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.     

Parasitoid fig‐wasp evolutionary diversification and variation in ecological opportunity

Ecological processes are manifest in the evolution and form of phenotype diversity. The great abundance of parasitoid species has led to speculation whether rates of speciation and extinction are dependent on parasitoid diversity. If these factors are mutually exclusive, species diversity should fluctuate instead of remaining relatively constant over time. It is not known whether radiations constrained by coevolutionary interactions conform to density‐dependent diversification processes. Here we test the prediction that parasitoid fig wasp diversification responds to changes in ecological opportunity and density‐independent processes. A phylogenetic approach is used to estimate relative divergence times and infer diversification rate changes using γ‐statistics. Monte Carlo constant rates tests that accommodate incomplete sampling could not reject constant rates diversification. Parasitoid fig wasp diversification is consistent with a more complex explanation than density‐dependent cladogenesis. The results suggest contemporary African parasitoid fig wasp diversity remains a legacy of an ancient ecological opportunity facilitated by fig tree diversification following the breakup of Pan‐African forests and evolution of the savanna biome over the last 55 Ma and the more recent aridification of the African continent in the last 5 Ma. These results imply that amplified phenotypic differentiation of specialist insects coevolving with plants is coupled to evolutionarily infrequent changes in ecological opportunity.     

Ecological and Ecomorphological Specialization Are Not Associated with Diversification Rates in Muroid Rodents (Rodentia: Muroidea)

Multiple diversification rate shifts explain uneven clade richness in muroid rodents. Previous muroid studies have shown that extrinsic factors, notwithstanding ecological opportunity, are poor predictors of clade diversity. Here, we use a 297-muroid species chronogram that is sampled proportional to total clade diversity, along with various trait-dependent diversification approaches to investigate the association between diversification rates with intrinsic attributes—diet, habitat, body mass, and relative tail length. We found some association between both dietary specialization and body mass, as well as between habitat specialization with relative tail lengths using phylogenetic analyses of variance. However, there was no significant association between diversification rates with the evolution of these traits in muroid rodents. We also show that several of the state-dependent diversification approaches are highly susceptible to Type I error—a result that is in accordance with recent criticisms of these methods. Finally, we discuss several potential causes for the lack of association between the examined trait data with diversification rates, ranging from methodological biases (e.g. method conservativism) to biology (e.g. behavioral plasticity and ecological opportunism of muroid rodents).     

Morphological disparity opposes latitudinal diversity gradient in lacertid lizards

While global variation in taxonomic diversity is strongly linked to latitude, the extent to which morphological disparity follows geographical gradients is less well known. We estimated patterns of lineage diversification, morphological disparity and rates of phenotypic evolution in the Old World lizard family Lacertidae, which displays a nearly inverse latitudinal diversity gradient with decreasing species richness towards the tropics. We found that lacertids exhibit relatively constant rates of lineage accumulation over time, although the majority of morphological variation appears to have originated during recent divergence events, resulting in increased partitioning of disparity within subclades. Among subclades, tropical arboreal taxa exhibited the fastest rates of shape change while temperate European taxa were the slowest, resulting in an inverse relationship between latitudinal diversity and rates of phenotypic evolution. This pattern demonstrates a compelling counterexample to the ecological opportunity theory of diversification, suggesting an uncoupling of the processes generating species diversity and morphological differentiation across spatial scales.     

Is regional species diversity bounded or unbounded?

Two conflicting hypotheses have been proposed to explain large‐scale species diversity patterns and dynamics. The unbounded hypothesis proposes that regional diversity depends only on time and diversification rate and increases without limit. The bounded hypothesis proposes that ecological constraints place upper limits on regional diversity and that diversity is usually close to its limit. Recent evidence from the fossil record, phylogenetic analysis, biogeography, and phenotypic disparity during lineage diversification suggests that diversity is constrained by ecological processes but that it is rarely asymptotic. Niche space is often unfilled or can be more finely subdivided and still permit coexistence, and new niche space is often created before ecological limits are reached. Damped increases in diversity over time are the prevalent pattern, suggesting the need for a new ‘damped increase hypothesis'. The damped increase hypothesis predicts that diversity generally increases through time but that its rate of increase is often slowed by ecological constraints. However, slowing due to niche limitation must be distinguished from other possible mechanisms creating similar patterns. These include sampling artifacts, the inability to detect extinctions or declines in clade diversity with some methods, the distorting effects of correlated speciation‐extinction dynamics, the likelihood that opportunities for allopatric speciation will vary in space and time, and the role of undetected natural enemies in reducing host ranges and thus slowing speciation rates. The taxonomic scope of regional diversity studies must be broadened to include all ecologically similar species so that ecological constraints may be accurately inferred. The damped increase hypothesis suggests that information on evolutionary processes such as time‐for‐speciation and intrinsic diversification rates as well as ecological factors will be required to explain why regional diversity varies among times, places and taxa.     

Ecological opportunity alters the timing and shape of adaptive radiation

The uneven distribution of diversity is a conspicuous phenomenon across the tree of life. Ecological opportunity is a prominent catalyst of adaptive radiation and therefore may alter patterns of diversification. We evaluated the distribution of shifts in diversification rates across the cichlid phylogeny and the distribution of major clades across phylogenetic space. We also tested if ecological opportunity influenced these patterns. Colonization‐associated ecological opportunity altered the tempo and mode of diversification during the adaptive radiation of cichlid fishes. Clades that arose following colonization events diversified faster than other clades. Speciation rate shifts were nonrandomly distributed across the phylogeny such that they were disproportionally concentrated around nodes that corresponded with colonization events (i.e., of continents, river basins, or lakes). Young clades tend to expand faster than older clades; however, colonization‐associated ecological opportunity accentuated this pattern. There was an interaction between clade age and ecological opportunity that explained the trajectory of clades through phylogenetic space over time. Our results indicate that ecological opportunities afforded by continental and ecosystem‐scale colonization events explain the dramatic speciation rate heterogeneity and phylogenetic imbalance that arose during the evolutionary history of cichlid fishes.     

Disparity and Evolutionary Rate Do Not Explain Diversity Patterns in Muroid Rodents (Rodentia: Muroidea)

A positive correlation between diversity and disparity/evolutionary rate is predicted by multiple evolutionary theories. However, recent empirical studies in various taxa do not always find such an association. Similarly, we find no correlation between these two levels of variation, based on cranial morphometric data and molecular phylogenetic data from 317 muroid rodent species and dipodoid outgroups, analyzed using three-dimensional geometric morphometrics. This disassociation was found using both phylogenetic and non-phylogenetic approaches, indicating that an increase in clade richness is not necessarily followed by an increase in morphological divergence and vice versa. Furthermore, the distribution of muroid families in morphospace is highly overlapping suggesting greater variation within than between clades. Taken together with the observation that families with the most distinctive cranial morphologies (nesomyids, dipodids, and spalacids) are the least diverse, indicates that evolution of new cranial morphologies may not play an important role in the diversification of muroid rodents.     

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.     

Contrasting global‐scale evolutionary radiations: phylogeny,diversification, and morphological evolution in the major clades of iguanian lizards

Parallel evolutionary radiations in adjacent locations have been documented in many systems, but typically at limited geographical scales. Here, we compare patterns of evolutionary radiation at the global scale in iguanian lizards, the dominant clade of lizards. We generated a new time‐calibrated phylogeny including 153 iguanian species (based on mitochondrial and nuclear data) and obtained data on morphology and microhabitats. We then compared patterns of species diversification, morphological disparity, and ecomorphological relationships in the predominantly Old World and New World clades (Acrodonta and Pleurodonta, respectively), focusing on the early portions of these radiations. Acrodonts show relatively constant rates of species diversification and disparity over time. In contrast, pleurodonts show an early burst of species diversification and less‐than‐expected morphological disparity early in their history, and slowing diversification and increasing disparity more recently. Analyses including all species (with MEDUSA) suggest accelerated diversification rates in certain clades within both Acrodonta and Pleurodonta, which strongly influences present‐day diversity patterns. We also find substantial differences in ecomorphological relationships between these clades. Our results demonstrate that sister clades in different global regions can undergo very different patterns of evolutionary radiation over similar time frames. © 2012 The Linnean Society of London, Biological Journal of the Linnean Society, 2012, ●● , ●●–●●.     

Relationships of diversity,disparity, and their evolutionary rates in squirrels (Sciuridae)

Several theories predict that rapidly diversifying clades will also rapidly diverge phenotypically; yet, there are also reasons for suspecting that diversification and divergence might not be correlated. In the widely distributed squirrel clade (Sciuridae), we test for correlations between per lineage speciation rates, species richness, disparity, and a time‐invariant measure of disparity that allows for comparing rates when evolutionary modes differ, as they do in squirrels. We find that species richness and speciation rates are not correlated with clade age or with each other. Disparity appears to be positively correlated with clade age because young, rapidly diversifying Nearctic grassland clades are strongly pulled to a single stable optimum but older, slowly diversifying Paleotropical forest clades contain lineages that diverge along multiple ecological and morphological lines. That contrast is likely due to both the environments they inhabit and their phylogenetic community structure. Our results argue against a shared explanation for diversity and disparity in favor of geographically mediated modes of speciation and ecologically mediated modes of phenotypic evolution.     

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.     

Spatial and temporal patterns of phenotypic variation in a Neotropical frog

Aim Studies of the spatial and temporal patterns of phenotypic diversity help to elucidate the fine‐scale evolutionary and ecological mechanisms underlying geographical differentiation. The red‐eyed tree frog, Agalychnis callidryas, is a widespread Neotropical frog that exhibits a broad range of polymorphism of coloration and flank‐stripe pattern. The goal of this study was two‐fold: first, to investigate the stability of polymorphisms over a 38‐year period; and second, to evaluate biogeographical hypotheses of diversification between lower Central American populations through quantification of phenotypic diversity on a fine geographical scale. Location This study was conducted at 12 sites across four biogeographical regions in Costa Rica and Panama. Methods We quantified colour, categorized flank‐stripe pattern from digital photos taken during field sampling, and measured body size for each individual. We compared the regional frequency of each flank‐stripe pattern in 2005 with the frequency distribution from a previous study of the same sites in 1967 using logistic regression analyses. We determined the geographical signal of leg coloration by employing linear discriminant function analyses to generate a classification matrix based on covariance similarities, and by comparison of the average hue values within and between regions. Results We found a temporal shift in the frequency of flank‐stripe patterns in three of four regions over 38 years. Based on measures of leg coloration, the frequency distribution of flank‐stripe patterns and body size, we conclude that A. callidryas populations are easily distinguishable at a regional scale. Main conclusions Agalychnis callidryas exhibits regional differentiation in all phenotypic traits measured in this study, supporting the role of three major biogeographical barriers to gene exchange. We found evidence of a putative contact zone between polytypic regions in Costa Rica. In addition, we report temporal instability of the relative frequency of stripe patterns located on the flanks. The ecological and evolutionary mechanisms that may underlie this variation include sexual selection and avoidance of predators.     

Do habitat shifts drive diversification in teleost fishes? An example from the pufferfishes (Tetraodontidae)

Habitat shifts are implicated as the cause of many vertebrate radiations, yet relatively few empirical studies quantify patterns of diversification following colonization of new habitats in fishes. The pufferfishes (family Tetraodon‐tidae) occur in several habitats, including coral reefs and freshwater, which are thought to provide ecological opportunity for adaptive radiation, and thus provide a unique system for testing the hypothesis that shifts to new habitats alter diversification rates. To test this hypothesis, we sequenced eight genes for 96 species of pufferfishes and closely related porcupine fishes, and added 19 species from sequences available in GenBank. We time‐calibrated the molecular phylogeny using three fossils, and performed several comparative analyses to test whether colonization of novel habitats led to shifts in the rate of speciation and body size evolution, central predictions of clades experiencing ecological adaptive radiation. Colonization of freshwater is associated with lower rates of cladogenesis in pufferfishes, although these lineages also exhibit accelerated rates of body size evolution. Increased rates of cladogenesis are associated with transitions to coral reefs, but reef lineages surprisingly exhibit significantly lower rates of body size evolution. These results suggest that ecological opportunity afforded by novel habitats may be limited for pufferfishes due to competition with other species, constraints relating to pufferfish life history and trophic ecology, and other factors.     

GEOGRAPHIC AND TAXONOMIC DISPARITIES IN SPECIES DIVERSITY: DISPERSAL AND DIVERSIFICATION RATES ACROSS WALLACE'S LINE

Broad‐scale patterns of species diversity have received much attention in the literature, yet the mechanisms behind their formation may not explain species richness disparities across small spatial scales. Few taxa display high species diversity on either side of Wallace's Line and our understanding of the processes causing this biogeographical pattern remains limited, particularly in plant lineages. To understand the evolution of this biogeographical pattern, a time‐calibrated molecular phylogeny of Livistoninae palms (Arecaceae) was used to infer the colonization history of the Sahul tectonic plate region and to test for disparities in diversification rates across taxa and across each side of Wallace's Line. Our analyses allowed us to examine how timing, migration history, and shifts in diversification rates have contributed to shape the biogeographical pattern observed in Livistoninae. We inferred that each of the three genera found in Sahul crossed Wallace's Line only once and relatively recently. In addition, at least two of the three dispersing genera underwent an elevation in their diversification rate leading to high species richness on each side of Wallacea. The correspondence of our results with Southeast Asian geologic and climatic history show how palms emerge as excellent models for understanding the historical formation of fine‐scale biogeographic patterns in a phylogenetic framework.     

Diversification rate shifts in the Cape Floristic Region: The right traits in the right place at the right time

Species diversity patterns are the product of diversification rate variation, but the factors influencing changes in diversification rates are poorly known. Radiation is thought to be the result of ecological opportunity: the right traits in the right environment at the right time. We test this in the Cape Floristic Region (CFR) of South Africa, in which pyrophytic heathland (fynbos) and non-pyrophytic Afromontane forest occur interdigitated. We infer transitions from forest to fynbos in three Cape clades (Penaeaceae, Phyliceae and Diosmeae) and test if they are associated with diversification rate shifts and the evolution of functional traits linked to fire, high insolation and seasonal drought. We estimate diversification rate shifts using maximum likelihood and use phylogenetic comparative methods to show that forest to fynbos shifts were associated with decreases in leaf area and specific leaf area and preceded or coincided with increases in diversification rates. Furthermore, we show that Penaeaceae, Phyliceae and Diosmeae species are typical members of their vegetation types in terms of their traits. The diversification rate shifts of Penaeaceae and Phyliceae are dated to the Miocene, when postulated aridification-driven changes in the CFR fire regimes may have triggered expansion of the fynbos at the cost of forest, providing an ecological opportunity for the diversification of fynbos lineages.     

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.     

Dynamics of clade diversification on the morphological hypercube

Understanding the relationship between taxonomic and morphological changes is important in identifying the reasons for accelerated morphological diversification early in the history of animal phyla. Here, a simple general model describing the joint dynamics of taxonomic diversity and morphological disparity is presented and applied to the data on the diversification of blastozoans. I show that the observed patterns of deceleration in clade diversification can be explicable in terms of the geometric structure of the morphospace and the effects of extinction and speciation on morphological disparity without invoking major declines in the size of morphological transitions or taxonomic turnover rates. The model allows testing of hypotheses about patterns of diversification and estimation of rates of morphological evolution. In the case of blastozoans, I find no evidence that major changes in evolutionary rates and mechanisms are responsible for the deceleration of morphological diversification seen during the period of this clade''s expansion. At the same time, there is evidence for a moderate decline in overall rates of morphological diversification concordant with a major change (from positive to negative values) in the clade''s growth rate.     

Decoupling of taxonomic diversity and morphological disparity during decline of the Cambrian trilobite family Pterocephaliidae

Although discordance between taxonomic diversity and morphological disparity is common, little is known about the underlying dynamics that drive this decoupling. Early in the history of the Cambrian trilobite family Pterocephaliidae, there was an increase in taxonomic diversity and morphological diversity. As taxonomic diversity declined in the later history of the clade, range of variation stayed high and disparity continued to increase. However, per‐branch rates of morphological evolution estimated from a recent phylogeny decreased with time. Neither within‐trait nor within‐species variation increased or decreased, suggesting that the declining rates of morphological evolution were more likely related to ecological opportunity or niche partitioning, rather than increasing intrinsic constraints. This is further supported by evidence for increased biofacies associations throughout the time period. Thus, the high disparity seen at low taxonomic diversity late in the history of this clade was due to extinction – either random or targeting mean forms – rather than increased rates of morphological evolution. This pattern also provides a scenario that could account for instances of low taxonomic diversity but high morphological disparity in modern groups.     

Allometric disparity in rodent evolution

In this study, allometric trajectories for 51 rodent species, comprising equal representatives from each of the major clades (Ctenohystrica, Muroidea, Sciuridae), are compared in a multivariate morphospace (=allometric space) to quantify magnitudes of disparity in cranial growth. Variability in allometric trajectory patterns was compared to measures of adult disparity in each clade, and dietary habit among the examined species, which together encapsulated an ecomorphological breadth. Results indicate that the evolution of allometric trajectories in rodents is characterized by different features in sciurids compared with muroids and Ctenohystrica. Sciuridae was found to have a reduced magnitude of inter‐trajectory change and growth patterns with less variation in allometric coefficient values among members. In contrast, a greater magnitude of difference between trajectories and an increased variation in allometric coefficient values was evident for both Ctenohystrica and muroids. Ctenohystrica and muroids achieved considerably higher adult disparities than sciurids, suggesting that conservatism in allometric trajectory modification may constrain morphological diversity in rodents. The results provide support for a role of ecology (dietary habit) in the evolution of allometric trajectories in rodents.     

Biogeographical network analysis of plant species distribution in the Mediterranean region

The delimitation of bioregions helps to understand historical and ecological drivers of species distribution. In this work, we performed a network analysis of the spatial distribution patterns of plants in south of France (Languedoc‐Roussillon and Provence‐Alpes‐Côte d'Azur) to analyze the biogeographical structure of the French Mediterranean flora at different scales. We used a network approach to identify and characterize biogeographical regions, based on a large database containing 2.5 million of geolocalized plant records corresponding to more than 3,500 plant species. This methodology is performed following five steps, from the biogeographical bipartite network construction to the identification of biogeographical regions under the form of spatial network communities, the analysis of their interactions, and the identification of clusters of plant species based on the species contribution to the biogeographical regions. First, we identified two sub‐networks that distinguish Mediterranean and temperate biota. Then, we separated eight statistically significant bioregions that present a complex spatial structure. Some of them are spatially well delimited and match with particular geological entities. On the other hand, fuzzy transitions arise between adjacent bioregions that share a common geological setting, but are spread along a climatic gradient. The proposed network approach illustrates the biogeographical structure of the flora in southern France and provides precise insights into the relationships between bioregions. This approach sheds light on ecological drivers shaping the distribution of Mediterranean biota: The interplay between a climatic gradient and geological substrate shapes biodiversity patterns. Finally, this work exemplifies why fragmented distributions are common in the Mediterranean region, isolating groups of species that share a similar eco‐evolutionary history.