Tightly congruent bursts of lineage and phenotypic diversification identified in a continental ant radiation

Adaptive diversification is thought to be shaped by ecological opportunity. A prediction of this ecological process of diversification is that it should result in congruent bursts of lineage and phenotypic diversification, but few studies have found this expected association. Here, we study the relationship between rates of lineage diversification and body size evolution in the turtle ants, a diverse Neotropical clade. Using a near complete, time‐calibrated phylogeny we investigated lineage diversification dynamics and body size disparity through model fitting analyses and estimation of per‐lineage rates of cladogenesis and phenotypic evolution. We identify an exceptionally high degree of congruence between the high rates of lineage and body size diversification in a young clade undergoing renewed diversification in the ecologically distinct Chacoan biogeographical region of South America. It is likely that the region presented turtle ants with novel ecological opportunity, which facilitated a nested burst of diversification and phenotypic evolution within the group. Our results provide a compelling quantitative example of tight congruence between rates of lineage and phenotypic diversification, meeting the key predicted pattern of adaptive diversification shaped by ecological opportunity.     

Transcontinental dispersal,ecological opportunity and origins of an adaptive radiation in the Neotropical catfish genus Hypostomus (Siluriformes: Loricariidae)

Ecological opportunity is often proposed as a driver of accelerated diversification, but evidence has been largely derived from either contemporary island radiations or the fossil record. Here, we investigate the potential influence of ecological opportunity on a transcontinental radiation of South American freshwater fishes. We generate a species‐dense, time‐calibrated molecular phylogeny for the suckermouth armored catfish subfamily Hypostominae, with a focus on the species‐rich and geographically widespread genus Hypostomus. We use the resulting chronogram to estimate ancestral geographical ranges, infer historical rates of cladogenesis and diversification in habitat and body size and shape, and test the hypothesis that invasions of previously unoccupied river drainages accelerated evolution and contributed to adaptive radiation. Both the subfamily Hypostominae and the included genus Hypostomus originated in the Amazon/Orinoco ecoregion. Hypostomus subsequently dispersed throughout tropical South America east of the Andes Mountains. Consequent to invasion of the peripheral, low‐diversity Paraná River basin in southeastern Brazil approximately 12.5 Mya, Paraná lineages of Hypostomus, experienced increased rates of cladogenesis and ecological and morphological diversification. Contemporary lineages of Paraná Hypostomus are less species rich but more phenotypically diverse than their congeners elsewhere. Accelerated speciation and morphological diversification rates within Paraná basin Hypostomus are consistent with adaptive radiation. The geographical remoteness of the Paraná River basin, its recent history of marine incursion, and its continuing exclusion of many species that are widespread in other tropical South American rivers suggest that ecological opportunity played an important role in facilitating the observed accelerations in diversification.     

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.     

Density-dependent diversification in North American wood warblers

Evidence from both molecular phylogenies and the fossil record suggests that rates of species diversification often decline through time during evolutionary radiations. One proposed explanation for this pattern is ecological opportunity, whereby an initial abundance of resources and lack of potential competitors facilitate rapid diversification. This model predicts density-dependent declines in diversification rates, but has not been formally tested in any species-level radiation. Here we develop a new conceptual framework that distinguishes density dependence from alternative processes that also produce temporally declining diversification, and we demonstrate this approach using a new phylogeny of North American Dendroica wood warblers. We show that explosive lineage accumulation early in the history of this avian radiation is best explained by a density-dependent diversification process. Our results suggest that the tempo of wood warbler diversification was mediated by ecological interactions among species and that lineage and ecological diversification in this group are coupled, as predicted under the ecological opportunity model.     

Genomic and phenomic analysis of island ant community assembly

Island biodiversity has long fascinated biologists as it typically presents tractable systems for unpicking the eco‐evolutionary processes driving community assembly. In general, two recurring themes are of central theoretical interest. First, immigration, diversification, and extinction typically depend on island geographical properties (e.g., area, isolation, and age). Second, predictable ecological and evolutionary trajectories readily occur after colonization, such as the evolution of adaptive trait syndromes, trends toward specialization, adaptive radiation, and eventual ecological decline. Hypotheses such as the taxon cycle draw on several of these themes to posit particular constraints on colonization and subsequent eco‐evolutionary dynamics. However, it has been challenging to examine these integrated dynamics with traditional methods. Here, we combine phylogenomics, population genomics and phenomics, to unravel community assembly dynamics among Pheidole (Hymenoptera, Formicidae) ants in the isolated Fijian archipelago. We uphold basic island biogeographic predictions that isolated islands accumulate diversity primarily through in situ evolution rather than dispersal, and population genomic support for taxon cycle predictions that endemic species have decreased dispersal ability and demography relative to regionally widespread taxa. However, rather than trending toward island syndromes, ecomorphological diversification in Fiji was intense, filling much of the genus‐level global morphospace. Furthermore, while most endemic species exhibit demographic decline and reduced dispersal, we show that the archipelago is not an evolutionary dead‐end. Rather, several endemic species show signatures of population and range expansion, including a successful colonization to the Cook islands. These results shed light on the processes shaping island biotas and refine our understanding of island biogeographic theory.     

Niche evolution and diversification in a Neotropical radiation of birds (Aves: Furnariidae)

Rapid diversification may be caused by ecological adaptive radiation via niche divergence. In this model, speciation is coupled with niche divergence and lineage diversification is predicted to be correlated with rates of niche evolution. Studies of the role of niche evolution in diversification have generally focused on ecomorphological diversification but climatic‐niche evolution may also be important. We tested these alternatives using a phylogeny of 298 species of ovenbirds (Aves: Furnariidae). We found that within Furnariidae, variation in species richness and diversification rates of subclades were best predicted by rate of climatic‐niche evolution than ecomorphological evolution. Although both are clearly important, univariate regression and multivariate model averaging more consistently supported the climatic‐niche as the best predictor of lineage diversification. Our study adds to the growing body of evidence, suggesting that climatic‐niche divergence may be an important driver of rapid diversification in addition to ecomorphological evolution. However, this pattern may depend on the phylogenetic scale at which rate heterogeneity is examined.     

Ecological opportunity and the origin of adaptive radiations

Ecological opportunity – through entry into a new environment, the origin of a key innovation or extinction of antagonists – is widely thought to link ecological population dynamics to evolutionary diversification. The population‐level processes arising from ecological opportunity are well documented under the concept of ecological release. However, there is little consensus as to how these processes promote phenotypic diversification, rapid speciation and adaptive radiation. We propose that ecological opportunity could promote adaptive radiation by generating specific changes to the selective regimes acting on natural populations, both by relaxing effective stabilizing selection and by creating conditions that ultimately generate diversifying selection. We assess theoretical and empirical evidence for these effects of ecological opportunity and review emerging phylogenetic approaches that attempt to detect the signature of ecological opportunity across geological time. Finally, we evaluate the evidence for the evolutionary effects of ecological opportunity in the diversification of Caribbean Anolis lizards. Some of the processes that could link ecological opportunity to adaptive radiation are well documented, but others remain unsupported. We suggest that more study is required to characterize the form of natural selection acting on natural populations and to better describe the relationship between ecological opportunity and speciation rates.     

Ecological opportunity and the adaptive diversification of lineages

The tenet that ecological opportunity drives adaptive diversification has been central to theories of speciation since Darwin, yet no widely accepted definition or mechanistic framework for the concept currently exists. We propose a definition for ecological opportunity that provides an explicit mechanism for its action. In our formulation, ecological opportunity refers to environmental conditions that both permit the persistence of a lineage within a community, as well as generate divergent natural selection within that lineage. Thus, ecological opportunity arises from two fundamental elements: (1) niche availability, the ability of a population with a phenotype previously absent from a community to persist within that community and (2) niche discordance, the diversifying selection generated by the adaptive mismatch between a population's niche‐related traits and the newly encountered ecological conditions. Evolutionary response to ecological opportunity is primarily governed by (1) spatiotemporal structure of ecological opportunity, which influences dynamics of selection and development of reproductive isolation and (2) diversification potential, the biological properties of a lineage that determine its capacity to diversify. Diversification under ecological opportunity proceeds as an increase in niche breadth, development of intraspecific ecotypes, speciation, and additional cycles of diversification that may themselves be triggered by speciation. Extensive ecological opportunity may exist in depauperate communities, but it is unclear whether ecological opportunity abates in species‐rich communities. Because ecological opportunity should generally increase during times of rapid and multifarious environmental change, human activities may currently be generating elevated ecological opportunity – but so far little work has directly addressed this topic. Our framework highlights the need for greater synthesis of community ecology and evolutionary biology, unifying the four major components of the concept of ecological opportunity.     

Adaptive radiation and the evolution of nectarivory in a large songbird clade

The accumulation of exceptional ecological diversity within a lineage is a key feature of adaptive radiation resulting from diversification associated with the subdivision of previously underutilized resources. The invasion of unoccupied niche space is predicted to be a key determinant of adaptive diversification, and this process may be particularly important if the diversity of competing lineages within the area, in which the radiation unfolds, is already high. Here, we test whether the evolution of nectarivory resulted in significantly higher rates of morphological evolution, more extensive morphological disparity, and a heightened build‐up of sympatric species diversity in a large adaptive radiation of passerine birds (the honeyeaters, about 190 species) that have diversified extensively throughout continental and insular settings. We find that a large increase in rates of body size evolution and general expansion in morphological space followed an ancestral shift to nectarivory, enabling the build‐up of large numbers of co‐occurring species that vary greatly in size, compared to related and co‐distributed nonnectarivorous clades. These results strongly support the idea that evolutionary shifts into novel areas of niche space play a key role in promoting adaptive radiation in the presence of likely competing lineages.     

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.     

Repeated evolution of terrestrial lineages in a continental lizard radiation

The “early‐burst” model of adaptive radiation predicts an early increase in phenotypic disparity concurrent with lineage diversification. Although most studies report a lack of this coupled pattern, the underlying processes are not identified. The continental radiation of Hemidactylus geckos from Peninsular India includes morphologically diverse species that occupy various microhabitats. This radiation began diversifying ~36 Mya with an early increase in lineage diversification. Here, we test the “early‐burst” hypothesis by investigating the presence of ecomorphs and examining the pattern of morphological diversification in a phylogenetic framework. Two ecomorphs—terrestrial and scansorial species—that vary significantly in body size and toepad size were identified. Unlike the prediction of the “early‐burst” model, we find that disparity in toepad morphology accumulated more recently ~14 Mya and fit the Ornstein‐Ulhenbeck model. Ancestral state reconstruction of the two ecomorphs demonstrates that terrestrial lineages evolved independently at least five times from scansorial ancestors, with the earliest diversification in terrestrial lineages 19–12 Mya. Our study demonstrates a delayed increase in morphological disparity as a result of the evolution of terrestrial ecomorphs. The diversification of terrestrial lineages is concurrent with the establishment of open habitat and grasslands in Peninsular India, suggesting that the appearance of this novel resource led to the adaptive diversification.     

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.     

HOW DOES ECOLOGICAL OPPORTUNITY INFLUENCE RATES OF SPECIATION,EXTINCTION, AND MORPHOLOGICAL DIVERSIFICATION IN NEW WORLD RATSNAKES (TRIBE LAMPROPELTINI)?

Ecological adaptive radiation theory predicts an increase in both morphological and specific diversification when organisms colonize new environments. Accordingly, bursts of morphological diversification, characterized by low within‐subclade morphological disparity, may be associated with these increases in speciation rates. Conversely, increasing species density, reduction in available habitat, or increasing extinction rates are expected to cause rates of diversification to decline. We test these hypotheses by examining the tempo and mode of speciation in the lampropeltinine snakes, a morphologically variable group that colonized the New World ～24 million years ago and radiated throughout the Miocene. We show that specific diversification increased early in the history of the group, and that most morphological variation is partitioned among, rather than within subclades. These patterns provide further evidence for the hypothesis that morphological variation tends to be strongly partitioned among lineages when clades undergo early bursts of species diversification. A reduction in speciation rates may be indicative of density dependent effects due to a saturation of available ecological opportunity, rather than increases in extinction rates at the onset of the Pleistocene/Pliocene glacial cycles. This evidence runs counter to the general Pleistocene species pump model.     

ECOLOGICAL OPPORTUNITY AND THE RATE OF MORPHOLOGICAL EVOLUTION IN THE DIVERSIFICATION OF GREATER ANTILLEAN ANOLES

The pace of phenotypic diversification during adaptive radiation should decrease as ecological opportunity declines. We test this prediction using phylogenetic comparative analyses of a wide range of morphological traits in Greater Antillean Anolis lizards. We find that the rate of diversification along two important axes of Anolis radiation—body size and limb dimensions—decreased as opportunity declined, with opportunity quantified either as time elapsed in the radiation or as the diversity of competing anole lineages inferred to have been present on an island at different times in the past. Most previous studies of the ecological opportunity hypothesis have focused on the rate of species diversification; our results provide a complementary perspective, indicating that the rate of phenotypic diversification declines with decreasing opportunity in an adaptive radiation.     

Tracing the Rise of Ants - Out of the Ground

The evolution of ants (Hymenoptera: Formicidae) is increasingly well-understood due to recent phylogenetic analyses, along with estimates of divergence times and diversification rates. Yet, leading hypotheses regarding the ancestral habitat of ants conflict with new findings that early ant lineages are cryptic and subterranean. Where the ants evolved, in respect to habitat, and how habitat shifts took place over time have not been formally tested. Here, we reconstruct the habitat transitions of crown-group ants through time, focusing on where they nest and forage (in the canopy, litter, or soil). Based on ancestral character reconstructions, we show that in contrast to the current consensus based on verbal arguments that ants evolved in tropical leaf litter, the soil is supported as the ancestral stratum of all ants. We also find subsequent movements up into the litter and, in some cases, into the canopy. Given the global importance of ants, because of their diversity, ecological influence and status as the most successful eusocial lineage on Earth, understanding the early evolution of this lineage provides insight into the factors that made this group so successful today.     

Disruptive selection as a driver of evolutionary branching and caste evolution in social insects

Theory suggests that evolutionary branching via disruptive selection may be a relatively common and powerful force driving phenotypic divergence. Here, we extend this theory to social insects, which have novel social axes of phenotypic diversification. Our model, built around turtle ant (Cephalotes) biology, is used to explore whether disruptive selection can drive the evolutionary branching of divergent colony phenotypes that include a novel soldier caste. Soldier evolution is a recurrent theme in social insect diversification that is exemplified in the turtle ants. We show that phenotypic mutants can gain competitive advantages that induce disruptive selection and subsequent branching. A soldier caste does not generally appear before branching, but can evolve from subsequent competition. The soldier caste then evolves in association with specialized resource preferences that maximize defensive performance. Overall, our model indicates that resource specialization may occur in the absence of morphological specialization, but that when morphological specialization evolves, it is always in association with resource specialization. This evolutionary coupling of ecological and morphological specialization is consistent with recent empirical evidence, but contrary to predictions of classical caste theory. Our model provides a new theoretical understanding of the ecology of caste evolution that explicitly considers the process of adaptive phenotypic divergence and diversification.     

Adaptive Evolution of Deep-Sea Amphipods from the Superfamily Lysiassanoidea in the North Atlantic

In this study we reconstruct phylogenies for deep sea amphipods from the North Atlantic in order to test hypotheses about the evolutionary mechanisms driving speciation in the deep sea. We sequenced five genes for specimens representing 21 families. Phylogenetic analyses showed incongruence between the molecular data and morphological taxonomy, with some morphologically distinct taxa showing close molecular similarity. Approximate dating of nodes based on available calibration suggested adaptation to the deep sea around the Cretaceous-Palaeogene boundary, with three identified lineages within the deep-sea radiation dating to the Eocene–Oligocene transition. Two of those lineages contained species currently classified in multiple families. We reconstructed ancestral nodes based on the mouthpart characters that define trophic guilds (also used to establish the current taxonomy), and show a consistent transition at the earliest node defining the deep-sea lineage, together with increasing diversification at more recent nodes within the deep-sea lineage. The data suggest that the divergence of species was adaptive, with successive diversification from a non-scavenging ancestor to ‘opportunistic’, ‘obligate’ and ‘specialised’ scavengers. We propose that the North Atlantic species studied provide a strong case for adaptive evolution promoted by ecological opportunity in the deep sea.     

Recent and rapid speciation with limited morphological disparity in the genus Rattus

Recent and rapid radiations provide rich material to examine the factors that drive speciation. Most recent and rapid radiations that have been well-characterized involve species that exhibit overt ecomorphological differences associated with clear partitioning of ecological niches in sympatry. The most diverse genus of rodents, Rattus (66 species), evolved fairly recently, but without overt ecomorphological divergence among species. We used multilocus molecular phylogenetic data and five fossil calibrations to estimate the tempo of diversification in Rattus, and their radiation on Australia and New Guinea (Sahul, 24 species). Based on our analyses, the genus Rattus originated at a date centered on the Pliocene-Pleistocene boundary (1.84-3.17 Ma) with a subsequent colonization of Sahul in the middle Pleistocene (0.85-1.28 Ma). Given these dates, the per lineage diversification rates in Rattus and Sahulian Rattus are among the highest reported for vertebrates (1.1-1.9 and 1.6-3.0 species per lineage per million years, respectively). Despite their rapid diversification, Rattus display little ecomorphological divergence among species and do not fit clearly into current models of adaptive radiations. Lineage through time plots and ancestral state reconstruction of ecological characters suggest that diversification of Sahulian Rattus was most rapid early on as they expanded into novel ecological conditions. However, rapid lineage accumulation occurred even when morphological disparity within lineages was low suggesting that future studies consider other phenotypes in the diversification of Rattus.     

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.     

Novel trophic niches drive variable progress towards ecological speciation within an adaptive radiation of pupfishes

Adaptive radiation is recognized by a rapid burst of phenotypic, ecological and species diversification. However, it is unknown whether different species within an adaptive radiation evolve reproductive isolation at different rates. We compared patterns of genetic differentiation between nascent species within an adaptive radiation of Cyprinodon pupfishes using genotyping by sequencing. Similar to classic adaptive radiations, this clade exhibits rapid morphological diversification rates and two species are novel trophic specialists, a scale‐eater and hard‐shelled prey specialist (durophage), yet the radiation is <10 000 years old. Both specialists and an abundant generalist species all coexist in the benthic zone of lakes on San Salvador Island, Bahamas. Based on 13 912 single‐nucleotide polymorphisms (SNPs), we found consistent differences in genetic differentiation between each specialist species and the generalist across seven lakes. The scale‐eater showed the greatest genetic differentiation and clustered by species across lakes, whereas durophage populations often clustered with sympatric generalist populations, consistent with parallel speciation across lakes. However, we found strong evidence of admixture between durophage populations in different lakes, supporting a single origin of this species and genome‐wide introgression with sympatric generalist populations. We conclude that the scale‐eater is further along the speciation‐with‐gene‐flow continuum than the durophage and suggest that different adaptive landscapes underlying these two niche environments drive variable progress towards speciation within the same habitat. Our previous measurements of fitness surfaces in these lakes support this conclusion: the scale‐eating fitness peak may be more distant than the durophage peak on the complex adaptive landscape driving adaptive radiation.