPL, and we show that BdGPL is hypervirulent. BdGPL uniquely bears the hallmarks of genomic recombination, manifested as extensive intergenomic phylogenetic conflict and patchily distributed heterozygosity. We postulate that contact between previously genetically isolated allopatric populations of Bd may have allowed recombination to occur, resulting in the generation, spread, and invasion of the hypervirulent BdGPL leading to contemporary disease-driven losses in amphibian biodiversity.

Divergent selection may initiate ecological speciation extremely rapidly. How often and at what pace ecological speciation proceeds to yield strong reproductive isolation is more uncertain. Here, we document a case of extraordinarily rapid speciation associated with ecological selection in the postglacial Baltic Sea. European flounders (Platichthys flesus) in the Baltic exhibit two contrasting reproductive behaviors: pelagic and demersal spawning. Demersal spawning enables flounders to thrive in the low salinity of the Northern Baltic, where eggs cannot achieve neutral buoyancy. We show that demersal and pelagic flounders are a species pair arising froma recent event of speciation. Despite having a parapatric distribution with extensive overlap, the two species are reciprocally monophyletic and show strongly bimodal genotypic clustering and no evidence of contemporary migration, suggesting strong reproductive isolation. Divergence across the genome is weak but shows strong signatures of selection, a pattern suggestive of a recent ecological speciation event. We propose that spawning behavior in Baltic flounders is the trait under ecologically based selection causing reproductive isolation, directly implicating a process of ecological speciation. We evaluated different possible evolutionary scenarios under the approximate Bayesian computation framework and estimate that the speciation process started in allopatry ∼2,400 generations ago, following the colonization of the Baltic by the demersal lineage. This is faster than most known cases of ecological speciation and represents the most rapid event of speciation ever reported for any marine vertebrate.

Aerobic metabolism in eukaryotic cells requires extensive interactions between products of the nuclear and mitochondrial genomes. Rapid evolution of the mitochondrial genome, including fixation of both adaptive and deleterious mutations, creates intrinsic selection pressures favoring nuclear gene mutations that maintain mitochondrial function. As this process occurs independently in allopatry, the resulting divergence between conspecific populations can subsequently be manifest in mitonuclear incompatibilities in inter-population hybrids. Such incompatibilities, mitonuclear versions of Bateson–Dobzhansky–Muller incompatibilities that form the standard model for allopatric speciation, can potentially restrict gene flow between populations, ultimately resulting in varying degrees of reproductive isolation. The potential role of mitonuclear incompatibilities in speciation is further enhanced where mtDNA substitution rates are elevated compared to the nuclear genome and where population structure maintains allopatry for adequate time to evolve multiple mitonuclear incompatibilities. However, the fact that mitochondrial introgression occurs across species boundaries has raised questions regarding the efficacy of mitonuclear incompatibilities in reducing gene flow. Several scenarios now appear to satisfactorily explain this phenomenon, including cases where differences in mtDNA genetic load may drive introgression or where co-introgression of coadapted nuclear genes may support the function of introgressed mtDNA. Although asymmetries in reproductive isolation between taxa are consistent with mitonuclear incompatibilities, interactions between autosomes and sex chromosomes yield similar predictions that are difficult to disentangle. With regard to establishing reproductive isolation while in allopatry, existing studies clearly suggest that mitonuclear incompatibilities can contribute to the evolution of barriers to gene flow. However, there is to date relatively little definitive evidence supporting a primary role for mitonuclear incompatibilities in the speciation process.