During the Late Devonian Biodiversity Crisis, the primary driver of biodiversity decline was the dramatic reduction in speciation rates, not elevated extinction rates; however, the causes of speciation decline have been previously unstudied. Speciation, the formation of new species from ancestral populations, occurs by two primary allopatric mechanisms: vicariance, where the ancestral population is passively divided into two large subpopulations that later diverge and form two daughter species, and dispersal, in which a small subset of the ancestral population actively migrates then diverges to form a new species. Studies of modern and fossil clades typically document speciation by vicariance in much higher frequencies than speciation by dispersal. To assess the mechanism behind Late Devonian speciation reduction, speciation rates were calculated within stratigraphically constrained species-level phylogenetic hypotheses for three representative clades and mode of speciation at cladogenetic events was assessed across four clades in three phyla: Arthropoda, Brachiopoda, and Mollusca. In all cases, Devonian taxa exhibited a congruent reduction in speciation rate between the Middle Devonian pre-crisis interval and the Late Devonian crisis interval. Furthermore, speciation via vicariance is almost entirely absent during the crisis interval; most episodes of speciation during this time were due to dispersal. The shutdown of speciation by vicariance during this interval was related to widespread interbasinal species invasions. The lack of Late Devonian vicariance is diametrically opposed to the pattern observed in other geologic intervals, which suggests the loss of vicariant speciation attributable to species invasions during the Late Devonian was a causal factor in the biodiversity crisis. Similarly, modern ecosystems, in which invasive species are rampant, may be expected to exhibit similar shutdown of speciation by vicariance as an outcome of the modern biodiversity crisis.
Conservation biologists routinely face the dilemma of keeping small, fragmented populations isolated, wherein inbreeding depression may ensue, or mixing such populations, which may exacerbate population declines via outbreeding depression. The joint evaluation of inbreeding and outbreeding risks in the wild cannot be readily conducted in endangered species, so a suggested ‘safe’ strategy is to mix ecologically and genetically similar populations. To evaluate this strategy, we carried out a reciprocal transplant experiment involving three neighboring populations of endangered Atlantic salmon (Salmo salar) now bred in captivity and maintained in captive and wild environments. Pure, inbred, and outbred (first and second generation) cross types were released and recaptured in the wild to simultaneously test for local adaptation, inbreeding depression, and outbreeding depression. We found little evidence of inbreeding depression after one generation of inbreeding and little evidence of either heterosis or outbreeding depression via genetic incompatibilities after one or two generations of outbreeding. A trend for outbreeding depression via the loss of local adaptation was documented in one of three populations. The effects of inbreeding were not significantly different from the effects of outbreeding. Hence, at the geographic scale evaluated (34–50 km), inbreeding for one generation and outbreeding over two generations may have similar effects on the persistence of small populations. The results further suggested that outbreeding outcomes may be highly variable or unpredictable at small genetic distances. Our work highlights the necessity of evaluating the relative costs of inbreeding and outbreeding in the conservation and management of endangered species on a case-by-case basis.
Atlantic salmon; Canada; conservation; heterosis; local adaptation; risk assessment
Fifty years ago, Baker and Fedorov proposed that the high species diversity of tropical forests could arise from the combined effects of inbreeding and genetic drift leading to population differentiation and eventually to sympatric speciation. Decades of research, however have failed to support the Baker–Fedorov hypothesis (BFH), and it has now been discarded in favor of a paradigm where most trees are self-incompatible or strongly outcrossing, and where long-distance pollen dispersal prevents population drift. Here, we propose that several hyper-diverse genera of tropical herbs and shrubs, including Piper (>1,000 species), may provide an exception. Species in this genus often have aggregated, high-density populations with self-compatible breeding systems; characteristics which the BFH would predict lead to high local genetic differentiation. We test this prediction for five Piper species on Barro Colorado Island, Panama, using Amplified Fragment Length Polymorphism (AFLP) markers. All species showed strong genetic structure at both fine- and large-spatial scales. Over short distances (200–750 m) populations showed significant genetic differentiation (Fst 0.11–0.46, P < 0.05), with values of spatial genetic structure that exceed those reported for other tropical tree species (Sp = 0.03–0.136). This genetic structure probably results from the combined effects of limited seed and pollen dispersal, clonal spread, and selfing. These processes are likely to have facilitated the diversification of populations in response to local natural selection or genetic drift and may explain the remarkable diversity of this rich genus.
AFLP; Barro Colorado Island; Clonal reproduction; Gene flow; Piperaceae
Under what circumstances speciation in sexually reproducing animals can occur without geographical disjunction is still controversial. According to the ring-species model, a reproductive barrier may arise through 'isolation by distance' when peripheral populations of a species meet after expanding around some uninhabitable barrier. The classical example of this kind of speciation is the herring gull (Larus argentatus) complex, with a circumpolar distribution in the Northern Hemisphere. Based on mitochondrial DNA variation among 21 gull taxa, we show that members of this complex differentiated largely in allopatry following multiple vicariance and long-distance-colonization events, not primarily through isolation by distance. Reproductive isolation evolved more rapidly between some lineages than between others, irrespective of their genetic distance. Extant taxa are the result of divergent as well as reticulate evolution between two ancestral lineages originally separated in a North Atlantic refugium and a continental Eurasian refugium, respectively. Continental birds expanded along the entire north Eurasian coast and via Beringia into North America. Contrary to the ring-species model, we find no genetic evidence for a closure of the circumpolar ring through colonization of Europe by North American herring gulls. However, closure of the ring in the opposite direction may be imminent, with lesser black-backed gulls about to colonize North America.
In wild animal populations, the degree of inbreeding differs between species and within species between populations. Because mating with kin often results in inbreeding depression, observed inbreeding is usually regarded to be caused by limited outbreeding opportunities due to demographic factors like small population size or population substructuring. However, theory predicts inclusive benefits from mating with kin, and thus part of the observed variation in inbreeding might be due to active inbreeding preferences. Although some recent studies indeed report kin mating preferences, the evidence is still highly ambiguous. Here, we investigate inbreeding in a natural population of the West African cichlid fish Pelvicachromis taeniatus which showed clear kin mating preferences in standardized laboratory experiments but no inbreeding depression. The presented microsatellite analysis reveals that the natural population has, in comparison to two reference populations, a reduced allelic diversity (A = 3) resulting in a low heterozygosity (Ho = 0.167) pointing to a highly inbred population. Furthermore, we found a significant heterozygote deficit not only at population (Fis = 0.116) but also at subpopulation level (Fis = 0.081) suggesting that inbreeding is not only a by-product of population substructuring but possibly a consequence of behavioral kin preferences.
The framework for modern studies of speciation was established as part of the Neo-Darwinian synthesis of the early twentieth century. Here we evaluate this framework in the light of recent empirical and theoretical studies. Evidence from experimental studies of selection, quantitative genetic studies of species’ differences, and the molecular evolution of ‘isolation’ genes, all agree that directional selection is the primary cause of speciation, as initially proposed by Darwin. Likewise, as suggested by Dobzhansky and Mayr, gene flow does hold species together, but probably more by facilitating the spread of beneficial mutants and associated hitchhiking events than by homogenizing neutral loci. Reproductive barriers are important as well in that they preserve adaptations, but as has been stressed by botanists for close to a century, they rarely protect the entire genome from gene flow in recently diverged species. Contrary to early views, it is now clear that speciation can occur in the presence of gene flow. However, recent theory does support the long-held view that population structure and small population size may increase speciation rates, but only under special conditions and not because of the increased efficacy of drift as suggested by earlier authors. Rather, low levels of migration among small populations facilitates the rapid accumulation of beneficial mutations that indirectly cause hybrid incompatibilities.
gene flow; introgression; population size; population subdivision; reproductive isolation; selection; selective sweep; speciation
Sympatric speciation—the divergence of populations into new species in absence of geographic barriers to hybridization—is the most debated mode of diversification of life forms. Parasitic organisms are prominent models for sympatric speciation, because they may colonise new hosts within the same geographic area and diverge through host specialization. However, it has been argued that this mode of parasite divergence is not strict sympatric speciation, because host shifts likely cause the sudden effective isolation of parasites, particularly if these are transmitted by vectors and therefore cannot select their hosts. Strict sympatric speciation would involve parasite lineages diverging within a single host species, without any population subdivision.
Here we report a case of extraordinary divergence of sympatric, ecologically distinct, and reproductively isolated malaria parasites within a single avian host species, which apparently occurred without historical or extant subdivision of parasite or host populations.
This discovery of within-host speciation changes our current view on the diversification potential of malaria parasites, because neither geographic isolation of host populations nor colonization of new host species are any longer necessary conditions to the formation of new parasite species.
Speciation is generally viewed as an irreversible process, although habitat alterations can erase reproductive barriers if divergence between ecologically differentiated species is recent. Reversed speciation might also occur if geographical contact is established between species that have evolved the same reproductive isolating barrier in parallel. Here, we demonstrate a loss of intrinsic reproductive isolation in a clade of scincid lizards as a result of parallel body size evolution, which has allowed for gene flow where large-bodied lineages are in secondary contact. An mtDNA phylogeny confirms the monophyly of the Plestiodon skiltonianus species complex, but rejects that of two size-differentiated ecomorphs. Mate compatibility experiments show that the high degree of body size divergence imposes a strong reproductive barrier between the two morphs; however, the strength of the barrier is greatly diminished between parallel-evolved forms. Since two large-bodied lineages are in geographical contact in the Sierra Nevada Mountains of California, we were also able to test for postzygotic isolation under natural conditions. Analyses of amplified fragment length polymorphisms show that extensive gene exchange is occurring across the contact zone, resulting in an overall pattern consistent with isolation by distance. These results provide evidence of reversed speciation between clades that diverged from a common ancestor more than 12 Myr ago.
parallel speciation; parallelism; reproductive isolation; scincid lizards; Plestiodon
Sexual antagonism, or conflict between the sexes, has been proposed as a driving force in both sex chromosome turnover and speciation. Although closely related species often have different sex chromosome systems, it is unknown whether sex chromosome turnover contributes to the evolution of reproductive isolation between species. In this study, we show that a newly evolved sex chromosome harbours genes that contribute to speciation in threespine stickleback fish (Gasterosteus aculeatus). We first identified a neo-sex chromosome system found only in one member of a sympatric species pair in Japan. We then performed genetic linkage mapping of male-specific traits important for reproductive isolation between the Japanese species pair. The neo-X chromosome harbours loci for male courtship display traits that contribute to behavioural isolation, while the ancestral X chromosome contains loci for both behavioural isolation and hybrid male sterility. Our work not only provides strong evidence for a large-X effect on reproductive isolation in a vertebrate system, but also provides direct evidence that a young neo-X chromosome contributes to reproductive isolation between closely related species. Our data suggest that sex chromosome turnover might play a greater role in speciation than previously appreciated.
The modern evolutionary synthesis codified the idea that species exist as distinct entities because intrinsic reproductive barriers prevent them from merging together. Understanding the origin of species therefore requires understanding the evolution and genetics of reproductive barriers between species. In most cases, speciation is an accident that happens as different populations adapt to different environments and, incidentally, come to differ in ways that render them reproductively incompatible. As with other reproductive barriers, the evolution and genetics of interspecific hybrid sterility and lethality were once also thought to evolve as pleiotripic side effects of adaptation. Recent work on the molecular genetics of speciation has raised an altogether different possibility—the genes that cause hybrid sterility and lethality often come to differ between species not because of adaptation to the external ecological environment but because of internal evolutionary arms races between selfish genetic elements and the genes of the host genome. Arguably one of the best examples supporting a role of ecological adaptation comes from a population of yellow monkey flowers, Mimulus guttatus, in Copperopolis, California, which recently evolved tolerance to soil contaminants from copper mines and simultaneously, as an incidental by-product, hybrid lethality in crosses with some off-mine populations. However, in new work, Wright and colleagues show that hybrid lethality is not a pleiotropic consequence of copper tolerance. Rather, the genetic factor causing hybrid lethality is tightly linked to copper tolerance and spread to fixation in Copperopolis by genetic hitchhiking.
Two models for speciation via selection have been proposed. In the well-known model of ‘ecological speciation’, divergent natural selection between environments drives the evolution of reproductive isolation. In a second ‘mutation-order’ model, different, incompatible mutations (alleles) fix in different populations adapting to the same selective pressure. How to demonstrate mutation-order speciation has been unclear, although it has been argued that it can be ruled out when gene flow occurs because the same, most advantageous allele will fix in all populations. However, quantitative examination of the interaction of factors influencing the likelihood of mutation-order speciation is lacking. We used simulation models to study how gene flow, hybrid incompatibility, selective advantage, timing of origination of new mutations and an initial period of allopatric differentiation affect population divergence via the mutation-order process. We find that at least some population divergence can occur under a reasonably wide range of conditions, even with moderate gene flow. However, strong divergence (e.g. fixation of different alleles in different populations) requires very low gene flow, and is promoted when (i) incompatible mutations have similar fitness advantages, (ii) less fit mutations arise slightly earlier in evolutionary time than more fit alternatives, and (iii) allopatric divergence occurs prior to secondary contact.
Dobzhansky–Muller incompatibilities; ecological speciation; gene flow; migration; reproductive isolation; uniform selection
Many continental sister species are allopatric or parapatric, ecologically similar and long separated, of the order of millions of years. Sympatric, ecologically differentiated, species, are often even older. This raises the question of whether build-up of sympatric diversity generally follows a slow process of divergence in allopatry, initially without much ecological change. I review patterns of speciation among birds belonging to the continental Eurasian Old World leaf warblers (Phylloscopus and Seicercus). I consider speciation to be a three-stage process (range expansions, barriers to gene flow, reproductive isolation) and ask how ecological factors at each stage have contributed to speciation, both among allopatric/parapatric sister species and among those lineages that eventually led to currently sympatric species. I suggest that time is probably the critical factor that leads to reproductive isolation between sympatric species and that a strong connection between ecological divergence and reproductive isolation remains to be established. Besides reproductive isolation, ecological factors can affect range expansions (e.g. habitat tracking) and the formation of barriers (e.g. treeless areas are effective barriers for warblers). Ecological factors may often limit speciation on continents because range expansions are difficult in ‘ecologically full’ environments.
allospecies; ecological speciation; Phylloscopus and Seicercus; speciation; time-dated phylogenies; vicariance
Marine allopatric speciation is an enigma because pelagic larval dispersal can potentially connect disjunct populations thereby preventing reproductive and morphological divergence. Here we present a new hierarchical approximate Bayesian computation model (HABC) that tests two hypotheses of marine allopatric speciation: 1.) "soft vicariance", where a speciation involves fragmentation of a large widespread ancestral species range that was previously connected by long distance gene flow; and 2.) peripatric colonization, where speciations in peripheral archipelagos emerge from sweepstakes colonizations from central source regions. The HABC approach analyzes all the phylogeographic datasets at once in order to make across taxon-pair inferences about biogeographic processes while explicitly allowing for uncertainty in the demographic differences within each taxon-pair. Our method uses comparative phylogeographic data that consists of single locus mtDNA sequences from multiple co-distributed taxa containing pairs of central and peripheral populations. We use the method on two comparative phylogeographic data sets consisting of cowrie gastropod endemics co-distributed in the Hawaiian (11 taxon-pairs) and Marquesan archipelagos (7 taxon-pairs).
Given the Marquesan data, we find strong evidence of simultaneous colonization across all seven cowrie gastropod endemics co-distributed in the Marquesas. In contrast, the lower sample sizes in the Hawaiian data lead to greater uncertainty associated with the Hawaiian estimates. Although, the hyper-parameter estimates point to soft vicariance in a subset of the 11 Hawaiian taxon-pairs, the hyper-prior and hyper-posterior are too similar to make a definitive conclusion. Both results are not inconsistent with what is known about the geologic history of the archipelagos. Simulations verify that our method can successfully distinguish these two histories across a wide range of conditions given sufficient sampling.
Although soft vicariance and colonization are likely to produce similar genetic patterns when a single taxon-pair is used, our hierarchical Bayesian model can potentially detect if either history is a dominant process across co-distributed taxon-pairs. As comparative phylogeographic datasets grow to include > 100 co-distributed taxon-pairs, the HABC approach will be well suited to dissect temporal patterns in community assembly and evolution, thereby providing a bridge linking comparative phylogeography with community ecology.
Bacteria of the genus Wolbachia are reproductive parasites widespread among arthropods. The most common effect arising from the presence of Wolbachia in a population is Cytoplasmic Incompatibility (CI), whereby postmating reproductive isolation occurs in crosses between an infected male and an uninfected female, or when a male is infected with a different strain of Wolbachia to that of the female (bidirectional CI). Previous theoretical models have demonstrated that bidirectional CI can contribute to the genetic divergence of populations in haploid and diploid organisms. However, haplodiploid organisms were not considered in these models even though they include Nasonia parasitoid wasps – the best example of the implication of Wolbachia in ongoing speciation. Moreover, previous work did not investigate inbreeding mating systems, which are frequently observed in arthropod species.
We developed a stochastic two-island model which simulated three genetic scenarios, diploidy, haploidy, and haplodiploidy, with two CI phenotypes being considered for the latter: (1) male development of female progeny; and (2) mortality of fertilized eggs. We also investigated the effect of varying the proportion of sib mating. In the model each allopatric population was initially fixed for a single allele at a nuclear locus under positive selection and infected with one strain of Wolbachia. Each simulation presupposed that the two populations were fixed for a different allele and a different strain of Wolbachia. The degree of genetic differentiation observed in the locus under selection due to bidirectional CI was much lower for the two haplodiploid phenotypes than for either diploids or haploids. Furthermore, we demonstrated that sib-mating may compensate for the lower efficiency of bidirectional CI in haplodiploids by maintaining genetic divergence.
Our model suggests that maintenance of genetic differentiation facilitated by Wolbachia is more likely to occur in diploids and haploids than in haplodiploids. However, increasing the level of sib-mating may compensate for the weak effect of bidirectional CI in haplodiploids. Our work therefore gives a potential explanation for why the haplodiploid Nasonia species, which are infected with bidirectionally incompatible Wolbachia strains and undergo sib-mating, have differentiated genetically and maintained this differentiation without premating isolation.
Maintaining wildtype zebrafish stocks for research while preserving viability within the lines used presents significant challenges to zebrafish husbandry practices. Genetic homogeneity is established through inbreeding in order to provide continuity across experiments. This, however, leads to decreased fitness through inbreeding depression. In the laboratory setting, it is imperative that researchers consistently obtain a large number of viable embryos, thus, inbreeding depression must be suppressed. Genetic variation can be established by creating hybrid lines, however, crosses between genetically distinct lines can cause an outbreeding depression as well. There is little data describing the effects of inbreeding depression or outbreeding depression from such crosses in zebrafish. Additionally, there is an unmet need to establish breeding standards within the zebrafish field. This study examines the susceptibility to inbreeding and outbreeding depression in crosses between four wildtype zebrafish lines: the inbred lines AB and Tab14 and the F1 generation of hybrid lines TuAB and TLAB. We report that mating frequency and clutch size were significantly greater in hybrid female crosses than inbred female crosses. This study demonstrates that inbreeding depression in common zebrafish lines such as the AB and Tab14 used here, results in fewer successful matings and smaller clutch sizes. Furthermore, we find evidence that outbreeding depression caused by crossing distantly related lines, such as the inbred Tab14 and the hybrid TLAB lines can also influence successful zebrafish mating. These data provide evidence needed to further characterize commonly used wildtype zebrafish lines. We suggest, that to maintain lines that mate frequently and yield large clutches, hybrid females of known backgrounds should be used.
Maintaining wild-type (WT) zebrafish stocks for research while preserving viability within the lines used presents significant challenges to zebrafish husbandry practices. Genetic homogeneity is established through inbreeding to provide continuity across experiments. This, however, leads to decreased fitness through inbreeding depression. In the laboratory setting, it is imperative that researchers consistently obtain a large number of viable embryos; thus, inbreeding depression must be suppressed. Genetic variation can be established by creating hybrid lines; however, crosses between genetically distinct lines can cause an outbreeding depression as well. There is little data describing the effects of inbreeding depression or outbreeding depression from such crosses in zebrafish. Additionally, there is a need to establish breeding standards within the zebrafish field. This study examines the susceptibility to inbreeding and outbreeding depression in crosses between four WT zebrafish lines: the inbred lines AB and Tab 14, and the F1 generation of hybrid lines TuAB and TLAB. We report that mating frequency and clutch size were significantly greater in hybrid female crosses than in inbred female crosses. Inbreeding depression in common zebrafish lines such as AB and Tab 14 used here results in fewer successful matings and smaller clutch sizes. Further, outbreeding depression caused by crossing distantly related lines, such as the inbred Tab 14 and the hybrid TLAB lines, can also influence successful zebrafish mating. These data provide evidence needed to further characterize commonly used WT zebrafish lines. We suggest that to maintain lines that mate frequently and yield large clutches, hybrid females of known backgrounds should be used.
Reinforcement, the strengthening of prezygotic reproductive isolation by natural selection in response to maladaptive hybridization [1, 2, 3], is one of the few processes in which natural selection directly favors the evolution of species as discrete groups [e.g., 4, 5, 6, 7]. The evolution of reproductive barriers via reinforcement is expected to evolve in regions where the ranges of two species overlap and hybridize, as an evolutionary solution to avoiding the costs of maladaptive hybridization [2, 3, 8]. The role of reinforcement in speciation has, however, been highly controversial because population-genetic theory suggests that the process is severely impeded by both hybridization [8, 9,10,11] and migration of individuals from outside the contact zone [12, 13]. To determine whether reinforcement could strengthen the reproductive barriers between two sister species of Drosophila in the face of these impediments, I initiated experimental populations of these two species that allowed different degrees of hybridization as well as migration from outside populations. Surprisingly, even in the face of gene flow, reinforcement could promote the evolution of reproductive isolation within only five generations. As theory predicts, high levels of hybridization (and/or strong selection against hybrids) and migration impeded this evolution. These results suggest that reinforcement can help complete the process of speciation.
Speciation; isolating barriers; postmating-prezygotic isolation; reinforcement; artificial selection; experimental evolution
Widely distributed species with populations adapted to different environmental conditions can provide valuable opportunities for tracing the onset of reproductive incompatibilities and their role in the speciation process. Drosophila montana, a D. virilis group species found in high latitude boreal forests in Nearctic and Palearctic regions around the globe, could be an excellent model system for studying the early stages of speciation, as a wealth of information concerning this species' ecology, mating system, life history, genetics and phylogeography is available. However, reproductive barriers between populations have hereto not been investigated.
We report both pre- and postmating barriers to reproduction between flies from European (Finnish) and North American (Canadian) populations of Drosophila montana. Using a series of mate-choice designs, we show that flies from these two populations mate assortatively (i.e., exhibit significant sexual isolation) while emphasizing the importance of experimental design in these kinds of studies. We also assessed potential postmating isolation by quantifying egg and progeny production in intra- and interpopulation crosses and show a significant one-way reduction in progeny production, affecting both male and female offspring equally.
We provide evidence that allopatric D. montana populations exhibit reproductive isolation and we discuss the potential mechanisms involved. Our data emphasize the importance of experimental design in studies on premating isolation between recently diverged taxa and suggest that postmating barriers may be due to postcopulatory-prezygotic mechanisms. D. montana populations seem to be evolving multiple barriers to gene flow in allopatry and our study lays the groundwork for future investigations of the genetic and phenotypic mechanisms underlying these barriers.
Using a weak migration and weak mutation approximation, I studied the average waiting time to parapatric speciation. The description of reproductive isolation used is based on the classical Dobzhansky model and its recently proposed multilocus generalizations. The dynamics of parapatric speciation are modelled as a biased random walk performed by the average genetic distance between the residents and immigrants. If a small number of genetic changes is sufficient for complete reproductive isolation, mutation and random genetic drift alone can cause speciation on the time-scale of ten to 1,000 times the inverse of the mutation rate over a set of loci underlying reproductive isolation. Even relatively weak selection for local adaptation can dramatically decrease the waiting time to speciation. The actual duration of the parapatric speciation process (that is the duration of intermediate forms in the actual transition to a state of complete reproductive isolation) is shorter by orders of magnitude than the overall waiting time to speciation. For a wide range of parameter values, the actual duration of parapatric speciation is of the order of one over the mutation rate. In general, parapatric speciation is expected to be triggered by changes in the environment.
The notion of a positive relation between geographical range and speciation rate or speciation probability may go back to Darwin, but a negative relation between these parameters is equally plausible. Here, we test these alternatives in fossil and living molluscan taxa. Late Cretaceous gastropod genera exhibit a strong negative relation between the geographical ranges of constituent species and speciation rate per species per million years; this result is robust to sampling biases against small-bodied taxa and is not attributable to phylogenetic effects. They also exhibit weak inverse or non-significant relations between geographical range and (i) the total number of species produced over the 18 million year timeframe, and (ii) the number of species in a single timeplane. Sister-group comparisons using extant molluscan species also show a non-significant relation between median geographical range and species richness of genera. These results support the view that the factors promoting broad geographical ranges also tend to damp speciation rates. They also demonstrate that a strong inverse relation between per-species speciation rate and geographical range need not be reflected in analyses conducted within a single timeplane, underscoring the inadequacy of treating net speciation as a proxy for raw per-taxon rates.
Analyses of speciation genes – genes that contribute to the cessation of gene flow between populations – can offer clues regarding the ecological settings, evolutionary forces and molecular mechanisms that drive the divergence of populations and species. This review discusses the identities and attributes of genes that contribute to reproductive isolation (RI) in plants, compares them with animal speciation genes and investigates what these genes can tell us about speciation.
Forty-one candidate speciation genes were identified in the plant literature. Of these, seven contributed to pre-pollination RI, one to post-pollination, prezygotic RI, eight to hybrid inviability, and 25 to hybrid sterility. Genes, gene families and genetic pathways that were frequently found to underlie the evolution of RI in different plant groups include the anthocyanin pathway and its regulators (pollinator isolation), S RNase-SI genes (unilateral incompatibility), disease resistance genes (hybrid necrosis), chimeric mitochondrial genes (cytoplasmic male sterility), and pentatricopeptide repeat family genes (cytoplasmic male sterility).
The most surprising conclusion from this review is that identities of genes underlying both prezygotic and postzygotic RI are often predictable in a broad sense from the phenotype of the reproductive barrier. Regulatory changes (both cis and trans) dominate the evolution of pre-pollination RI in plants, whereas a mix of regulatory mutations and changes in protein-coding genes underlie intrinsic postzygotic barriers. Also, loss-of-function mutations and copy number variation frequently contribute to RI. Although direct evidence of positive selection on speciation genes is surprisingly scarce in plants, analyses of gene family evolution, along with theoretical considerations, imply an important role for diversifying selection and genetic conflict in the evolution of RI. Unlike in animals, however, most candidate speciation genes in plants exhibit intraspecific polymorphism, consistent with an important role for stochastic forces and/or balancing selection in development of RI in plants.
Speciation; reproductive isolation; mating system isolation; pollinator isolation; ecological isolation; unilateral incompatibility; hybrid necrosis; hybrid sterility; hybrid inviability; hybrid breakdown; cytoplasmic male sterility; restoration
After the discovery of eusociality in the naked mole-rat, it was proposed that inbreeding and high colony relatedness in this species were the major underlying factors driving cooperative breeding in African molerats. By contrast, field and laboratory studies of the eusocial Damaraland mole-rat (Cryptomys damarensis) have raised the possibility that this species is an obligate outbreeder, although the build-up of inbreeding over several generations could still occur. Using microsatellite markers, we show that most breeding pairs in wild colonies of the Damaraland mole-rat are indeed unrelated (R = 0.02 +/- 0.04) and that mean colony relatedness (R = 0.46 +/- 0.01), determined across 15 colonies from three separate populations, is little more than half that previously identified in naked mole-rats. This finding demonstrates that normal familial levels of relatedness are sufficient for the occurrence of eusociality in mammals. Variation in the mean colony relatedness among populations provides support both for the central role played by ecological constraints in cooperative breeding and for the suggestion that inbreeding in naked mole-rats is a response to extreme constraints on dispersal. Approaches that determine the relative importance of an array of extrinsic factors in driving social evolution in African mole-rats are now required.
The study of speciation and maintenance of species barriers is at the core of evolutionary biology. During speciation the genome of one population becomes separated from other populations of the same species, which may lead to genomic incompatibility with time. This separation is complete when no fertile offspring is produced from inter-population matings, which is the basis of the biological species concept. Birds, in particular ducks, are recognised as a challenging and illustrative group of higher vertebrates for speciation studies. There are many sympatric and ecologically similar duck species, among which fertile hybrids occur relatively frequently in nature, yet these species remain distinct.
We show that the degree of shared single nucleotide polymorphisms (SNPs) between five species of dabbling ducks (genus Anas) is an order of magnitude higher than that previously reported between any pair of eukaryotic species with comparable evolutionary distances. We demonstrate that hybridisation has led to sustained exchange of genetic material between duck species on an evolutionary time scale without disintegrating species boundaries. Even though behavioural, genetic and ecological factors uphold species boundaries in ducks, we detect opposing forces allowing for viable interspecific hybrids, with long-term evolutionary implications. Based on the superspecies concept we here introduce the novel term "supra-population" to explain the persistence of SNPs identical by descent within the studied ducks despite their history as distinct species dating back millions of years.
By reviewing evidence from speciation theory, palaeogeography and palaeontology we propose a fundamentally new model of speciation to accommodate our genetic findings in dabbling ducks. This model, we argue, may also shed light on longstanding unresolved general speciation and hybridisation patterns in higher organisms, e.g. in other bird groups with unusually high hybridisation rates. Observed parallels to horizontal gene transfer in bacteria facilitate the understanding of why ducks have been such an evolutionarily successful group of animals. There is large evolutionary potential in the ability to exchange genes among species and the resulting dramatic increase of effective population size to counter selective constraints.
Speciation is characterized by the evolution of reproductive isolation between two groups of organisms. Understanding the process of speciation requires the quantification of barriers to reproductive isolation, dissection of the genetic mechanisms that contribute to those barriers and determination of the forces driving the evolution of those barriers. Through a comprehensive analysis involving 19 pairs of plant taxa, we assessed the strength and patterns of asymmetry of multiple prezygotic and postzygotic reproductive isolating barriers. We then reviewed contemporary knowledge of the genetic architecture of reproductive isolation and the relative role of chromosomal and genic factors in intrinsic postzygotic isolation. On average, we found that prezygotic isolation is approximately twice as strong as postzygotic isolation, and that postmating barriers are approximately three times more asymmetrical in their action than premating barriers. Barriers involve a variable number of loci, and chromosomal rearrangements may have a limited direct role in reproductive isolation in plants. Future research should aim to understand the relationship between particular genetic loci and the magnitude of their effect on reproductive isolation in nature, the geographical scale at which plant speciation occurs, and the role of different evolutionary forces in the speciation process.
speciation; asymmetry; Bateson–Dobzhansky–Muller incompatibilities; chromosomal rearrangements; quantitative trait loci
Islands are bounded areas where high endemism is explained either by allopatric speciation through the fragmentation of the limited amount of space available, or by sympatric speciation and accumulation of daughter species. Most empirical evidence point out the dominant action of allopatric speciation. We evaluate this general view by looking at a case study where sympatric speciation is suspected. We analyse the mode, tempo and geography of speciation in Agnotecous, a cricket genus endemic to New Caledonia showing a generalized pattern of sympatry between species making sympatric speciation plausible. We obtained five mitochondrial and five nuclear markers (6.8 kb) from 37 taxa corresponding to 17 of the 21 known extant species of Agnotecous, and including several localities per species, and we conducted phylogenetic and dating analyses. Our results suggest that the diversification of Agnotecous occurred mostly through allopatric speciation in the last 10 Myr. Highly microendemic species are the most recent ones (<2 Myr) and current sympatry is due to secondary range expansion after allopatric speciation. Species distribution should then be viewed as a highly dynamic process and extreme microendemism only as a temporary situation. We discuss these results considering the influence of climatic changes combined with intricate soil diversity and mountain topography. A complex interplay between these factors could have permitted repeated speciation events and range expansion.