The cryptic origins of evolutionary novelty: 1000‐fold faster trophic diversification rates without increased ecological opportunity or hybrid swarm

Ecological opportunity is frequently proposed as the sole ingredient for adaptive radiation into novel niches. An additional trigger may be genome‐wide hybridization resulting from “hybrid swarm.” However, these hypotheses have been difficult to test due to the rarity of comparable control environments lacking adaptive radiations. Here I exploit such a pattern in microendemic radiations of Caribbean pupfishes. I show that a sympatric three species radiation on San Salvador Island, Bahamas diversified 1445 times faster than neighboring islands in jaw length due to the evolution of a novel scale‐eating adaptive zone from a generalist ancestral niche. I then sampled 22 generalist populations on seven neighboring islands and measured morphological diversity, stomach content diversity, dietary isotopic diversity, genetic diversity, lake/island areas, macroalgae richness, and Caribbean‐wide patterns of gene flow. None of these standard metrics of ecological opportunity or gene flow were associated with adaptive radiation, except for slight increases in macroalgae richness. Thus, exceptional trophic diversification is highly localized despite myriad generalist populations in comparable environmental and genetic backgrounds. This study provides a strong counterexample to the ecological and hybrid swarm theories of adaptive radiation and suggests that diversification of novel specialists on a sparse fitness landscape is constrained by more than ecological opportunity and gene flow.     

Allopatric distribution and diversification without niche shift in a bryophyte-feeding basal moth lineage (Lepidoptera: Micropterigidae)

The Lepidoptera represent one of the most successful radiations of plant-feeding insects, which predominantly took place within angiosperms beginning in the Cretaceous period. Angiosperm colonization is thought to underlie the evolutionary success of the Lepidoptera because angiosperms provide an enormous range of niches for ecological speciation to take place. By contrast, the basal lepidopteran lineage, Micropterigidae, remained unassociated with angiosperms since Jurassic times but nevertheless achieved a modest diversity in the Japanese Archipelago. We explored the causes and processes of diversification of the Japanese micropterigid moths by performing molecular phylogenetic analysis and extensive ecological surveying. Phylogenetic analysis recovered a monophyletic group of approximately 25 East Asian endemic species that feed exclusively on the liverwort Conocephalum conicum, suggesting that niche shifts hardly played a role in their diversification. Consistent with the low flying ability of micropterigid moths, the distributions of the Conocephalum specialists are each localized and allopatric, indicating that speciation by geographical isolation has been the major process shaping the diversity of Japanese Micropterigidae. To our knowledge, this is the largest radiation of herbivorous insects that does not accompany any apparent niche differentiation. We suggest that the significance of non-ecological speciation during the diversification of the Lepidoptera is commonly underestimated.     

Climatic Niche Dynamics and Its Role in the Insular Endemism of <Emphasis Type="Italic">Anolis</Emphasis> Lizards

Insular systems are usually characterized by have a high species diversity, endemism, and evolutionary uniqueness. Although ecological and evolutionary factors shaping insular diversity and endemism are relatively well established, there is a little understanding about climatic niche dynamics for many insular adaptive radiations. Here, we evaluate the tempo and mode of climatic niche evolution in an iconic insular radiation of lizards. By using an extensive dataset of phylogenetic and coarse-grain climatic niches, we evaluated phylogenetic niche divergence and niche conservatism across temporal and spatial scales in the Caribbean Anolis lizard radiation. We found several instances of niche shifts during the anole radiation across islands. Many of these niche shifts converged to similar climatic regimes between different islands. Furthermore, we find evidence that single-island endemic species are more limited by low suitability of climatic conditions outside its native islands than oceanic barriers due to the high climatic heterogeneity observed at least between Greater Antillean islands. These results suggest that within-lineage climatic niche conservatism has been prevalent in short time scales and likely played a role driving the exceptional insular endemism observed today.     

Trophic novelty is linked to exceptional rates of morphological diversification in two adaptive radiations of Cyprinodon pupfish

Adaptive radiations are known for rapid morphological and species diversification in response to ecological opportunity, but it remains unclear if distinct mechanisms drive this pattern. Here, we show that rapid rates of morphological diversification are linked to the evolution of novel ecological niches in two independent Cyprinodon radiations nested within a wide-ranging group repeatedly isolated in extreme environments. We constructed a molecular phylogeny for the Cyprinodontidae, measured 16 functional traits across this group, and compared the likelihoods of single or multiple rates of morphological diversification. We found that rates of morphological diversification within two sympatric Cyprinodon clades containing unique trophic specialists are not part of an adaptive continuum with other clades, but are instead extreme outliers with rates up to 131 times faster than other Cyprinodontidae. High rates were not explained by clade age, but were instead linked to unique trophic niches within Cyprinodon, including scale-eating, zooplanktivory, and piscivory. Furthermore, although both radiations occur in similar environments and have similar sister species, they each evolved unique trophic specialists and high rates of morphological diversification in different sets of traits. We propose that the invasion of novel ecological niches may be a key mechanism driving many classic examples of adaptive radiation.     

Rapid lineage accumulation in a non-adaptive radiation: phylogenetic analysis of diversification rates in eastern North American woodland salamanders (Plethodontidae: Plethodon)

Adaptive radiations have served as model systems for quantifying the build-up of species richness. Few studies have quantified the tempo of diversification in species-rich clades that contain negligible adaptive disparity, making the macroevolutionary consequences of different modes of evolutionary radiation difficult to assess. We use mitochondrial-DNA sequence data and recently developed phylogenetic methodologies to explore the tempo of diversification of eastern North American Plethodon, a species-rich clade of woodland salamanders exhibiting only limited phenotypic disparity. Lineage-through-time analysis reveals a high rate of lineage accumulation, 0.8 species per million years, occurring 11-8 million years ago in the P. glutinosus species group, followed by decreasing rates. This high rate of lineage accumulation is exceptional, comparable to the most rapid of adaptive radiations. In contrast to classic models of adaptive radiation where ecological niche divergence is linked to the origin of species, we propose that phylogenetic niche conservatism contributes to the rapid accumulation of P. glutinosus-group lineages by promoting vicariant isolation and multiplication of species across a spatially and temporally fluctuating environment. These closely related and ecologically similar lineages persist through long-periods of evolutionary time and form strong barriers to the geographic spread of their neighbours, producing a subsequent decline in lineage accumulation. Rapid diversification among lineages exhibiting long-term maintenance of their bioclimatic niche requirements is an under-appreciated phenomenon driving the build-up of species richness.     

Parallelism in adaptive radiations of experimental Escherichia coli populations

Adaptive radiations are major contributors to species diversity. Although the underlying mechanisms of adaptive radiations, specialization and trade‐offs, are relatively well understood, the tempo and repeatability of adaptive radiations remain elusive. Ecological specialization can occur through the expansion into novel niches or through partitioning of an existing niche. To test how the mode of resource specialization affects the tempo and repeatability of adaptive radiations, we selected replicate bacterial populations in environments that promoted the evolution of diversity either through niche expansion or through niche partitioning, and in a third low‐quality single‐resource environment, in which diversity was not expected to evolve. Colony size diversity evolved equally fast in environments that provided ecological opportunities regardless of the mode of resource specialization. In the low‐quality environments, diversity did not consistently evolve. We observed the largest fitness improvement in the low‐quality environment and the smallest the glucose‐limited environment. We did not observe a change in the rate of evolutionary change in either trait or environment, suggesting that the pool of beneficial mutations was not exhausted. Overall, the mode of resource specialization did not affect the tempo or repeatability of adaptive radiations. These results demonstrate the limitations of eco‐evolutionary feedbacks to affect evolutionary outcomes.     

Rates of Dinosaur Body Mass Evolution Indicate 170 Million Years of Sustained Ecological Innovation on the Avian Stem Lineage

Large-scale adaptive radiations might explain the runaway success of a minority of extant vertebrate clades. This hypothesis predicts, among other things, rapid rates of morphological evolution during the early history of major groups, as lineages invade disparate ecological niches. However, few studies of adaptive radiation have included deep time data, so the links between extant diversity and major extinct radiations are unclear. The intensively studied Mesozoic dinosaur record provides a model system for such investigation, representing an ecologically diverse group that dominated terrestrial ecosystems for 170 million years. Furthermore, with 10,000 species, extant dinosaurs (birds) are the most speciose living tetrapod clade. We assembled composite trees of 614–622 Mesozoic dinosaurs/birds, and a comprehensive body mass dataset using the scaling relationship of limb bone robustness. Maximum-likelihood modelling and the node height test reveal rapid evolutionary rates and a predominance of rapid shifts among size classes in early (Triassic) dinosaurs. This indicates an early burst niche-filling pattern and contrasts with previous studies that favoured gradualistic rates. Subsequently, rates declined in most lineages, which rarely exploited new ecological niches. However, feathered maniraptoran dinosaurs (including Mesozoic birds) sustained rapid evolution from at least the Middle Jurassic, suggesting that these taxa evaded the effects of niche saturation. This indicates that a long evolutionary history of continuing ecological innovation paved the way for a second great radiation of dinosaurs, in birds. We therefore demonstrate links between the predominantly extinct deep time adaptive radiation of non-avian dinosaurs and the phenomenal diversification of birds, via continuing rapid rates of evolution along the phylogenetic stem lineage. This raises the possibility that the uneven distribution of biodiversity results not just from large-scale extrapolation of the process of adaptive radiation in a few extant clades, but also from the maintenance of evolvability on vast time scales across the history of life, in key lineages.     

Macroevolutionary dynamics in environmental space and the latitudinal diversity gradient in New World birds

Correlations between species richness and climate suggest non-random occupation of environmental space and niche evolution through time. However, the evolutionary mechanisms involved remain unresolved. Here, we partition the occupation of environmental space into intra- and inter-clade components to differentiate a model based on pure conservation of ancestral niches with higher diversification rates in the tropics, and an adaptive radiation model based on shifts in adaptive peaks at the family level allowing occupation of temperate regions. We examined these mechanisms using within- and among-family skewness components based on centroids of 3560 New World bird species across four environmental variables. We found that the accumulation of species in the tropics is a result of both processes. The components of adaptive radiation have family level skewness of species' distributions strongly structured in space, but not phylogenetically, according to the integrated analyses of spatial filters and phylogenetic eigenvectors. Moreover, stronger radiation components were found for energy variables, which are often used to argue for direct climatic effects on diversity. Thus, the correspondence between diversity and climate may be due to the conservation of ancestral tropical niches coupled with repeated broad shifts in adaptive peaks during birds' evolutionary history more than by higher diversification rates driven by more energy in the tropics.     

Sexual dimorphism in an adaptive radiation: Does intersexual niche differentiation result in ecological character displacement?

Evolutionary radiations are one plausible explanation for the rich biodiversity on Earth. Adaptive radiations are the most studied form of evolutionary radiations, and ecological opportunity has been identified as one factor permitting them. Competition among individuals is supposedly highest in populations of conspecifics. Divergent modes of resource use might minimize trophic overlap, and thus intersexual competition, resulting in ecological character displacement between sexes. However, the role of intersexual differentiation in speciation processes is insufficiently studied. The few studies available suggest that intersexual niche differentiation exists in adaptive radiations, but their role within the radiation, and the extent of differentiation within the organism itself, remains largely unexplored. Here, we test the hypothesis that multiple morphological structures are affected by intersexual niche differentiation in “roundfin” Telmatherina, the first case where intersexual niche differentiation was demonstrated in an adaptive fish radiation. We show that sexes of two of the three morphospecies differ in several structural components of the head, all of these are likely adaptive. Sexual dimorphism is linked to the respective morphospecies‐specific ecology and affects several axes of variation. Trait variation translates into different feeding modes, processing types, and habitat usages that add to interspecific variation in all three morphospecies. Intrasexual selection, that is, male–male competition, may contribute to variation in some of the traits, but appears unlikely in internal structures, which are invisible to other individuals. We conclude that intersexual variation adds to the adaptive diversity of roundfins and might play a key role in minimizing intersexual competition in emerging radiations.     

Absence of phylogenetic signal in the niche structure of meadow plant communities

A significant proportion of the global diversity of flowering plants has evolved in recent geological time, probably through adaptive radiation into new niches. However, rapid evolution is at odds with recent research which has suggested that plant ecological traits, including the beta- (or habitat) niche, evolve only slowly. We have quantified traits that determine within-habitat alpha diversity (alpha niches) in two communities in which species segregate on hydrological gradients. Molecular phylogenetic analysis of these data shows practically no evidence of a correlation between the ecological and evolutionary distances separating species, indicating that hydrological alpha niches are evolutionarily labile. We propose that contrasting patterns of evolutionary conservatism for alpha- and beta-niches is a general phenomenon necessitated by the hierarchical filtering of species during community assembly. This determines that species must have similar beta niches in order to occupy the same habitat, but different alpha niches in order to coexist.     

Evolution of cranial shape in a continental‐scale evolutionary radiation of Australian lizards

A defining character of adaptive radiations is the evolution of a diversity of morphological forms that are associated with the use of different habitats, following the invasion of vacant niches. Island adaptive radiations have been thoroughly investigated but continental scale radiations are more poorly understood. Here, we use 52 species of Australian agamid lizards and their Asian relatives as a model group, and employ three‐dimensional geometric morphometrics to characterize cranial morphology and investigate whether variation in cranial shape reflects patterns expected from the ecological process of adaptive radiation. Phylogenetic affinity, evolutionary allometry, and ecological life habit all play major roles in the evolution of cranial shape in the sampled lizards. We find a significant association between cranial shapes and life habit. Our results are in line with the expectations of an adaptive radiation, and this is the first time detailed geometric morphometric analyses have been used to understand the selective forces that drove an adaptive radiation at a continental scale.     

AN ADAPTIVE RADIATION OF FROGS IN A SOUTHEAST ASIAN ISLAND ARCHIPELAGO

Living amphibians exhibit a diversity of ecologies, life histories, and species‐rich lineages that offers opportunities for studies of adaptive radiation. We characterize a diverse clade of frogs (Kaloula, Microhylidae) in the Philippine island archipelago as an example of an adaptive radiation into three primary habitat specialists or ecotypes. We use a novel phylogenetic estimate for this clade to evaluate the tempo of lineage accumulation and morphological diversification. Because species‐level phylogenetic estimates for Philippine Kaloula are lacking, we employ dense population sampling to determine the appropriate evolutionary lineages for diversification analyses. We explicitly take phylogenetic uncertainty into account when calculating diversification and disparification statistics and fitting models of diversification. Following dispersal to the Philippines from Southeast Asia, Kaloula radiated rapidly into several well‐supported clades. Morphological variation within Kaloula is partly explained by ecotype and accumulated at high levels during this radiation, including within ecotypes. We pinpoint an axis of morphospace related directly to climbing and digging behaviors and find patterns of phenotypic evolution suggestive of ecological opportunity with partitioning into distinct habitat specialists. We conclude by discussing the components of phenotypic diversity that are likely important in amphibian adaptive radiations.     

Limiting similarity and functional diversity along environmental gradients

Recent developments in community models emphasize the importance of incorporating stochastic processes (e.g. ecological drift) in models of niche‐structured community assembly. We constructed a finite, spatially explicit, lottery model to simulate the distribution of species in a one‐dimensional landscape with an underlying gradient in environmental conditions. Our framework combines the potential for ecological drift with environmentally‐mediated competition for space in a heterogeneous environment. We examined the influence of niche breadth, dispersal distances, community size (total number of individuals) and the breadth of the environmental gradient on levels of species and functional trait diversity (i.e. differences in niche optima). Three novel results emerge from this model: (1) niche differences between adjacent species (e.g. limiting similarity) increase in smaller communities, because of the interaction of competitive effects and finite population sizes; (2) immigration from a regional species pool, stochasticity and niche‐assembly generate a bimodal distribution of species residence times (‘transient’ and ‘resident’) under a heterogeneous environment; and (3) the magnitude of environmental heterogeneity has a U‐shaped effect on diversity, because of shifts in species richness of resident vs. transient species. These predictions illustrate the potential importance of stochastic (although not necessarily neutral) processes in community assembly.     

Apparent signal of competition limiting diversification after ecological transitions from marine to freshwater habitats

Adaptive radiations are typically triggered when a lineage encounters a significant range of open niche space (ecological opportunity), stemming from colonisation of new areas, extinction of competitors or key innovations. The most well-known of these is the colonisation of new areas, through either dispersal into new regions or the invasion of novel ecological regimes. One aspect of ecological opportunity that has rarely been studied, however, is the extent to which pre-existent competitors act to limit diversification in newly colonised adaptive zones. Herein, we show that in multiple geographically independent invasions of freshwaters by marine Sea Catfishes (Ariidae), rates of both morphological disparification and lineage diversification are inversely related to the presence and diversity of other freshwater fish lineages. Only in one region (Australia-New Guinea) with an otherwise depauperate freshwater fauna, has an ariid invasion gained any substantial traction. This is true at both regional and community scales, suggesting that competitive constraints may be an important factor regulating adaptive radiation.     

Phylogenetic Patterns of Geographical and Ecological Diversification in the Subgenus Drosophila

Colonisation of new geographic regions and/or of new ecological resources can result in rapid species diversification into the new ecological niches available. Members of the subgenus Drosophila are distributed across the globe and show a large diversity of ecological niches. Furthermore, taxonomic classification of Drosophila includes the rank radiation, which refers to closely related species groups. Nevertheless, it has never been tested if these taxonomic radiations correspond to evolutionary radiations. Here we present a study of the patterns of diversification of Drosophila to test for increased diversification rates in relation to the geographic and ecological diversification processes. For this, we have estimated and dated a phylogeny of 218 species belonging to the major species groups of the subgenus. The obtained phylogenies are largely consistent with previous studies and indicate that the major groups appeared during the Oligocene/Miocene transition or early Miocene, characterized by a trend of climate warming with brief periods of glaciation. Ancestral reconstruction of geographic ranges and ecological resource use suggest at least two dispersals to the Neotropics from the ancestral Asiatic tropical disribution, and several transitions to specialized ecological resource use (mycophagous and cactophilic). Colonisation of new geographic regions and/or of new ecological resources can result in rapid species diversification into the new ecological niches available. However, diversification analyses show no significant support for adaptive radiations as a result of geographic dispersal or ecological resource shift. Also, cactophily has not resulted in an increase in the diversification rate of the repleta and related groups. It is thus concluded that the taxonomic radiations do not correspond to adaptive radiations.     

A stochastic biodiversity model with overlapping niche structure

The niche is a fundamental ecological concept that underpins many explanations of patterns of biodiversity. The complexity of niche processes in ecological systems, however, means that it is difficult to capture them accurately in theoretical models of community assembly. In this study, we build upon simple neutral biodiversity models by adding the important ingredient of overlapping niche structure. Our model is spatially implicit and contains a fixed number of equal-sized habitats. Each species in the metacommunity arises through a speciation event; at which time, it is randomly assigned a fundamental niche or set of environments/habitats in which it can persist. Within each habitat, species compete with other species that have different but overlapping fundamental niches. Species abundances then change through ecological drift; each, however, is constrained by its maximum niche breadth and by the presence of other species in its habitats. Using our model, we derive analytical expressions for steady-state species abundance distributions, steady-state distributions of niche breadth across individuals and across species, and dynamic distributions of niche breadth across species. With this framework, we identify the conditions that produce the log-series species abundance distribution familiar from neutral models. We then identify how overlapping niche structure can lead to other species abundance distributions and, in particular, ask whether these new distributions differ significantly from species abundance distributions predicted by non-overlapping niche models. Finally, we extend our analysis to consider additional distributions associated with realized niche breadths. Overall, our results show that models with overlapping niches can exhibit behavior similar to neutral models, with the caveat that species with narrow fundamental niche breadths will be very rare. If narrow-niche species are common, it must be because they are in a non-overlapping niche or have countervailing advantages over broad-niche species. This result highlights the role that niches can play in establishing demographic neutrality.     

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.     

Overshooting dynamics in a model adaptive radiation

The history of life is punctuated by repeated periods of unusually rapid evolutionary diversification called adaptive radiation. The dynamics of diversity during a radiation reflect an overshooting pattern with an initial phase of exponential-like increase followed by a slower decline. Much attention has been paid to the factors that drive the increase phase, but far less is known about the causes of the decline phase. Decreases in diversity are rarely associated with climatic changes or catastrophic events, suggesting that they may be an intrinsic consequence of diversification. We experimentally identify the factors responsible for losses in diversity during the later stages of the model adaptive radiation of the bacterium Pseudomonas fluorescens. Proximately, diversity declines because of the loss of biofilm-forming niche specialist morphotypes. We show that this loss occurs despite the presence of strong divergent selection late in the radiation and is associated with continued adaptation of resident niche specialists to both the biotic and abiotic environments. These results suggest that losses of diversity in the latter stages of an adaptive radiation may be a general consequence of diversification through competition and lends support to the idea that the conditions favouring the emergence of diversity are different from those that ensure its long-term maintenance.     

The repeatability of adaptive radiation during long-term experimental evolution of Escherichia coli in a multiple nutrient environment

Adaptive radiations occur when a species diversifies into different ecological specialists due to competition for resources and trade-offs associated with the specialization. The evolutionary outcome of an instance of adaptive radiation cannot generally be predicted because chance (stochastic events) and necessity (deterministic events) contribute to the evolution of diversity. With increasing contributions of chance, the degree of parallelism among different instances of adaptive radiations and the predictability of an outcome will decrease. To assess the relative contributions of chance and necessity during adaptive radiation, we performed a selection experiment by evolving twelve independent microcosms of Escherichia coli for 1000 generations in an environment that contained two distinct resources. Specialization to either of these resources involves strong trade-offs in the ability to use the other resource. After selection, we measured three phenotypic traits: 1) fitness, 2) mean colony size, and 3) colony size diversity. We used fitness relative to the ancestor as a measure of adaptation to the selective environment; changes in colony size as a measure of the evolution of new resource specialists because colony size has been shown to correlate with resource specialization; and colony size diversity as a measure of the evolved ecological diversity. Resource competition led to the rapid evolution of phenotypic diversity within microcosms. Measurements of fitness, colony size, and colony size diversity within and among microcosms showed that the repeatability of adaptive radiation was high, despite the evolution of genetic variation within microcosms. Consistent with the observation of parallel evolution, we show that the relative contributions of chance are far smaller and less important than effects due to adaptation for the traits investigated. The two-resource environment imposed similar selection pressures in independent populations and promoted parallel phenotypic adaptive radiations in all independently evolved microcosms.     

Diversification of the climatic niche drove the recent processes of speciation in Sigmodontinae (Rodentia,Cricetidae)

Evolutionary radiations are among the most intriguing natural phenomena. Sigmodontine rodents form a megadiverse group for which doubts exist about the adaptive or non‐adaptive nature of its radiation. We analysed whether or not the rates of diversification of species of Sigmodontinae are related to the rates of diversification of the climatic niches occupied by the species. Our results show a clear association between niche diversification and speciation processes. However, this association is linked to recent and independent processes of diversification in sigmodontines, as opposed to an early link that would indicate a niche‐filling consistent with an adaptive radiation of the subfamily.