Comparative analyses for adaptive radiations

Biologists generally agree that most morphological variation between closely related species is adaptive. The most common method of comparative analysis to test for co-evolved character variation is based on a Brownian-motion model of character evolution. If we are to test for the evolution of character-covariation, and we believe that characters have evolved adaptively to fill niches during an adaptive radiation, then it is appropriate to employ appropriate models for character evolution. We show here that under several models of adaptive character evolution and coevolution during an adaptive radiation, which result in closely related species being more similar to each other than to more distantly related species, cross-species analyses are statistically more appropriate than contrast analyses. If the evolution of some traits fits the Brownian-motion model, while others evolve to fill niches during an adaptive radiation, it might be necessary to identify the number of relevant niche dimensions and the modes of character evolution before deciding on appropriate statistical procedures. Alternatively, maximum-likelihood procedures might be used to determine appropriate transformations of phylogenetic branch lengths that accord with particular models of character evolution.     

Taxon sampling, correlated evolution, and independent contrasts

Independent contrasts are widely used to incorporate phylogenetic information into studies of continuous traits, particularly analyses of evolutionary trait correlations, but the effects of taxon sampling on these analyses have received little attention. In this paper, simulations were used to investigate the effects of taxon sampling patterns and alternative branch length assignments on the statistical performance of correlation coefficients and sign tests; "full-tree" analyses based on contrasts at all nodes and "paired-comparisons" based only on contrasts of terminal taxon pairs were also compared. The simulations showed that random samples, with respect to the traits under consideration, provide statistically robust estimates of trait correlations. However, exact significance tests are highly dependent on appropriate branch length information; equal branch lengths maintain lower Type I error than alternative topological approaches, and adjusted critical values of the independent contrast correlation coefficient are provided for use with equal branch lengths. Nonrandom samples, with respect to univariate or bivariate trait distributions, introduce discrepancies between interspecific and phylogenetically structured analyses and bias estimates of underlying evolutionary correlations. Examples of nonrandom sampling processes may include community assembly processes, convergent evolution under local adaptive pressures, selection of a nonrandom sample of species from a habitat or life-history group, or investigator bias. Correlation analyses based on species pairs comparisons, while ignoring deeper relationships, entail significant loss of statistical power and as a result provide a conservative test of trait associations. Paired comparisons in which species differ by a large amount in one trait, a method introduced in comparative plant ecology, have appropriate Type I error rates and high statistical power, but do not correctly estimate the magnitude of trait correlations. Sign tests, based on full-tree or paired-comparison approaches, are highly reliable across a wide range of sampling scenarios, in terms of Type I error rates, but have very low power. These results provide guidance for selecting species and applying comparative methods to optimize the performance of statistical tests of trait associations.     

Rates of phenotypic evolution of ecological characters and sexual traits during the Tanganyikan cichlid adaptive radiation

Theory suggests that sexual traits evolve faster than ecological characters. However, characteristics of a species niche may also influence evolution of sexual traits. Hence, a pending question is whether ecological characters and sexual traits present similar tempo and mode of evolution during periods of rapid ecological divergence, such as adaptive radiation. Here, we use recently developed phylogenetic comparative methods to analyse the temporal dynamics of evolution for ecological and sexual traits in Tanganyikan cichlids. Our results indicate that whereas disparity in ecological characters was concentrated early in the radiation, disparity in sexual traits remained high throughout the radiation. Thus, closely related Tanganyikan cichlids presented higher disparity in sexual traits than ecological characters. Sexual traits were also under stronger selection than ecological characters. In sum, our results suggest that ecological characters and sexual traits present distinct evolutionary patterns, and that sexual traits can evolve faster than ecological characters, even during adaptive radiation.     

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.     

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.     

Are species adapted to their regeneration niche, adult niche, or both?

Functional traits are important drivers of successional processes and the assembly of plant communities. It is generally assumed that functional traits are closely linked to the regeneration niche because of the high selection pressures in the seedling stage, but recent studies have challenged this view. In this study, I use cross species and phylogenetic correlation analysis between leaf traits and light environment to evaluate whether species are adapted to the regeneration niche, adult niche, or both. Leaf chemistry, morphology, physiology, and crown exposure were quantified for up to 58 Bolivian tropical moist forest tree species that differ in their regeneration and adult light niche. Multiple regression analysis shows that leaf traits of seedlings, saplings, and trees are most strongly related to the regeneration niche, and once this is taken into account, adult niche does not significantly explain any of the remaining variation in leaf traits. This suggests that, although the regeneration phase is short, it has a long-lasting effect on the form and shape of plant species.     

Ecology and macroevolution – evolutionary niche monopolisation as a mechanisms of niche conservatism

Explaining macroevolution from microevolution is a key issue in contemporary evolutionary theory. A recurrent macroevolutionary pattern is that some niche‐related traits consistently evolve slower than others, so called niche conservatism. Despite a growing amount of data, the underlying evolutionary processes are not fully understood. I here analyse adaptive radiations in an individual‐based eco‐evolutionary model. I find a coevolutionary mechanism – evolutionary niche monopolisation – as a possibly important generator of niche conservatism. A single lineage of a radiating clade can monopolise, and later diversify within, a substantial part of the available niche space – much larger than what can be explained by limiting similarity. This leads to niche conservatism, since no species evolves into or out of the monopolised region. The region can in this sense also be described as an adaptive zone. The model indicates that evolutionary niche monopolisation is operative in a large part of parameter space, underlining its possible importance. The mechanism is driven by competitive interactions and differences in niche widths in alternative niche dimensions. I discuss plausible examples of evolutionary niche monopolisation in well‐studied natural systems.     

A Unimodal Species Response Model Relating Traits to Environment with Application to Phytoplankton Communities

In this paper we attempt to explain observed niche differences among species (i.e. differences in their distribution along environmental gradients) by differences in trait values (e.g. volume) in phytoplankton communities. For this, we propose the trait-modulated Gaussian logistic model in which the niche parameters (optimum, tolerance and maximum) are made linearly dependent on species traits. The model is fitted to data in the Bayesian framework using OpenBUGS (Bayesian inference Using Gibbs Sampling) to identify according to which environmental variables there is niche differentiation among species and traits. We illustrate the method with phytoplankton community data of 203 lakes located within four climate zones and associated measurements on 11 environmental variables and six morphological species traits of 60 species. Temperature and chlorophyll-a (with opposite signs) described well the niche structure of all species. Results showed that about 25% of the variance in the niche centres with respect to chlorophyll-a were accounted for by traits, whereas niche width and maximum could not be predicted by traits. Volume, mucilage, flagella and siliceous exoskeleton are found to be the most important traits to explain the niche centres. Species were clustered in two groups with different niches structures, group 1 high temperature-low chlorophyll-a species and group 2 low temperature-high chlorophyll-a species. Compared to group 2, species in group 1 had larger volume but lower surface area, had more often flagella but neither mucilage nor siliceous exoskeleton. These results might help in understanding the effect of environmental changes on phytoplankton community. The proposed method, therefore, can also apply to other aquatic or terrestrial communities for which individual traits and environmental conditioning factors are available.     

ASYNCHRONOUS EVOLUTION OF PHYSIOLOGY AND MORPHOLOGY IN ANOLIS LIZARDS

Species‐rich adaptive radiations typically diversify along several distinct ecological axes, each characterized by morphological, physiological, and behavioral adaptations. We test here whether different types of adaptive traits share similar patterns of evolution within a radiation by investigating patterns of evolution of morphological traits associated with microhabitat specialization and of physiological traits associated with thermal biology in Anolis lizards. Previous studies of anoles suggest that close relatives share the same “structural niche” (i.e., use the same types of perches) and are similar in body size and shape, but live in different “climatic niches” (i.e., use habitats with different insolation and temperature profiles). Because morphology is closely tied to structural niche and field active body temperatures are tied to climatic niches in Anolis, we expected phylogenetic analyses to show that morphology is more evolutionarily conservative than thermal physiology. In support of this hypothesis, we find (1) that thermal biology exhibits more divergence among recently diverged Anolis taxa than does morphology; and (2) diversification of thermal biology among all species often follows diversification in morphology. These conclusions are remarkably consistent with predictions made by anole biologists in the 1960s and 1970s.     

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.     

The relationship between geographic range size and life history traits: is biogeographic history uncovered? A test using the Iberian butterflies

The geographic range of a species is influenced by past phylogenetic and biogeographic patterns. However, other historical interactions, including the interplay between life history and geography, are also likely involved. Therefore, the range size of a species can be explained on the basis of niche‐breadth or dispersal related hypotheses, and previous work on European butterflies suggests that both, under the respective guise of ecological specialisation and colonising ability may apply. In the present study, data from 205 species of butterflies from the Iberian peninsula were processed through multiple regression analyses to test for correlations between geographic range size, life history traits and geographic features of the species distribution types. In addition, the percentage of variance explained by the subsets of variables analyzed in the study, with and without control for phylogenetic effects was tested. Despite a complex pattern of bivariate correlations, we found that larval polyphagy was the single best correlate of range size, followed by dispersal. Models that combined both life history traits and geographic characteristics performed better than models generated independently. The combined variables explained at least 39% of the variance. Bivariate correlations between range size and body size, migratory habits or egg size primarily reflected taxonomic patterning and reciprocal correlations with larval diet breadth and adult phenology. Therefore, aspects of niche breadth i.e. potential larval diet breadth emerged as the most influential determinants of range size. However, the relationships between these types of ecological traits and biogeographic history must still be considered when associations between life history and range size are of interest.     

The coexistence of fish species in streams: relationships between assemblage attributes and trophic and environmental variables

Diet overlap and niche breadth are well-known species traits from trophic ecology that can assist in explaining how species interact and coexist as well as the ecological mechanisms that influence biodiversity. In the present study, we analyzed the relationships between these trophic variables and indicators of resource availability with some attributes of fish assemblages (species richness, Shannon diversity index, evenness, density and individual body size). The physical and chemical characteristics of the biotopes (topography, water quality and conservation of slopes) were examined to identify possible patterns. Monthly sampling using electrofishing was conducted in 2003 along five streams located in the Cuiabá River watershed. The relationships between environmental variables and attributes of fish assemblages were evaluated using Spearman correlation. Species richness and abundance varied among streams, with higher values (54 and 82 species) found in low-gradient streams that drained small swampy areas discharging in Cuiabá River. Diet overlap showed significant and negative correlations with species richness, the diversity index, abundance, variation in body size and food availability and positive correlations with evenness and niche breadth. Environments that had greater food availability had a reduced variety of food items (smaller amplitude) and distinct values in terms of dietary overlap. Nevertheless, to explain resource partitioning in a fish assemblage (overlap), it is necessary to consider food availability and niche breadth (degree of trophic specialization) beyond the interaction of these variables with species richness and density. In conclusion, high diversity and abundance values were strongly associated with a high degree of trophic specialization (low amplitude of trophic niche) and a small degree of overlap in the diet.     

The role of ecological opportunity in shaping disparate diversification trajectories in a bicontinental primate radiation

Exceptional species and phenotypic diversity commonly are attributed to ecological opportunity (EO). The conventional EO model predicts that rates of lineage diversification and phenotypic evolution are elevated early in a radiation only to decline later in response to niche availability. Foregut fermentation is hypothesized to be a key innovation that allowed colobine monkeys (subfamily Colobinae), the only primates with this trait, to successfully colonize folivore adaptive zones unavailable to other herbivorous species. Therefore, diversification rates also are expected to be strongly linked with the evolution of traits related to folivory in these monkeys. Using dated molecular phylogenies and a dataset of feeding morphology, I test predictions of the EO model to evaluate the role of EO conferred by foregut fermentation in shaping the African and Asian colobine radiations. Findings from diversification methods coupled with colobine biogeographic history provide compelling evidence that decreasing availability of new adaptive zones during colonization of Asia together with constraints presented by dietary specialization underlie temporal changes in diversification in the Asian but not African clade. Additionally, departures from the EO model likely reflect iterative diversification events in Asia.     

Relationships between geographical range size, body size, local abundance, and habitat breadth in North American suckers and sunfishes

Aim I examine the relationship between geographical range size and three variables (body size, an index of habitat breadth, and an index of local abundance) within a phylogenetic framework in North American species of suckers and sunfishes. Location North America Methods Regressions after independent contrasts of geographical range size, body size, habitat breadth, and local abundance. Results Species with large range sizes tend to be larger-bodied, be more locally abundant, and have higher habitat breadths. Character reconstructions support the prediction that variables associated with rarity (small geographical range size, low local abundance, low niche breadth, and large body size) evolve in unison, although large body size was associated with the opposite traits in these taxa. Gaston & Blackburn (1996a) suggested using visual identification of the lower boundary of the geographical range-body size relationship to identify extinction-prone species; this resulted in thirteen species that are potentially extinction-prone. Main conclusions Similar evolutionary mechanisms appear to operate on body size and other variables related to rarity, even in distantly related taxa.     

DOES NICHE DIVERGENCE ACCOMPANY ALLOPATRIC DIVERGENCE IN APHELOCOMA JAYS AS PREDICTED UNDER ECOLOGICAL SPECIATION?: INSIGHTS FROM TESTS WITH NICHE MODELS

The role of ecology in the origin of species has been the subject of long‐standing interest to evolutionary biologists. New sources of spatially explicit ecological data allow for large‐scale tests of whether speciation is associated with niche divergence or whether closely related species tend to be similar ecologically (niche conservatism). Because of the confounding effects of spatial autocorrelation of environmental variables, we generate null expectations for niche divergence for both an ecological‐niche modeling and a multivariate approach to address the question: do allopatrically distributed taxa occupy similar niches? In a classic system for the study of niche evolution—the Aphelocoma jays—we show that there is little evidence for niche divergence among Mexican Jay (A. ultramarina) lineages in the process of speciation, contrary to previous results. In contrast, Aphelocoma species that exist in partial sympatry in some regions show evidence for niche divergence. Our approach is widely applicable to the many cases of allopatric lineages in the beginning stages of speciation. These results do not support an ecological speciation model for Mexican Jay lineages because, in most cases, the allopatric environments they occupy are not significantly more divergent than expected under a null model.     

Developmental life history is associated with variation in rates of climatic niche evolution in a salamander adaptive radiation*

Rates of climatic niche evolution vary widely across the tree of life and are strongly associated with rates of diversification among clades. However, why the climatic niche evolves more rapidly in some clades than others remains unclear. Variation in life history traits often plays a key role in determining the environmental conditions under which species can survive, and therefore, could impact the rate at which lineages can expand in available climatic niche space. Here, we explore the relationships among life-history variation, climatic niche breadth, and rates of climatic niche evolution. We reconstruct a phylogeny for the genus Desmognathus, an adaptive radiation of salamanders distributed across eastern North America, based on nuclear and mitochondrial genes. Using this phylogeny, we estimate rates of climatic niche evolution for species with long, short, and no aquatic larval stage. Rates of climatic niche evolution are unrelated to the mean climatic niche breadth of species with different life histories. Instead, we find that the evolution of a short larval period promotes greater exploration of climatic space, leading to increased rates of climatic niche evolution across species having this trait. We propose that morphological and physiological differences associated with variation in larval stage length underlie the heterogeneous ability of lineages to explore climatic niche space. Rapid rates of climatic niche evolution among species with short larval periods were an important dimension of the clade's adaptive radiation and likely contributed to the rapid rate of lineage accumulation following the evolution of an aquatic life history in this clade. Our results show how variation in a key life-history trait can constrain or promote divergence of the climatic niche, leading to variation in rates of climatic niche evolution among species.     

Sexual selection and natural selection in bird speciation

The role of sexual selection in speciation is investigated, addressing two main issues. First, how do sexually selected traits become species recognition traits? Theory and empirical evidence suggest that female preferences often do not evolve as a correlated response to evolution of male traits. This implies that, contrary to runaway (Fisherian) models of sexual selection, premating isolation will not arise as an automatic side effect of divergence between populations in sexually selected traits. I evaluate premating isolating mechanisms in one group, the birds. In this group premating isolation is often a consequence of sexual imprinting, whereby young birds learn features of their parents and use these features in mate choice. Song, morphology and plumage are known recognition cues. I conclude that perhaps the main role for sexual selection in speciation is in generating differences between populations in traits. Sexual imprinting then leads to these traits being used as species recognition mechanisms. The second issue addressed in this paper is the role of sexual selection in adaptive radiation, again concentrating on birds. Ecological differences between species include large differences in size, which may in themselves be sufficient for species recognition, and differences in habitat, which seem to evolve frequently and at all stages of an adaptive radiation. Differences in habitat often cause song and plumage patterns to evolve as a result of sexual selection for efficient communication. Therefore sexual selection is likely to have an important role in generating premating isolating mechanisms throughout an adaptive radiation. It is also possible that sexual selection, by creating more allopatric species, creates more opportunity for ecological divergence to occur. The limited available evidence does not support this idea. A role for sexual selection in accelerating ecological diversification has yet to be demonstrated.     

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.     

Crater lake cichlids individually specialize along the benthic–limnetic axis

A common pattern of adaptive diversification in freshwater fishes is the repeated evolution of elongated open water (limnetic) species and high‐bodied shore (benthic) species from generalist ancestors. Studies on phenotype‐diet correlations have suggested that population‐wide individual specialization occurs at an early evolutionary and ecological stage of divergence and niche partitioning. This variable restricted niche use across individuals can provide the raw material for earliest stages of sympatric divergence. We investigated variation in morphology and diet as well as their correlations along the benthic‐limnetic axis in an extremely young Midas cichlid species, Amphilophus tolteca, endemic to the Nicaraguan crater lake Asososca Managua. We found that A. tolteca varied continuously in ecologically relevant traits such as body shape and lower pharyngeal jaw morphology. The correlation of these phenotypes with niche suggested that individuals are specialized along the benthic‐limnetic axis. No genetic differentiation within the crater lake was detected based on genotypes from 13 microsatellite loci. Overall, we found that individual specialization in this young crater lake species encompasses the limnetic‐ as well as the benthic macro‐habitat. Yet there is no evidence for any diversification within the species, making this a candidate system for studying what might be the early stages preceding sympatric divergence.     

Trait adaptation promotes species coexistence in diverse predator and prey communities

Species can adjust their traits in response to selection which may strongly influence species coexistence. Nevertheless, current theory mainly assumes distinct and time‐invariant trait values. We examined the combined effects of the range and the speed of trait adaptation on species coexistence using an innovative multispecies predator–prey model. It allows for temporal trait changes of all predator and prey species and thus simultaneous coadaptation within and among trophic levels. We show that very small or slow trait adaptation did not facilitate coexistence because the stabilizing niche differences were not sufficient to offset the fitness differences. In contrast, sufficiently large and fast trait adaptation jointly promoted stable or neutrally stable species coexistence. Continuous trait adjustments in response to selection enabled a temporally variable convergence and divergence of species traits; that is, species became temporally more similar (neutral theory) or dissimilar (niche theory) depending on the selection pressure, resulting over time in a balance between niche differences stabilizing coexistence and fitness differences promoting competitive exclusion. Furthermore, coadaptation allowed prey and predator species to cluster into different functional groups. This equalized the fitness of similar species while maintaining sufficient niche differences among functionally different species delaying or preventing competitive exclusion. In contrast to previous studies, the emergent feedback between biomass and trait dynamics enabled supersaturated coexistence for a broad range of potential trait adaptation and parameters. We conclude that accounting for trait adaptation may explain stable and supersaturated species coexistence for a broad range of environmental conditions in natural systems when the absence of such adaptive changes would preclude it. Small trait changes, coincident with those that may occur within many natural populations, greatly enlarged the number of coexisting species.