Adaptive radiation in labrid fishes: A central role for functional innovations during 65 My of relentless diversification

Early burst patterns of diversification have become closely linked with concepts of adaptive radiation, reflecting interest in the role of ecological opportunity in modulating diversification. But, this model has not been widely explored on coral reefs, where biodiversity is exceptional, but many lineages have high dispersal capabilities and a pan‐tropical distribution. We analyze adaptive radiation in labrid fishes, arguably the most ecologically dominant and diverse radiation of fishes on coral reefs. We test for time‐dependent speciation, trophic diversification, and origination of 15 functional innovations, and early bursts in a series of functional morphological traits associated with feeding and locomotion. We find no evidence of time‐dependent or early burst evolution. Instead, the pace of speciation, ecological diversification, and trait evolution has been relatively constant. The origination of functional innovations has slowed over time, although few arose early. The labrid radiation seems to have occurred in response to extensive and still increasing ecological opportunity, but within a rich community of antagonists that may have prevented abrupt diversification. Labrid diversification is closely tied to a series of substantial functional innovations that individually broadened ecological diversity, ultimately allowing them to invade virtually every trophic niche held by fishes on coral reefs.     

Adaptive landscape and functional diversity of Neotropical cichlids: implications for the ecology and evolution of Cichlinae (Cichlidae; Cichliformes)

Morphological, lineage and ecological diversity can vary substantially even among closely related lineages. Factors that influence morphological diversification, especially in functionally relevant traits, can help to explain the modern distribution of disparity across phylogenies and communities. Multivariate axes of feeding functional morphology from 75 species of Neotropical cichlid and a stepwise‐AIC algorithm were used to estimate the adaptive landscape of functional morphospace in Cichlinae. Adaptive landscape complexity and convergence, as well as the functional diversity of Cichlinae, were compared with expectations under null evolutionary models. Neotropical cichlid feeding function varied primarily between traits associated with ram feeding vs. suction feeding/biting and secondarily with oral jaw muscle size and pharyngeal crushing capacity. The number of changes in selective regimes and the amount of convergence between lineages was higher than expected under a null model of evolution, but convergence was not higher than expected under a similarly complex adaptive landscape. Functional disparity was compatible with an adaptive landscape model, whereas the distribution of evolutionary change through morphospace corresponded with a process of evolution towards a single adaptive peak. The continentally distributed Neotropical cichlids have evolved relatively rapidly towards a number of adaptive peaks in functional trait space. Selection in Cichlinae functional morphospace is more complex than expected under null evolutionary models. The complexity of selective constraints in feeding morphology has likely been a significant contributor to the diversity of feeding ecology in this clade.     

Relationships among habitat,ecomorphology and diets of cichlids in the Bladen River,Belize

The Neotropical Cichlidae is among the most species-rich and ecologically diverse groups of freshwater fishes. This study investigated interspecific morphological and ecological relationships within an assemblage of six cichlids in the Upper Bladen River, Belize. This portion of the river drains a nearly pristine watershed within a nature reserve, and thus should provide a natural ecological context for interpretation of ecological patterns. Species distributions within morphological, habitat and dietary space yielded patterns consistent with a hypothesis of niche partitioning. Statistical analyses of the species assemblage revealed relationships between two principal morphological gradients from multivariate analysis with several diet and habitat variables, and these patterns were consistent with prior functional morphological interpretations. Given that this local cichlid assemblage contains no congeneric species, it is apparent that morphological divergence resulting in niche segregation reflects selective establishment of species from a more species-rich regional species pool rather than in situ adaptive evolution.     

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.     

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.     

Large-scale patterns of diversification in the widespread legume genus Senna and the evolutionary role of extrafloral nectaries

Unraveling the diversification history of old, species-rich and widespread clades is difficult because of extinction, undersampling, and taxonomic uncertainty. In the context of these challenges, we investigated the timing and mode of lineage diversification in Senna (Leguminosae) to gain insights into the evolutionary role of extrafloral nectaries (EFNs). EFNs secrete nectar, attracting ants and forming ecologically important ant-plant mutualisms. In Senna, EFNs characterize one large clade (EFN clade), including 80% of its 350 species. Taxonomic accounts make Senna the largest caesalpinioid genus, but quantitative comparisons to other taxa require inferences about rates. Molecular dating analyses suggest that Senna originated in the early Eocene, and its major lineages appeared during early/mid Eocene to early Oligocene. EFNs evolved in the late Eocene, after the main radiation of ants. The EFN clade diversified faster, becoming significantly more species-rich than non-EFN clades. The shift in diversification rates associated with EFN evolution supports the hypothesis that EFNs represent a (relatively old) key innovation in Senna. EFNs may have promoted the colonization of new habitats appearing with the early uplift of the Andes. This would explain the distinctive geographic concentration of the EFN clade in South America.     

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.     

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.     

EARLY BURSTS OF BODY SIZE AND SHAPE EVOLUTION ARE RARE IN COMPARATIVE DATA

George Gaylord Simpson famously postulated that much of life's diversity originated as adaptive radiations—more or less simultaneous divergences of numerous lines from a single ancestral adaptive type. However, identifying adaptive radiations has proven difficult due to a lack of broad‐scale comparative datasets. Here, we use phylogenetic comparative data on body size and shape in a diversity of animal clades to test a key model of adaptive radiation, in which initially rapid morphological evolution is followed by relative stasis. We compared the fit of this model to both single selective peak and random walk models. We found little support for the early‐burst model of adaptive radiation, whereas both other models, particularly that of selective peaks, were commonly supported. In addition, we found that the net rate of morphological evolution varied inversely with clade age. The youngest clades appear to evolve most rapidly because long‐term change typically does not attain the amount of divergence predicted from rates measured over short time scales. Across our entire analysis, the dominant pattern was one of constraints shaping evolution continually through time rather than rapid evolution followed by stasis. We suggest that the classical model of adaptive radiation, where morphological evolution is initially rapid and slows through time, may be rare in comparative data.     

Temporal diversification of Central American cichlids

Background  

Cichlid fishes are classic examples of adaptive radiation because of their putative tendency to explosively diversify after invading novel environments. To examine whether ecological opportunity increased diversification (speciation minus extinction) early in a species-rich cichlid radiation, we determined if Heroine cichlids experienced a burst of diversification following their invasion of Central America.     

Hierarchy in adaptive radiation: A case study using the Carnivora (Mammalia)

Simpson's “early burst” model of adaptive radiation was intended to explain the early proliferation of morphological and functional variation in diversifying clades. Yet, despite much empirical testing, questions remain regarding its frequency across the tree of life. Here, we evaluate the support for an early burst model of adaptive radiation in 14 ecomorphological traits plus body mass for the extant mammalian order Carnivora and its constituent families. We find strong support for early bursts of dental evolution, suggesting a classic Simpsonian adaptive radiation along dietary resource axes. However, the signal of this early burst is not consistently recovered in analyses at the family level, where support for a variety of different models emerges. Furthermore, we find no evidence for early burst–like dynamics in size–related traits, and Bayesian analyses of evolutionary correlations corroborate a decoupling of size and dental evolution, driven in part by dietary specialization. Our results are consistent with the perspective that trait diversification unfolds hierarchically, with early bursts restricted to traits associated with higher level niches, such as macrohabitat use or dietary strategy, and thus with the origins of higher taxa. The lack of support for early burst adaptive radiation in previous phylogenetic studies may be a consequence of focusing on low‐level niche traits (i.e., those associated with microhabitat use) in clades at shallow phylogenetic levels. A richer understanding of early burst adaptive radiation will require a renewed focus on functional traits and their evolution over higher level clades.     

Impact of the terrestrial-aquatic transition on disparity and rates of evolution in the carnivoran skull

Background

Which factors influence the distribution patterns of morphological diversity among clades? The adaptive radiation model predicts that a clade entering new ecological niche will experience high rates of evolution early in its history, followed by a gradual slowing. Here we measure disparity and rates of evolution in Carnivora, specifically focusing on the terrestrial-aquatic transition in Pinnipedia. We analyze fissiped (mostly terrestrial, arboreal, and semi-arboreal, but also including the semi-aquatic otter) and pinniped (secondarily aquatic) carnivorans as a case study of an extreme ecological transition. We used 3D geometric morphometrics to quantify cranial shape in 151 carnivoran specimens (64 fissiped, 87 pinniped) and five exceptionally-preserved fossil pinnipeds, including the stem-pinniped Enaliarctos emlongi. Range-based and variance-based disparity measures were compared between pinnipeds and fissipeds. To distinguish between evolutionary modes, a Brownian motion model was compared to selective regime shifts associated with the terrestrial-aquatic transition and at the base of Pinnipedia. Further, evolutionary patterns were estimated on individual branches using both Ornstein-Uhlenbeck and Independent Evolution models, to examine the origin of pinniped diversity.

Results

Pinnipeds exhibit greater cranial disparity than fissipeds, even though they are less taxonomically diverse and, as a clade nested within fissipeds, phylogenetically younger. Despite this, there is no increase in the rate of morphological evolution at the base of Pinnipedia, as would be predicted by an adaptive radiation model, and a Brownian motion model of evolution is supported. Instead basal pinnipeds populated new areas of morphospace via low to moderate rates of evolution in new directions, followed by later bursts within the crown-group, potentially associated with ecological diversification within the marine realm.

Conclusion

The transition to an aquatic habitat in carnivorans resulted in a shift in cranial morphology without an increase in rate in the stem lineage, contra to the adaptive radiation model. Instead these data suggest a release from evolutionary constraint model, followed by aquatic diversifications within crown families.

Electronic supplementary material

The online version of this article (doi:10.1186/s12862-015-0285-5) contains supplementary material, which is available to authorized users.     

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.     

Adaptive radiation of island plants: evidence from Aeonium (Crassulaceae) of the Canary Islands

The presence of diverse and species-rich plant lineages on oceanic islands is most often associated with adaptive radiation. Here we discuss the possible adaptive significance of some of the most prominent traits in island plants, including woodiness, monocarpy and sexual dimorphisms. Indirect evidence that such traits have been acquired through convergent evolution on islands comes from molecular phylogenies; however, direct evidence of their selective value rarely is obtained. The importance of hybridization in the evolution of island plants is also considered as part of a more general discussion of the mechanisms governing radiations on islands. Most examples are from the Hawaiian and Canarian floras, and in particular from studies on the morphological, ecological and molecular diversification of the genus Aeonium, the largest plant radiation of the Canarian Islands.     

Continuous and arrested morphological diversification in sister clades of characiform fishes: a phylomorphospace approach

Understanding how and why certain clades diversify greatly in morphology whereas others do not remains a major theme in evolutionary biology. Projecting families of phylogenies into multivariate morphospaces can distinguish two scenarios potentially leading to unequal morphological diversification: unequal magnitude of change per phylogenetic branch, and unequal efficiency in morphological innovation. This approach is demonstrated using a case study of skulls in sister clades within the South American fish superfamily Anostomoidea. Unequal morphological diversification in this system resulted not from the morphologically diverse clade changing more on each phylogenetic branch, but from that clade distributing an equal amount of change more widely through morphospace and innovating continually. Although substantial morphological evolution occurred throughout the less diverse clade's history, most of that clade's expansion in morphospace occurred in the most basal branches, and more derived portions of that radiation oscillated within previously explored limits. Because simulations revealed that there is a maximum 2.7% probability of generating two clades that differ so greatly in the density of lineages within morphospace under a null Brownian model, the observed difference in pattern likely reflects a difference in the underlying evolutionary process. Clade-specific factors that may have promoted or arrested morphological diversification are discussed.     

When should we expect early bursts of trait evolution in comparative data? Predictions from an evolutionary food web model

Conceptual models of adaptive radiation predict that competitive interactions among species will result in an early burst of speciation and trait evolution followed by a slowdown in diversification rates. Empirical studies often show early accumulation of lineages in phylogenetic trees, but usually fail to detect early bursts of phenotypic evolution. We use an evolutionary simulation model to assemble food webs through adaptive radiation, and examine patterns in the resulting phylogenetic trees and species' traits (body size and trophic position). We find that when foraging trade-offs result in food webs where all species occupy integer trophic levels, lineage diversity and trait disparity are concentrated early in the tree, consistent with the early burst model. In contrast, in food webs in which many omnivorous species feed at multiple trophic levels, high levels of turnover of species' identities and traits tend to eliminate the early burst signal. These results suggest testable predictions about how the niche structure of ecological communities may be reflected by macroevolutionary patterns.     

Multigene phylogeny of the Mustelidae: Resolving relationships,tempo and biogeographic history of a mammalian adaptive radiation

Background  

Adaptive radiation, the evolution of ecological and phenotypic diversity from a common ancestor, is a central concept in evolutionary biology and characterizes the evolutionary histories of many groups of organisms. One such group is the Mustelidae, the most species-rich family within the mammalian order Carnivora, encompassing 59 species classified into 22 genera. Extant mustelids display extensive ecomorphological diversity, with different lineages having evolved into an array of adaptive zones, from fossorial badgers to semi-aquatic otters. Mustelids are also widely distributed, with multiple genera found on different continents. As with other groups that have undergone adaptive radiation, resolving the phylogenetic history of mustelids presents a number of challenges because ecomorphological convergence may potentially confound morphologically based phylogenetic inferences, and because adaptive radiations often include one or more periods of rapid cladogenesis that require a large amount of data to resolve.     

Ecological correlates of species differences in the Lake Tanganyika crab radiation

The endemic crabs of Lake Tanganyika include a phenotypically diverse clade that exhibits recent divergence and low phylogenetic species resolution. There are indications that ecological niche segregation has played a prominent role in the divergence of this clade. We used habitat surveys, gut content analyses and stable isotope analyses to test the extent to which morphological species are ecologically different. Our data show some interspecific segregation in depth, substrate type and mean stable isotope signatures. At the same time, a considerable level of ecological niche overlap is evident among species of Platythelphusa that coexist in rocky littoral habitats. We consider these results in the framework of adaptive radiation theory, and we discuss general ramifications for the maintenance of species diversity in Lake Tanganyika.     

Physiological evolution during adaptive radiation: A test of the island effect in Anolis lizards

Phenotypic evolution is often exceptionally rapid on islands, resulting in numerous, ecologically diverse species. Although adaptive radiation proceeds along various phenotypic axes, the island effect of faster evolution has been mostly tested with regard to morphology. Here, we leveraged the physiological diversity and species richness of Anolis lizards to examine the evolutionary dynamics of three key traits: heat tolerance, body temperature, and cold tolerance. Contrary to expectation, we discovered slower heat tolerance evolution on islands. Additionally, island species evolve toward higher optimal body temperatures than mainland species. Higher optima and slower evolution in upper physiological limits are consistent with the Bogert effect, or evolutionary inertia due to thermoregulation. Correspondingly, body temperature is higher and more stable on islands than on the American mainland, despite similarity in thermal environments. Greater thermoregulation on islands may occur due to ecological release from competitors and predators compared to mainland environments. By reducing the costs of thermoregulation, ecological opportunity on islands may actually stymie, rather than hasten, physiological evolution. Our results emphasize that physiological diversity is an important axis of ecological differentiation in the adaptive radiation of anoles, and that behavior can impart distinct macroevolutionary footprints on physiological diversity on islands and continents.     

Trait evolution rates shape continental patterns of species richness in North America's most diverse angiosperm genus (Carex,Cyperaceae)

Ecological opportunity has been associated with increases in diversification rates across the tree of life. Under an ecological diversification model, the emergence of novel environments is hypothesized to promote morpho- and ecospace evolution. Whether this model holds at the clade level within the most species-rich angiosperm genus found in North America (Carex, Cyperaceae) is yet to be tested. Recent works demonstrate a temporal coupling of climate cooling and widespread colonization of Carex in North America, implicating ecological diversification. In addition, research has consistently found asymmetric patterns of lineage-level diversification in the genus. Why does variation in clade sizes exist in the genus? Is ecological diversification involved? In this study, we tested whether rates of morphological and ecological trait evolution are correlated with clade-level species richness in Carex of North America north of Mexico. We constructed a phylogeny of 477 species—an almost complete regional sample. We estimated rates of evolution of morphological traits, habitat, and climatic niche and assessed whether differences in rates of evolution correlate with species richness differences in replicate non-nested sister clades. Our work demonstrates significant positive correlations between climatic niche rates, habitat and reproductive morphological evolution, and species richness. This coupling of trait and niche evolution and species richness in a diverse, continental clade sample strongly suggests that the ability of clades to explore niche and functional space has shaped disparities in richness and functional diversity across the North American flora region. Our findings highlight the importance of the evolutionary history of trait and niche evolution in shaping continental and regional floras.