The Maynard Smith model of sympatric speciation

The paper entitled "Sympatric speciation," which was published by John Maynard Smith in 1966, initiated the development of mathematical models aiming to identify the conditions for sympatric speciation. A part of that paper was devoted to a specific two-locus, two-allele model of sympatric speciation in a population occupying a two-niche system. Maynard Smith provided some initial numerical results on this model. Later, Dickinson and Antonovics (1973) and Caisse and Antonovics (1978) performed more extensive numerical studies on the model. Here, I report analytical results on the haploid version of the Maynard Smith model. I show how the conditions for sympatric and parapatric speciation and the levels of resulting genetic divergence and reproductive isolation are affected by the strength of disruptive selection and nonrandom mating, recombination rate, and the rates of male and female dispersal between the niches.     

Ecological opportunity and diversification in a continental radiation of birds: climbing adaptations and cladogenesis in the Furnariidae

Ecological theories of adaptive radiation predict that ecological opportunity stimulates cladogenesis through its effects on competitive release and niche expansion. Given that key innovations may confer ecological opportunity, we investigated the effect of the acquisition of climbing adaptations on rates of cladogenesis in a major avian radiation, the Neotropical bird family Furnariidae, using a species-level phylogeny. Morphological specializations for vertical climbing originated in the woodcreepers ～23 million years ago, well before that adaptation occurred in woodpeckers (Picidae) or in other potential competitors in South America. This suggests that the acquisition of climbing adaptations conferred ample ecological opportunity to early woodcreepers. Nonetheless, we found that increases in speciation rates in Furnariidae did not coincide with the acquisition of climbing adaptations and that the relationship between the accumulation of climbing adaptations and rates of speciation was negative. In addition, we did not detect a diversity-dependent decline in woodcreeper diversification rates consistent with saturation of the trunk-climbing niche. These findings do not support the hypothesis that ecological opportunity related to trunk foraging stimulated cladogenesis in this radiation. The negative effect of climbing on diversification may be mediated by an indirect positive effect of climbing on dispersal ability, which may reduce speciation rates over evolutionary timescales.     

Speciation along a depth gradient in a marine adaptive radiation

Oceans are home to much of the world''s biodiversity, but we know little about the processes driving speciation in marine ecosystems with few geographical barriers to gene flow. Ecological speciation resulting from divergent natural selection between ecological niches can occur in the face of gene flow. Sister species in the young and ecologically diverse rockfish genus Sebastes coexist in the northeast Pacific, implying that speciation may not require geographical isolation. Here, I use a novel phylogenetic comparative analysis to show that rockfish speciation is instead associated with divergence in habitat depth and depth-associated morphology, consistent with models of parapatric speciation. Using the same analysis, I find no support for alternative hypotheses that speciation involves divergence in diet or life history, or that speciation involves geographic isolation by latitude. These findings support the hypothesis that rockfishes undergo ecological speciation on an environmental gradient.     

Species interactions during diversification and community assembly in an island radiation of shrews

Background

Closely related, ecologically similar species often have adjacent distributions, suggesting competitive exclusion may contribute to the structure of some natural communities. In systems such as island archipelagos, where speciation is often tightly associated with dispersal over oceanic barriers, competitive exclusion may prevent population establishment following inter-island dispersal and subsequent cladogenesis.

Methodology/Principal Findings

Using a combination of tools, we test the hypothesis that the distributions of shrew (Crocidura) species in the Philippines are the result of competitive exclusion preventing secondary invasion of occupied islands. We first compare ecological niche models between two widespread, allopatric species and find statistical support for their ecological similarity, implying that competition for habitat between these species is possible. We then examine dispersion patterns among sympatric species and find some signal for overdispersion of body size, but not for phylogenetic branch length. Finally, we simulate the process of inter-island colonization under a stochastic model of dispersal lacking ecological forces. Results are dependent on the geographic scope and colonization probability employed. However, some combinations suggest that the number of inter-island dispersal events necessary to populate the archipelago may be much higher than the minimum number of colonization events necessary to explain current estimates of species richness and phylogenetic relationships. If our model is appropriate, these results imply that alternative factors, such as competitive exclusion, may have influenced the process of inter-island colonization and subsequent cladogenesis.

Conclusions/Significance

We interpret the combined results as providing tenuous evidence that similarity in body size may prevent co-occurrence in Philippine shrews and that competitive exclusion among ecologically similar species, rather than an inability to disperse among islands, may have limited diversification in this group, and, possibly other clades endemic to island archipelagos.     

Modes of speciation and the neutral theory of biodiversity

Hubbell's neutral theory of biodiversity has generated much debate over the need for niches to explain biodiversity patterns. Discussion of the theory has focused on its neutrality assumption, i.e. the functional equivalence of species in competition and dispersal. Almost no attention has been paid to another critical aspect of the theory, the assumptions on the nature of the speciation process. In the standard version of the neutral theory each individual has a fixed probability to speciate. Hence, the speciation rate of a species is directly proportional to its abundance in the metacommunity. We argue that this assumption is not realistic for most speciation modes because speciation is an emergent property of complex processes at larger spatial and temporal scales and, consequently, speciation rate can either increase or decrease with abundance. Accordingly, the assumption that speciation rate is independent of abundance (each species has a fixed probability to speciate) is a more natural starting point in a neutral theory of biodiversity. Here we present a neutral model based on this assumption and we confront this new model to 20 large data sets of tree communities, expecting the new model to fit the data better than Hubbell's original model. We find, however, that the data sets are much better fitted by Hubbell's original model. This implies that species abundance data can discriminate between different modes of speciation, or, stated otherwise, that the mode of speciation has a large impact on the species abundance distribution. Our model analysis points out new ways to study how biodiversity patterns are shaped by the interplay between evolutionary processes (speciation, extinction) and ecological processes (competition, dispersal).     

The evolution of conditional dispersal and reproductive isolation along environmental gradients

Dispersal modulates gene flow throughout a population's spatial range. Gene flow affects adaptation at local spatial scales, and consequently impacts the evolution of reproductive isolation. A recent theoretical investigation has demonstrated that local adaptation along an environmental gradient, facilitated by the evolution of limited dispersal, can lead to parapatric speciation even in the absence of assortative mating. This and other studies assumed unconditional dispersal, so individuals start dispersing without regard to local environmental conditions. However, many species disperse conditionally; their propensity to disperse is contingent upon environmental cues, such as the degree of local crowding or the availability of suitable mates. Here, we use an individual-based model in continuous space to investigate by numerical simulation the relationship between the evolution of threshold-based conditional dispersal and parapatric speciation driven by frequency-dependent competition along environmental gradients. We find that, as with unconditional dispersal, parapatric speciation occurs under a broad range of conditions when reproduction is asexual, and under a more restricted range of conditions when reproduction is sexual. In both the asexual and sexual cases, the evolution of conditional dispersal is strongly influenced by the slope of the environmental gradient: shallow environmental gradients result in low dispersal thresholds and high dispersal distances, while steep environmental gradients result in high dispersal thresholds and low dispersal distances. The latter, however, remain higher than under unconditional dispersal, thus undermining isolation by distance, and hindering speciation in sexual populations. Consequently, the speciation of sexual populations under conditional dispersal is triggered by a steeper gradient than under unconditional dispersal. Enhancing the disruptiveness of frequency-dependent selection, more box-shaped competition kernels dramatically lower the speciation-enabling slope of the environmental gradient.     

ALTRUISM IN MENDELIAN POPULATIONS DERIVED FROM SIBLING GROUPS: THE HAYSTACK MODEL REVISITED

A group-selection model is presented in which each group is initiated by a single fertilized female and persists for several generations before dispersal. Maynard Smith (1964) concluded that altruism could not plausibly evolve under these circumstances. I show that his conclusion is an artifact of a simplifying assumption that amounts to a worst-case scenario for group selection. When the standard donor-recipient equations for altruistic behavior are used in Maynard Smith's model, Mendelian populations derived from sibling groups are often more favorable for the evolution of altruism than are the sibling groups themselves. In general, long-term and large-scale aspects of population structure may at times be important in the evolution of altruistic and other group-advantageous behaviors.     

Seed dispersal by wind decreases when plants are water‐stressed,potentially counteracting species coexistence and niche evolution

Hydrology is a major environmental factor determining plant fitness, and hydrological niche segregation (HNS) has been widely used to explain species coexistence. Nevertheless, the distribution of plant species along hydrological gradients does not only depend on their hydrological niches but also depend on their seed dispersal, with dispersal either weakening or reinforcing the effects of HNS on coexistence. However, it is poorly understood how seed dispersal responds to hydrological conditions. To close this gap, we conducted a common‐garden experiment exposing five wind‐dispersed plant species (Bellis perennis, Chenopodium album, Crepis sancta, Hypochaeris glabra, and Hypochaeris radicata) to different hydrological conditions. We quantified the effects of hydrological conditions on seed production and dispersal traits, and simulated seed dispersal distances with a mechanistic dispersal model. We found species‐specific responses of seed production, seed dispersal traits, and predicted dispersal distances to hydrological conditions. Despite these species‐specific responses, there was a general positive relationship between seed production and dispersal distance: Plants growing in favorable hydrological conditions not only produce more seeds but also disperse them over longer distances. This arises mostly because plants growing in favorable environments grow taller and thus disperse their seeds over longer distances. We postulate that the positive relationship between seed production and dispersal may reduce the concentration of each species to the environments favorable for it, thus counteracting species coexistence. Moreover, the resulting asymmetrical gene flow from favorable to stressful habitats may slow down the microevolution of hydrological niches, causing evolutionary niche conservatism. Accounting for context‐dependent seed dispersal should thus improve ecological and evolutionary models for the spatial dynamics of plant populations and communities.     

Reed frog diversification in the Gulf of Guinea: Overseas dispersal,the progression rule,and in situ speciation

Oceanic islands accumulate endemic species when new colonists diverge from source populations or by in situ diversification of resident island endemics. The relative importance of dispersal versus in situ speciation in generating diversity on islands varies with a number of archipelago characteristics including island size, age, and remoteness. Here, we characterize interisland dispersal and in situ speciation in frogs endemic to the Gulf of Guinea islands. Using mitochondrial sequence and genome‐wide single‐nucleotide polymorphism data, we demonstrate that dispersal proceeded from the younger island (São Tomé) to the older island (Príncipe) indicating that for organisms that disperse overseas on rafts, dispersal between islands may be determined by ocean currents and not island age. We find that dispersal between the islands is not ongoing, resulting in genotypically distinct but phenotypically similar lineages on the two islands. Finally, we demonstrate that in situ diversification on São Tomé Island likely proceeded in allopatry due to the geographic separation of breeding sites, resulting in phenotypically distinct species. We find evidence of hybridization between the species where their ranges are sympatric and the hybrid zone coincides with a transition from agricultural land to primary forest, indicating that anthropogenic development may have facilitated secondary contact between previously allopatric species.     

Diversification and the adaptive radiation of the vangas of Madagascar

The vangas of Madagascar exhibit extreme diversity in morphology and ecology. Recent studies have shown that several other Malagasy species also are part of this endemic radiation, even as the monophyly of the clade remains in question. Using DNA sequences from 13 genes and representatives of all 15 vanga genera, we find strong support for the monophyly of the Malagasy vangids and their inclusion in a family along with six aberrant genera of shrike-like corvoids distributed in Asia and Africa. Biogeographic reconstructions of these lineages include both Asia and Africa as possible dispersal routes to Madagascar. To study patterns of speciation through time, we introduce a method that can accommodate phylogenetically non-random patterns of incomplete taxon sampling in diversification studies. We demonstrate that speciation rates in vangas decreased dramatically through time following the colonization of Madagascar. Foraging strategies of these birds show remarkable congruence with phylogenetic relationships, indicating that adaptations to feeding specializations played a role in the diversification of these birds. Vangas fit the model of an 'adaptive radiation' in that they show an explosive burst of speciation soon after colonization, increased diversification into novel niches and extraordinary ecomorphological diversity.     

Origin and evolution of the Micronesian biota: Insights from molecular phylogenies and biogeography reveal long-distance dispersal scenarios and founder-event speciation

Micronesian islands taxa show high endemism rates, but very little is known about their biogeographical histories. The lack of systematic biogeography is mainly due to insufficient phylogenetic research in Micronesia. With the recent increase in published molecular biogeographic data, we were able to, for the first time, answer fundamental biogeography questions by reviewing and analyzing numerous geological, ecological, and evolutionary studies. This review, in addition to providing an overview of Micronesian geological history, confirmed the importance of long-distance dispersal mechanisms and founder-event speciation, and morphological and physiological adaptations of plant propagules to cross vast stretches of ocean by wind, ocean currents, bird, or bat dispersal. These adaptations to habitat and geological features, including reef types, determined colonization success as well as inland dispersal and speciation mechanisms. We further identified the source areas of the Micronesian biota and reconstructed historical dispersal scenarios: a dominant Austro-Melanesian dispersal scenario, an Indo-Malaysian connecting to the Austro-Melanesian dispersal scenario, and a Neotropical American and an African dispersal scenario toward Micronesia. Most generic origins were estimated between the Eocene and the Miocene and dispersed to Micronesia between the Miocene and the Pleistocene.     

Environmental niche equivalency versus conservatism: quantitative approaches to niche evolution

Environmental niche models, which are generated by combining species occurrence data with environmental GIS data layers, are increasingly used to answer fundamental questions about niche evolution, speciation, and the accumulation of ecological diversity within clades. The question of whether environmental niches are conserved over evolutionary time scales has attracted considerable attention, but often produced conflicting conclusions. This conflict, however, may result from differences in how niche similarity is measured and the specific null hypothesis being tested. We develop new methods for quantifying niche overlap that rely on a traditional ecological measure and a metric from mathematical statistics. We reexamine a classic study of niche conservatism between sister species in several groups of Mexican animals, and, for the first time, address alternative definitions of "niche conservatism" within a single framework using consistent methods. As expected, we find that environmental niches of sister species are more similar than expected under three distinct null hypotheses, but that they are rarely identical. We demonstrate how our measures can be used in phylogenetic comparative analyses by reexamining niche divergence in an adaptive radiation of Cuban anoles. Our results show that environmental niche overlap is closely tied to geographic overlap, but not to phylogenetic distances, suggesting that niche conservatism has not constrained local communities in this group to consist of closely related species. We suggest various randomization tests that may prove useful in other areas of ecology and evolutionary biology.     

Disruptive natural selection predicts divergence between the sexes during adaptive radiation

Evolution of sexual dimorphism in ecologically relevant traits, for example, via resource competition between the sexes, is traditionally envisioned to stall the progress of adaptive radiation. An alternative view is that evolution of ecological sexual dimorphism could in fact play an important positive role by facilitating sex‐specific adaptation. How competition‐driven disruptive selection, ecological sexual dimorphism, and speciation interact during real adaptive radiations is thus a critical and open empirical question. Here, we examine the relationships between these three processes in a clade of salamanders that has recently radiated into divergent niches associated with an aquatic life cycle. We find that morphological divergence between the sexes has occurred in a combination of head shape traits that are under disruptive natural selection within breeding ponds, while divergence among species means has occurred independently of this disruptive selection. Further, we find that adaptation to aquatic life is associated with increased sexual dimorphism across taxa, consistent with the hypothesis of clade‐wide character displacement between the sexes. Our results suggest the evolution of ecological sexual dimorphism may play a key role in niche divergence among nascent species and demonstrate that ecological sexual dimorphism and ecological speciation can and do evolve concurrently in the early stages of adaptive radiation.     

CORRELATED TROPHIC SPECIALIZATION AND GENETIC DIVERGENCE IN SYMPATRIC LAKE WHITEFISH ECOTYPES (COREGONUS CLUPEAFORMIS): SUPPORT FOR THE ECOLOGICAL SPECIATION HYPOTHESIS

There is ample empirical evidence that phenotypic diversification in an adaptive radiation is the outcome of divergent natural selection related to differential resource use. In contrast, the role of ecological forces in favoring and maintaining reproductive isolation in nature remains poorly understood. If the same forces driving phenotypic divergence are also responsible for speciation, one would predict a correlation between the extent of trophic specialization (reflecting variable intensity of divergent natural selection) and that of reproductive isolation being reached in a given environment. We tested this hypothesis by comparing the extent of morphological and genetic differentiation between sympatric dwarf and normal whitefish ecotypes (Coregonus sp.) from six lakes of the St. John River basin (eastern Canada and northern Maine). Eight meristic variables, 19 morphometric variables, and six microsatellite loci were used to quantify morphological and genetic differentiation, respectively. Dwarf and normal ecotypes in each lake differed primarily by traits related to trophic specialization, but the extent of differentiation varied among lakes. Significant but variable genetic divergence between ecotypes within lakes was also observed. A negative correlation was observed between the extent of gene flow between ecotypes within a lake and that of their morphological differentiation in trophic-related traits. The extent of reproductive isolation reached between dwarf and normal whitefish ecotypes appears to be driven by the potential for occupying distinct trophic niches and, thus, by the same selective forces driving tropic specialization in each lake. These results therefore support the hypothesis of ecological speciation.     

Social selection parapatry in Afrotropical sunbirds

The extent of range overlap of incipient and recent species depends on the type and magnitude of phenotypic divergence that separates them, and the consequences of phenotypic divergence on their interactions. Signal divergence by social selection likely initiates many speciation events, but may yield niche‐conserved lineages predisposed to limit each others’ ranges via ecological competition. Here, we examine this neglected aspect of social selection speciation theory in relation to the discovery of a nonecotonal species border between sunbirds. We find that Nectarinia moreaui and Nectarinia fuelleborni meet in a ～6 km wide contact zone, as estimated by molecular cline analysis. These species exploit similar bioclimatic niches, but sing highly divergent learned songs, consistent with divergence by social selection. Cline analyses suggest that within‐species stabilizing social selection on song‐learning predispositions maintains species differences in song despite both hybridization and cultural transmission. We conclude that ecological competition between moreaui and fuelleborni contributes to the stabilization of the species border, but that ecological competition acts in conjunction with reproductive interference. The evolutionary maintenance of learned song differences in a hybrid zone recommend this study system for future studies on the mechanisms of learned song divergence and its role in speciation.     

Effects of dispersal plasticity on population divergence and speciation

Phenotypic plasticity is thought to have a role in driving population establishment, local adaptation and speciation. However, dispersal plasticity has been underappreciated in this literature. Plasticity in the decision to disperse is taxonomically widespread and I provide examples for insects, molluscs, polychaetes, vertebrates and flowering plants. Theoretical work is limited but indicates an interaction between dispersal distance and plasticity in the decision to disperse. When dispersal is confined to adjacent patches, dispersal plasticity may enhance local adaptation over unconditional (non-plastic) dispersal. However, when dispersal distances are greater, plasticity in dispersal decisions strongly reduces the potential for local adaptation and population divergence. Upon dispersal, settlement may be random, biased but genetically determined, or biased but plastically determined. Theory shows that biased settlement of either type increases population divergence over random settlement. One model suggests that plasticity further enhances chances of speciation. However, there are many strategies for deciding on where to settle such as a best-of-N strategy, sequential sampling with a threshold for acceptance or matching with natal habitat. To date, these strategies do not seem to have been compared within a single model. Although we are just beginning to explore evolutionary effects of dispersal plasticity, it clearly has the potential to enhance as well as inhibit population divergence. Additional work should pay particular attention to dispersal distance and the strategy used to decide on where to settle.     

Synergistic selection between ecological niche and mate preference primes diversification

The ecological niche and mate preferences have independently been shown to be important for the process of speciation. Here, we articulate a novel mechanism by which ecological niche use and mate preference can be linked to promote speciation. The degree to which individual niches are narrow and clustered affects the strength of divergent natural selection and population splitting. Similarly, the degree to which individual mate preferences are narrow and clustered affects the strength of divergent sexual selection and assortative mating between diverging forms. This novel perspective is inspired by the literature on ecological niches; it also explores mate preferences and how they may contribute to speciation. Unlike much comparative work, we do not search for evolutionary patterns using proxies for adaptation and sexual selection, but rather we elucidate how ideas from niche theory relate to mate preference, and how this relationship can foster speciation. Recognizing that individual and population niches are conceptually and ecologically linked to individual and population mate preference functions will significantly increase our understanding of rapid evolutionary diversification in nature. It has potential to help solve the difficult challenge of testing the role of sexual selection in the speciation process. We also identify ecological factors that are likely to affect individual niche and individual mate preference in synergistic ways and as a consequence to promote speciation. The ecological niche an individual occupies can directly affect its mate preference. Clusters of individuals with narrow, differentiated niches are likely to have narrow, differentiated mate preference functions. Our approach integrates ecological and sexual selection research to further our understanding of diversification processes. Such integration may be necessary for progress because these processes seem inextricably linked in the natural world.     

The consequences of phenotypic plasticity for ecological speciation

We use an individual-based numerical simulation to study the effects of phenotypic plasticity on ecological speciation. We find that adaptive plasticity evolves readily in the presence of dispersal between populations from different ecological environments. This plasticity promotes the colonization of new environments but reduces genetic divergence between them. We also find that the evolution of plasticity can either enhance or degrade the potential for divergent selection to form reproductive barriers. Of particular importance here is the timing of plasticity in relation to the timing of dispersal. If plasticity is expressed after dispersal, reproductive barriers are generally weaker because plasticity allows migrants to be better suited for their new environment. If plasticity is expressed before dispersal, reproductive barriers are either unaffected or enhanced. Among the potential reproductive barriers we considered, natural selection against migrants was the most important, primarily because it was the earliest-acting barrier. Accordingly, plasticity had a much greater effect on natural selection against migrants than on sexual selection against migrants or on natural and sexual selection against hybrids. In general, phenotypic plasticity can strongly alter the process of ecological speciation and should be considered when studying the evolution of reproductive barriers.     

Detecting local diversity‐dependence in diversification

Whether there are ecological limits to species diversification is a hotly debated topic. Molecular phylogenies show slowdowns in lineage accumulation, suggesting that speciation rates decline with increasing diversity. A maximum‐likelihood (ML) method to detect diversity‐dependent (DD) diversification from phylogenetic branching times exists, but it assumes that diversity‐dependence is a global phenomenon and therefore ignores that the underlying species interactions are mostly local, and not all species in the phylogeny co‐occur locally. Here, we explore whether this ML method based on the nonspatial diversity‐dependence model can detect local diversity‐dependence, by applying it to phylogenies, simulated with a spatial stochastic model of local DD speciation, extinction, and dispersal between two local communities. We find that type I errors (falsely detecting diversity‐dependence) are low, and the power to detect diversity‐dependence is high when dispersal rates are not too low. Interestingly, when dispersal is high the power to detect diversity‐dependence is even higher than in the nonspatial model. Moreover, estimates of intrinsic speciation rate, extinction rate, and ecological limit strongly depend on dispersal rate. We conclude that the nonspatial DD approach can be used to detect diversity‐dependence in clades of species that live in not too disconnected areas, but parameter estimates must be interpreted cautiously.     

Speciation accelerated and stabilized by pleiotropic major histocompatibility complex immunogenes

Speciation and the maintenance of recently diverged species has been subject of intense research in evolutionary biology for decades. Although the concept of ecological speciation has been accepted, its mechanisms and genetic bases are still under investigation. Here, we present a mechanism for speciation that is orchestrated and strengthened by parasite communities acting on polymorphic genes of the immune system. In vertebrates, these genes have a pleiotropic role with regard to parasite resistance and mate choice. In contrasting niches, parasite communities differ and thus the pools of alleles of the adapted major histocompatibility complex (MHC) also differ between niches. Mate choice for the best-adapted MHC genotype will favour local adaptations and will accelerate separation of both populations: thus immune genes act as pleiotropic speciation genes –'magic traits'. This mechanism should operate not only in sympatric populations but also under allopatry or parapatry. Each individual has a small subset of the many MHC alleles present in the population. If all individuals could have all MHC alleles from the pool, MHC-based adaptation is neither necessary nor possible. However, the typically small optimal individual number of MHC loci thus enables MHC-based speciation. Furthermore, we propose a new mechanism selecting against species hybrids. Hybrids are expected to have super-optimal individual MHC diversity and should therefore suffer more from parasites in all habitats.