The effect of habitat on modern shark diversification

Sharks occupy marine habitats ranging from shallow, inshore environments to pelagic, and deepwaters, and thus provide a model system for testing how gross habitat differences have shaped vertebrate macroevolution. Palaeontological studies have shown that onshore lineages diversify more quickly than offshore taxa. Among onshore habitats, coral reef‐association has been shown to increase speciation rates in several groups of fishes and invertebrates. In this study, we investigated whether speciation rates are habitat dependent by generating the first comprehensive molecular timescale for shark divergence. Using phylogenetic comparative methods, we rejected the hypothesis that shelf (i.e. onshore) lineages have higher speciation rates compared to those occupying deepwater and oceanic (i.e. offshore) habitats. Our results, however, support the hypothesis of increased speciation rates in coral reef‐associated lineages within the Carcharhinidae. Our new timetree suggests that the two major shark lineages leading to the extant shark diversity began diversifying mostly after the end‐Permian mass extinction: the squalimorphs into deepwater and the galeomorphs into shelf habitats. We suggest that the breakdown of the onshore–offshore speciation rate pattern in sharks is mediated by success in deepwater environments through ecological partitioning, and in some cases, the evolution of morphological novelty.     

Speciation: more likely through a genetic or through a learned habitat preference?

A problem in understanding sympatric speciation is establishing how reproductive isolation can arise when there is disruptive selection on an ecological trait. One of the solutions that has been proposed is that a habitat preference evolves, and that mates are chosen within the preferred habitat. We present a model where the habitat preference can evolve either by means of a genetic mechanism or by means of learning. Employing an adaptive-dynamical analysis, we show that evolution proceeds either to a single population of specialists with a genetic preference for their optimal habitat, or to a population of generalists without a habitat preference. The generalist population subsequently experiences disruptive selection. Learning promotes speciation because it increases the intensity of disruptive selection. An individual-based version of the model shows that, when loci are completely unlinked and learning confers little cost, the presence of disruptive selection most probably leads to speciation via the simultaneous evolution of a learned habitat preference. For high costs of learning, speciation is most likely to occur via the evolution of a genetic habitat preference. However, the latter only happens when the effect of mutations is large, or when there is linkage between genes coding for the different traits.     

Speciation rates are correlated with changes in plumage color complexity in the largest family of songbirds

Although evolutionary theory predicts an association between the evolution of elaborate ornamentation and speciation, empirical evidence for links between speciation and ornament evolution has been mixed. In birds, the evolution of increasingly complex and colorful plumage may promote speciation by introducing prezygotic mating barriers. However, overall changes in color complexity, including both increases and decreases, may also promote speciation by altering the sexual signals that mediate reproductive choices. Here, we examine the relationship between complex plumage and speciation rates in the largest family of songbirds, the tanagers (Thraupidae). First, we test whether species with more complex plumage coloration are associated with higher speciation rates and find no correlation. We then test whether rates of male or female plumage color complexity evolution are correlated with speciation rates. We find that elevated rates of plumage complexity evolution are associated with higher speciation rates, regardless of sex and whether species are evolving more complex or less complex ornamentation. These results extend to whole-plumage color complexity and regions important in signaling (crown and throat) but not nonsignaling regions (back and wingtip). Our results suggest that the extent of change in plumage traits, rather than overall values of plumage complexity, may play a role in speciation.     

Dispersal is associated with morphological innovation,but not increased diversification,in Cyphostemma (Vitaceae)

Multiple processes − including dispersal, morphological innovation, and habitat change − are frequently cited as catalysts for increased diversification. We investigate these processes and the causal linkages among them in the genus Cyphostemma (Vitaceae), a clade comprising ∼200 species that is unique in the Vitaceae for its diversity of growth habits. We reconstruct time‐calibrated evolutionary relationships among 64 species in the genus using five nuclear and chloroplast markers and infer the group's morphological and biogeographic history. We test for changes in speciation rate and evaluate the temporal association and sequencing of events with respect to dispersal, habitat change, and morphological evolution using a Monte Carlo simulation approach. In Cyphostemma, neither dispersal nor morphological evolution is associated with shifts in speciation rate, but dispersal is associated with evolutionary shifts in growth form. Evolution of stem succulence, in particular, is associated with adaptation to local, pre‐existing conditions following long‐distance dispersal, not habitat change in situ. We suggest that the pattern of association between dispersal, morphological innovation, and diversification may depend on the particular characters under study. Lineages with evolutionarily labile characters, such as stem succulence, do not necessarily conform to the notion of niche conservatism and instead demonstrate remarkable morphological adaptation to local climate and edaphic conditions following dispersal.     

Tracing the first step to speciation: ecological and genetic differentiation of a salamander population in a small forest

Mechanisms and processes of ecologically driven adaptive speciation are best studied in natural situations where the splitting process is still occurring, i.e. before complete reproductive isolation is achieved. Here, we present a case of an early stage of adaptive differentiation under sympatric conditions in the fire salamander, Salamandra salamandra, that allows inferring the underlying processes for the split. Larvae of S. salamandra normally mature in small streams until metamorphosis, but in an old, continuous forest area near Bonn (the Kottenforst), we found salamander larvae not only in small streams but also in shallow ponds, which are ecologically very different from small streams. Common-environment experiments with larvae from both habitat types reveal specific adaptations to these different ecological conditions. Mitochondrial and microsatellite analyses show that the two ecologically differentiated groups also show signs of genetic differentiation. A parallel analysis of animals from a neighbouring much larger forest area (the Eifel), in which larvae mature only in streams, shows no signs of genetic differentiation, indicating that gene flow between ecologically similar types can occur over large distances. Hence, geographical factors cannot explain the differential larval habitat adaptations in the Kottenforst, in particular since adult life and mating of S. salamandra is strictly terrestrial and not associated with larval habitats. We propose therefore that the evolution of these adaptations was coupled with the evolution of cues for assortative mating which would be in line with models of sympatric speciation that suggest a co-evolution of habitat adaptations and associated mating signals.     

Speciation with gene flow in a heterogeneous virtual world: can physical obstacles accelerate speciation?

The origin of species remains one of the most controversial and least understood topics in evolution. While it is being widely accepted that complete cessation of gene-flow between populations owing to long-lasting geographical barriers results in a steady, irreversible increase of divergence and eventually speciation, the extent to which various degrees of habitat heterogeneity influences speciation rates is less well understood. Here, we investigate how small, randomly distributed physical obstacles influence the distribution of populations and species, the level of population connectivity (e.g. gene flow), as well as the mode and tempo of speciation in a virtual ecosystem composed of prey and predator species. We adapted an existing individual-based platform, EcoSim, to allow fine tuning of the gene flow's level between populations by adding various numbers of obstacles in the world. The platform implements a simple food chain consisting of primary producers, herbivores (prey) and predators. It allows complex intra- and inter-specific interactions, based on individual evolving behavioural models, as well as complex predator-prey dynamics and coevolution in spatially homogenous and heterogeneous worlds. We observed a direct and continuous increase in the speed of evolution (e.g. the rate of speciation) with the increasing number of obstacles in the world. The spatial distribution of species was also more compact in the world with obstacles than in the world without obstacles. Our results suggest that environmental heterogeneity and other factors affecting demographic stochasticity can directly influence speciation and extinction rates.     

Song evolution,speciation, and vocal learning in passerine birds

Phenotypic divergence can promote reproductive isolation and speciation, suggesting a possible link between rates of phenotypic evolution and the tempo of speciation at multiple evolutionary scales. To date, most macroevolutionary studies of diversification have focused on morphological traits, whereas behavioral traits─including vocal signals─are rarely considered. Thus, although behavioral traits often mediate mate choice and gene flow, we have a limited understanding of how behavioral evolution contributes to diversification. Furthermore, the developmental mode by which behavioral traits are acquired may affect rates of behavioral evolution, although this hypothesis is seldom tested in a phylogenetic framework. Here, we examine evidence for rate shifts in vocal evolution and speciation across two major radiations of codistributed passerines: one oscine clade with learned songs (Thraupidae) and one suboscine clade with innate songs (Furnariidae). We find that evolutionary bursts in rates of speciation and song evolution are coincident in both thraupids and furnariids. Further, overall rates of vocal evolution are higher among taxa with learned rather than innate songs. Taken together, these findings suggest an association between macroevolutionary bursts in speciation and vocal evolution, and that the tempo of behavioral evolution can be influenced by variation in developmental modes among lineages.     

Demographic processes shaping genetic variation

Demographic processes modulate genome-wide levels and patterns of genetic variation via impacting effective population size independently of natural selection. Such processes include the perturbation of population distributions from external events shaping habitat landscape and internal factors shaping the probability of contemporaneous alleles in a population (coalescence). Several patterns have recently emerged: spatial and temporal heterogeneity in population structure have different influences on the persistence of new mutations and genetic variation, multi-locus analyses indicate that gene flow continues to occur during speciation and the incorporation of demographic processes into models of molecular evolution and association genetics approaches has improved statistical power to detect deviations from neutral-equilibrium expectations and decreased false positive rates.     

No ecological opportunity signal on a continental scale? Diversification and life‐history evolution of African true toads (Anura: Bufonidae)

The niche‐filling process predicted by the “ecological opportunity” (EO) model is an often‐invoked mechanism for generating exceptional diversity in island colonizers. Whether the same process governs lineage accumulation and trait disparity during continental colonization events is less clear. Here, we test this prediction by investigating the rate dynamics and trait evolution of one of Africa's most widespread amphibian colonizers, the true toads (Bufonidae). By reconstructing the most complete molecular phylogeny of African Bufonidae to date, we find that the diversification of lineages in Africa best conforms to a constant rate model throughout time and across subclades, with little support for EO. Evolutionary rates of life‐history traits have similarly been constant over time. However, an analysis of generalists and specialists showed a shift toward higher speciation rates associated with habitat specialization. The overall lack of EO signal can be interpreted in a number of ways and we propose several explanations. Firstly, methodological issues might preclude the detection of EO. Secondly, colonizers might not experience true EO conditions and due to the size, ecological heterogeneity and age of landmasses, the diversification processes might be more complex. Thirdly, lower speciation rates of habitat generalists may have affected overall proliferation of lineages.     

Early burst in body size evolution is uncoupled from species diversification in diving beetles (Dytiscidae)

Changes in morphology are often thought to be linked to changes in species diversification, which is expected to leave a signal of early burst (EB) in phenotypic traits. However, such signal is rarely recovered in empirical phylogenies, even for groups with well‐known adaptive radiation. Using a comprehensive phylogenetic approach in Dytiscidae, which harbours ~4,300 species with as much as 50‐fold variation in body size among them, we ask whether pattern of species diversification correlates with morphological evolution. Additionally, we test whether the large variation in body size is linked to habitat preference and whether the latter influences species turnover. We found, in sharp contrast to most animal groups, that Dytiscidae body size evolution follows an early‐burst model with subsequent high phylogenetic conservatism. However, we found no evidence for associated shifts in species diversification, which point to an uncoupled evolution of morphology and species diversification. We recovered the ancestral habitat of Dytiscidae as lentic (standing water), with many transitions to lotic habitat (running water) that are concomitant to a decrease in body size. Finally, we found no evidence for difference in net diversification rates between habitats nor difference in turnover in lentic and lotic species. This result, together with recent findings in dragonflies, contrasts with some theoretical expectations of the habitat stability hypothesis. Thus, a thorough reassessment of the impact of dispersal, gene flow and range size on the speciation process is needed to fully encompass the evolutionary consequences of the lentic–lotic divide for freshwater fauna.     

Evolutionary bottlenecks in brackish water habitats drive the colonization of fresh water by stingrays

Species richness in freshwater bony fishes depends on two main processes: the transition into and the diversification within freshwater habitats. In contrast to bony fishes, only few cartilaginous fishes, mostly stingrays (Myliobatoidei), were able to colonize fresh water. Respective transition processes have been mainly assessed from a physiological and morphological perspective, indicating that the freshwater lifestyle is strongly limited by the ability to perform osmoregulatory adaptations. However, the transition history and the effect of physiological constraints on the diversification in stingrays remain poorly understood. Herein, we estimated the geographic pathways of freshwater colonization and inferred the mode of habitat transitions. Further, we assessed habitat‐related speciation rates in a time‐calibrated phylogenetic framework to understand factors driving the transition of stingrays into and the diversification within fresh water. Using South American and Southeast Asian freshwater taxa as model organisms, we found one independent freshwater colonization event by stingrays in South America and at least three in Southeast Asia. We revealed that vicariant processes most likely caused freshwater transition during the time of major marine incursions. The habitat transition rates indicate that brackish water species switch preferably back into marine than forth into freshwater habitats. Moreover, our results showed significantly lower diversification rates in brackish water lineages, whereas freshwater and marine lineages exhibit similar rates. Thus, brackish water habitats may have functioned as evolutionary bottlenecks for the colonization of fresh water by stingrays, probably because of the higher variability of environmental conditions in brackish water.     

The shape and temporal dynamics of phylogenetic trees arising from geographic speciation

Phylogenetic trees often depart from the expectations of stochastic models, exhibiting imbalance in diversification among lineages and slowdowns in the rate of lineage accumulation through time. Such departures have led to a widespread perception that ecological differences among species or adaptation and subsequent niche filling are required to explain patterns of diversification. However, a key element missing from models of diversification is the geographical context of speciation and extinction. In this study, we develop a spatially explicit model of geographic range evolution and cladogenesis, where speciation arises via vicariance or peripatry, and explore the effects of these processes on patterns of diversification. We compare the results with those observed in 41 reconstructed avian trees. Our model shows that nonconstant rates of speciation and extinction are emergent properties of the apportioning of geographic ranges that accompanies speciation. The dynamics of diversification exhibit wide variation, depending on the mode of speciation, tendency for range expansion, and rate of range evolution. By varying these parameters, the model is able to capture many, but not all, of the features exhibited by birth-death trees and extant bird clades. Under scenarios with relatively stable geographic ranges, strong slowdowns in diversification rates are produced, with faster rates of range dynamics leading to constant or accelerating rates of apparent diversification. A peripatric model of speciation with stable ranges also generates highly unbalanced trees typical of bird phylogenies but fails to produce realistic range size distributions among the extant species. Results most similar to those of a birth-death process are reached under a peripatric speciation scenario with highly volatile range dynamics. Taken together, our results demonstrate that considering the geographical context of speciation and extinction provides a more conservative null model of diversification and offers a very different perspective on the phylogenetic patterns expected in the absence of ecology.     

Testing the link between the latitudinal gradient in species richness and rates of molecular evolution

Numerous hypotheses have been proposed to explain latitudinal gradients in species richness, but all are subject to ongoing debate. Here we examine Rohde's (1978, 1992) hypothesis, which proposes that climatic conditions at low latitudes lead to elevated rates of speciation. This hypothesis predicts that rates of molecular evolution should increase towards lower latitudes, but this prediction has never been tested. We discuss potential links between rates of molecular evolution and latitudinal diversity gradients, and present the first test of latitudinal variation in rates of molecular evolution. Using 45 phylogenetically independent, latitudinally separated pairs of bird species and higher taxa, we compare rates of evolution of two mitochondrial genes and DNA-DNA hybridization distances. We find no support for an effect of latitude on rate of molecular evolution. This result casts doubt on the generality of a key component of Rohde's hypothesis linking climate and speciation.     

Environmental harshness is positively correlated with intraspecific divergence in mammals and birds

Life on Earth is conspicuously more diverse in the tropics. Although this intriguing geographical pattern has been linked to many biotic and abiotic factors, their relative importance and potential interactions are still poorly understood. The way in which latitudinal changes in ecological conditions influence evolutionary processes is particularly controversial, as there is evidence for both a positive and a negative latitudinal gradient in speciation rates. Here, we identify and address some methodological issues (how patterns are analysed and how latitude is quantified) that could lead to such conflicting results. To address these issues, we assemble a comprehensive data set of the environmental correlates of latitude (including climate, net primary productivity and habitat heterogeneity) and combine it with biological, historical and molecular data to explore global patterns in recent divergence events (subspeciation). Surprisingly, we find that the harsher conditions that typify temperate habitats (lower primary productivity, decreased rainfall and more variable and unpredictable temperatures) are positively correlated with greater subspecies richness in terrestrial mammals and birds. Thus, our findings indicate that intraspecific divergence is greater in regions with lower biodiversity, a pattern that is robust to both sampling variation and latitudinal biases in taxonomic knowledge. We discuss possible causal mechanisms for the link between environmental harshness and subspecies richness (faster rates of evolution, greater likelihood of range discontinuities and more opportunities for divergence) and conclude that this pattern supports recent indications that latitudinal gradients of diversity are maintained by simultaneously higher potentials for both speciation and extinction in temperate than tropical regions.     

Habitat light and dewlap color diversity in four species of Puerto Rican anoline lizards

Closely related species often have signals that differ dramatically in design. The evolution of such differences may be important in the process of speciation. Selection for signal detectability under different habitat conditions has been proposed as a mechanism leading to the evolution of signal diversity. We examined dewlap color in four closely related species of Anolis lizards that occupy habitats with different light conditions. Initially, we tested the hypothesis that lizards choose specific light conditions within each habitat in which to signal. We rejected this hypothesis for all four species. We next calculated the detectability of the dewlap color of all four species at display locations in each habitat. If selection for detectability under the different light conditions explained the divergence in signal design, the occupant of a given habitat was predicted to have the highest signal detectability in that habitat. However, the rank order of detectability of the four dewlap colors was nearly the same in all four habitats. We concluded that divergent selection for signal detectability does not, by itself, explain the evolution of dewlap color diversity. We hypothesize that the evolution of dewlap color diversity results from simultaneous selection for multiple functions of dewlap color.     

Environmental predictors of global parrot (Aves: Psittaciformes) species richness and phylogenetic diversity

Aim Spatial patterns of phylogenetic diversity (PD) aid our ability to discern diversification rate mechanisms underlying hypotheses for the large‐scale distribution of biodiversity. We develop a predictive framework for the way in which spatial patterns of PD vary with those of species richness, depending on the balance between speciation and extinction rates. Within this framework, diversification processes thought to underlie the productive energy, ambient energy, topographic variability and habitat variety hypotheses predict that gradients of increase in species richness will be associated with: (1) decreasing extinction rates where driven by productive energy, hence increasing relative PD (i.e. PD controlling for species richness, or PD_rel); (2) a similar positive relationship between ambient energy and PD_rel; (3) increasing speciation rates where driven by topographic variability, hence decreasing PD_rel; and (4) no consistent relationship between PD_rel and habitat variety when driven by the latter. We test these predictions using distributional data on parrots. Location Neotropical, Afrotropical, Indo‐Malayan and Australasian realms. Methods Spatial models were used to test the predictions. Results Globally, a positive association between productive energy and PD_rel confirms prediction (1). However, within realms, hump‐shaped relationships suggest the importance of decreasing extinction rates up to a threshold level of productive energy, and the increasing importance of speciation rates thereafter. Ambient energy is positively associated with PD_rel in Australasia, Indo‐Malaya, and globally, supporting prediction (2). However, this is driven by the coincidence of highest PD_rel in areas of high ambient energy and intermediate productive energy (i.e. in seasonal tropical environments), which may be characterized by relatively low speciation and extinction rates. In the Neotropics, increasing topographic variability is associated with decreasing PD_rel and increasing species richness, suggesting an increasing gradient of speciation, supporting prediction (3). Elsewhere, the signal of this mechanism may be obscured by collinearities with energy gradients. The lack of an overall relationship between habitat diversity and PD_rel confirms prediction (4). Main conclusions Spatial patterns of PD_rel in relation to environmental gradients may be sensitive to collinearities among those gradients. Nevertheless, patterns emerge which have implications for the relative importance of speciation and extinction processes in generating latitudinal diversity gradients.     

Habitat type predicts genetic population differentiation in freshwater invertebrates

A basic challenge in evolutionary biology is to establish links between ecology and evolution of species. One important link is the habitat template. It has been hypothesized, that the spatial and temporal settings of a habitat strongly influence the evolution of species dispersal propensity. Here, we evaluate the importance of the habitat type on genetic population differentiation of species using freshwater habitats as a model system. Freshwater habitats are either lentic (standing) or lotic (running). On average, lotic habitats are more stable and predictable over space and time than lentic habitats. Therefore, lentic habitats should favour the evolution of higher dispersal propensity which ensures population survival of lentic species. To test for such a relationship, we used extensive data on species' genetic population differentiation of lentic and lotic freshwater invertebrates retrieved from published allozyme studies. Overall, we analysed more than 150 species from all over the world. Controlling for several experimental, biological and geographical confounding effects, we always found that lentic invertebrates exhibit, on average, lower genetic population differentiation than lotic species. This pattern was consistent across insects, crustaceans and molluscs. Our results imply fundamental differences in genetic population differentiation among species adapted to either lentic or lotic habitats. We propose that such differences should occur in a number of other habitat types that differ in spatio-temporal stability. Furthermore, our results highlight the important role of lotic habitats as reservoirs for evolutionary processes and the potential for rapid speciation.     

VARIABLE PROGRESS TOWARD ECOLOGICAL SPECIATION IN PARAPATRY: STICKLEBACK ACROSS EIGHT LAKE-STREAM TRANSITIONS

Divergent selection between contrasting habitats can sometimes drive adaptive divergence and the evolution of reproductive isolation in the face of initially high gene flow. "Progress" along this ecological speciation pathway can range from minimal divergence to full speciation. We examine this variation for threespine stickleback fish that evolved independently across eight lake-stream habitat transitions. By quantifying stickleback diets, we show that lake-stream transitions usually coincide with limnetic-benthic ecotones. By measuring genetically based phenotypes, we show that these ecotones often generate adaptive divergence in foraging morphology. By analyzing neutral genetic markers (microsatellites), we show that adaptive divergence is often associated with the presence of two populations maintaining at least partial reproductive isolation in parapatry. Coalescent-based simulations further suggest that these populations have diverged with gene flow within a few thousand generations, although we cannot rule out the possibility of phases of allopatric divergence. Finally, we find striking variation among the eight lake-stream transitions in progress toward ecological speciation. This variation allows us to hypothesize that progress is generally promoted by strong divergent selection and limited dispersal across the habitat transitions. Our study thus makes a case for ecological speciation in a parapatric context, while also highlighting variation in the outcome.     

Linking the investigations of character evolution and species diversification

Variation in diversification rates is often studied by investigating traits related to species' ecology and life history. Often, however, it is unknown whether these traits evolve gradually or in punctuated bursts during speciation. Using phylogenetic data and species' present-day trait information, we present a novel approach to assessing the mode of character change while accounting for trait-dependent speciation and extinction. Our model, "Binary-State Speciation and Extinction-node enhanced state shift" (BiSSE-ness), estimates both the rate of change occurring along lineages and the probability of change occurring during speciation, as well as independent speciation and extinction rates for each character state. Using simulations, we found that BiSSE-ness is able to distinguish along-lineage and speciational change and accurately estimate the parameters associated with character change and diversification rates. We applied BiSSE-ness to an empirical primate data set and found evidence for along-lineage changes in primate mating systems and social behaviors, whereas shifts in habitat were associated with speciation. In cases where trait changes may be linked to the speciation process itself (e.g., niche-related traits), BiSSE-ness provides a suitable framework with which to simultaneously address questions regarding species diversification and character change.     

The geography and ecology of plant speciation: range overlap and niche divergence in sister species

A goal of evolutionary biology is to understand the roles of geography and ecology in speciation. The recent shared ancestry of sister species can leave a major imprint on their geographical and ecological attributes, possibly revealing processes involved in speciation. We examined how ecological similarity, range overlap and range asymmetry are related to time since divergence of 71 sister species pairs in the California Floristic Province (CFP). We found that plants exhibit strikingly different age-range correlation patterns from those found for animals; the latter broadly support allopatric speciation as the primary mode of speciation. By contrast, plant sisters in the CFP were sympatric in 80% of cases and range sizes of sisters differed by a mean of 10-fold. Range overlap and range asymmetry were greatest in younger sisters. These results suggest that speciation mechanisms broadly grouped under ‘budding’ speciation, in which a larger ranged progenitor gives rise to a smaller ranged derivative species, are probably common. The ecological and reproductive similarity of sisters was significantly greater than that of sister–non-sister congeners for every trait assessed. However, shifts in at least one trait were present in 93% of the sister pairs; habitat and soil shifts were especially common. Ecological divergence did not increase with range overlap contrary to expectations under character displacement in sympatry. Our results suggest that vicariant speciation is more ubiquitous in animals than plants, perhaps owing to the sensitivity of plants to fine-scale environmental heterogeneity. Despite high levels of range overlap, ecological shifts in the process of budding speciation may result in low rates of fine-scale spatial co-occurrence. These results have implications for ecological studies of trait evolution and community assembly; despite high levels of sympatry, sister taxa and potentially other close relatives, may be missing from local communities.