Phylogenetic perspectives on reef fish functional traits

Functional traits have been fundamental to the evolution and diversification of entire fish lineages on coral reefs. Yet their relationship with the processes promoting speciation, extinction and the filtering of local species pools remains unclear. We review the current literature exploring the evolution of diet, body size, water column use and geographic range size in reef‐associated fishes. Using published and new data, we mapped functional traits on to published phylogenetic trees to uncover evolutionary patterns that have led to the current functional diversity of fishes on coral reefs. When examining reconstructed patterns for diet and feeding mode, we found examples of independent transitions to planktivory across different reef fish families. Such transitions and associated morphological alterations may represent cases in which ecological opportunity for the exploitation of different resources drives speciation and adaptation. In terms of body size, reconstructions showed that both large and small sizes appear multiple times within clades of mid‐sized fishes and that extreme body sizes have arisen mostly in the last 10 million years (Myr). The reconstruction of range size revealed many cases of disparate range sizes among sister species. Such range size disparity highlights potential vicariant processes through isolation in peripheral locations. When accounting for peripheral speciation processes in sister pairs, we found a significant relationship between labrid range size and lineage age. The diversity and evolution of traits within lineages is influenced by trait–environment interactions as well as by species and trait–trait interactions, where the presence of a given trait may trigger the development of related traits or behaviours. Our effort to assess the evolution of functional diversity across reef fish clades adds to the burgeoning research focusing on the evolutionary and ecological roles of functional traits. We argue that the combination of a phylogenetic and a functional approach will improve the understanding of the mechanisms of species assembly in extraordinarily rich coral reef communities.     

Adaptive processes drive ecomorphological convergent evolution in antwrens (Thamnophilidae)

Phylogenetic niche conservatism (PNC) and convergence are contrasting evolutionary patterns that describe phenotypic similarity across independent lineages. Assessing whether and how adaptive processes give origin to these patterns represent a fundamental step toward understanding phenotypic evolution. Phylogenetic model‐based approaches offer the opportunity not only to distinguish between PNC and convergence, but also to determine the extent that adaptive processes explain phenotypic similarity. The Myrmotherula complex in the Neotropical family Thamnophilidae is a polyphyletic group of sexually dimorphic small insectivorous forest birds that are relatively homogeneous in size and shape. Here, we integrate a comprehensive species‐level molecular phylogeny of the Myrmotherula complex with morphometric and ecological data within a comparative framework to test whether phenotypic similarity is described by a pattern of PNC or convergence, and to identify evolutionary mechanisms underlying body size and shape evolution. We show that antwrens in the Myrmotherula complex represent distantly related clades that exhibit adaptive convergent evolution in body size and divergent evolution in body shape. Phenotypic similarity in the group is primarily driven by their tendency to converge toward smaller body sizes. Differences in body size and shape across lineages are associated to ecological and behavioral factors.     

Environmental and scale-dependent evolutionary trends in the body size of crustaceans

The ecological and physiological significance of body size is well recognized. However, key macroevolutionary questions regarding the dependency of body size trends on the taxonomic scale of analysis and the role of environment in controlling long-term evolution of body size are largely unknown. Here, we evaluate these issues for decapod crustaceans, a group that diversified in the Mesozoic. A compilation of body size data for 792 brachyuran crab and lobster species reveals that their maximum, mean and median body size increased, but no increase in minimum size was observed. This increase is not expressed within lineages, but is rather a product of the appearance and/or diversification of new clades of larger, primarily burrowing to shelter-seeking decapods. This argues against directional selective pressures within lineages. Rather, the trend is a macroevolutionary consequence of species sorting: preferential origination of new decapod clades with intrinsically larger body sizes. Furthermore, body size evolution appears to have been habitat-controlled. In the Cretaceous, reef-associated crabs became markedly smaller than those in other habitats, a pattern that persists today. The long-term increase in body size of crabs and lobsters, coupled with their increased diversity and abundance, suggests that their ecological impact may have increased over evolutionary time.     

Body size and coexistence in gamasid mites parasitic on small mammals: null model analyses at three hierarchical scales

We studied body size ratio in gamasid mites (Acari: Mesostigmata) parasitic on Palearctic small mammals at 3 hierarchical scales, namely infracommunities (an assemblage of mites harboured by an individual host), component communities (an assemblage of mites harboured by a host population), and compound communities (an assemblage of mites harboured by a host community). We used null models and asked a) whether body size distributions in these communities demonstrate non‐random patterns; b) whether these patterns indicate segregation or aggregation of body sizes of coexisting species; and c) whether patterns of body size distribution are scale‐dependent, that is, differ among infracommunities, component communities, and compound communities. In most mite assemblages, the observed pattern of body size distribution did not differ from that expected by chance. However, meta‐analyses demonstrated that component and compound communities of gamasid mites consistently demonstrated a tendency to reduced body size overlap, while we did not find any clear trend in mite body size distribution across infracommunities. We discuss reasons for scale‐dependence of body size distribution pattern in parasite communities and propose ecological and evolutionary mechanisms that allowed the reduced body size overlap in component and compound communities of ectoparasites to arise.     

The geography of body size – challenges of the interspecific approach

Recent compilations of large-scale data bases on the geographical distributions and body sizes of animals, coupled with developments in spatial statistics, have led to renewed interest in the geographical distribution of animal body sizes and the interspecific version of Bergmann's rule. Standard practice seems to be an examination of mean body sizes within higher taxa on gridded maps, with little regard to species richness or phylogeny. However, because the frequency distribution of body sizes is typically highly skewed, average size within grid cells may differ significantly between species-rich and species-poor cells even when the median and modal sizes remain constant. Species richness influences body size patterns because species are not added to communities at random in relation to their size: areas of low diversity are characterized by a higher range of body sizes than is expected by chance. Finally, a consideration of phylogenetic structure within taxa is necessary to elucidate whether patterns in the geography of size result from turnover between or within intermediate taxonomic levels. We suggest that the highest and lowest quantiles of body size distribution be mapped in order to expose possible physiological or ecological limitations on body size.     

Using sensitivity analysis to identify keystone species and keystone links in size‐based food webs

Human‐induced alterations in the birth and mortality rates of species and in the strength of interactions within and between species can lead to changes in the structure and resilience of ecological communities. Recent research points to the importance of considering the distribution of body sizes of species when exploring the response of communities to such perturbations. Here, we present a new size‐based approach for assessing the sensitivity and elasticity of community structure (species equilibrium abundances) and resilience (rate of return to equilibrium) to changes in the intrinsic growth rate of species and in the strengths of species interactions. We apply this approach on two natural systems, the pelagic communities of the Baltic Sea and Lake Vättern, to illustrate how it can be used to identify potential keystone species and keystone links. We find that the keystone status of a species is closely linked to its body size. The analysis also suggests that communities are structurally and dynamically more sensitive to changes in the effects of prey on their consumers than in the effects of consumers on their prey. Moreover, we discuss how community sensitivity analysis can be used to study and compare the fragility of communities with different body size distributions by measuring the mean sensitivity or elasticity over all species or all interaction links in a community. We believe that the community sensitivity analysis developed here holds some promise for identifying species and links that are critical for the structural and dynamic robustness of ecological communities.     

THE MICRO AND MACRO IN BODY SIZE EVOLUTION

The diversity of body sizes of organisms has traditionally been explained in terms of microevolutionary processes: natural selection owing to differential fitness of individual organisms, or to macroevolutionary processes: species selection owing to the differential proliferation of phylogenetic lineages. Data for terrestrial mammals and birds indicate that even on a logarithmic scale frequency distributions of body mass among species are significantly skewed towards larger sizes. We used simulation models to evaluate the extent to which macro- and microevolutionary processes are sufficient to explain these distributions. Simulations of a purely cladogenetic process with no bias in extinction or speciation rates for different body sizes did not produce skewed log body mass distributions. Simulations that included size-biased extinction rates, especially those that incorporated anagenetic size change within species between speciation and extinction events, regularly produced skewed distributions. We conclude that although cladogenetic processes probably play a significant role in body size evolution, there must also be a significant anagenetic component. The regular variation in the form of mammalian body size distributions among different-sized islands and continents suggests that environmental conditions, operating through both macro- and microevolutionary processes, determine to a large extent the diversification of body sizes within faunas. Macroevolution is not decoupled from microevolution.     

Body size distribution in flea communities harboured by Siberian small mammals as affected by host species,host sex and scale: scale matters the most

The distribution of body sizes of co-existing species at different scales reflects the scale-dependency of rules governing community assembly. Investigation of among-scale variation in community assembly is impeded by the methodological difficulties of establishing scale boundaries. Studying body size distribution in parasites allows us to avoid the problem of defining scale because parasite communities have clear boundaries and are represented by infracommunities (an assemblage harboured by an individual host), component communities (an assemblage harboured by a host population in a locality), and compound communities (an assemblage harboured by a host community in a locality). We studied body size distribution of fleas parasitic on small mammals in Western Siberia using null models. We asked whether body size ratios (i.e., size differences among coexisting species) in these communities demonstrate non-random segregated or aggregated patterns and whether these patterns differ between (a) host species, (b) host sexes and (c) infra-, component, and compound communities. No effect of host sex on the pattern of body size distribution was found at either scale, whereas an effect of host species was found in infracommunities only. We found a tendency of flea infracommunities toward segregation, whereas body size distributions in component and compound communities were consistently aggregated. We propose that the former could be caused by apparent competition (=?negative indirect interactions among fleas due to shared natural enemy, i.e. a host), whereas we the latter could be explained by host- and environment-associated filtering (=?factors restricting co-occurring species to a certain subset that share certain traits). We conclude that, counterintuitively, flea communities at the lowest hierarchical scale are mainly governed by evolutionary mechanisms, whereas communities at higher scale are assembled via ecological processes.     

Assembly of local communities: consequences of an optimal body size for the organization of competitively structured communities

Much empirical evidence suggests that there is an optimal body size for mammals and that this optimum is in the vicinity of l00g. This presumably reflects an underlying fitness function that is greatest at this mass. Here, I combine such a fitness function with an equilibrium model of competitive character displacement to assess the potential influence of a globally optimal body size in structuring local ecological communities. The model accurately predicts the range of body sizes and the average difference in size for species in communities of varying species richness. The model also predicts a uniform spacing of body sizes, rather than the gaps and clumps in the sizes of coexisting species observed in real communities. Alternative explanations for this phenomenon are discussed. The allometric relationships that result in a body size optimum subsume a large number of characteristics associated with the physiological, behavioral, demographic, and evolutionary dynamics of the species. Further integration of the underlying dynamics (e.g. individual energetics) of these relationships into all hierarchical levels of ecology will have to incorporate multiple interactive sites, spatial heterogeneity, and phylogenetic structure, but it has the potential to provide important discoveries into the means by which natural selection operates.     

Local extinctions may be evidenced by the holes of the morphometric hypervolume in dung beetle communities

The body shape of a species is associated with its evolutionary history and can reflect behavioural peculiarities related to the ecological niche of each species. Morphology can characterise the morphometric niche of species and can be represented as body shape points within a morphometric universe. This information can be to calculate the morphometric diversity of communities through hypervolume metrics, and the hole sizes that remain in the morphometric hypervolume, which are empty areas with no species. Such holes may be ‘natural’ or caused by a local extinction. In this study, we evaluate the ecological community of dung beetles through the lens of morphometric diversity. We evaluated 38 dung beetle species from 30 subtropical communities in southern Brazil sampled in the summer of 2015, including 15 forest remnant communities from the Atlantic Forest and 15 communities from adjacent maize cultivations. The shape of 495 dung beetle specimens was measured using geometric morphometric and hypervolume techniques to calculate the morphometric diversity and the hole size of each of the 30 communities. We found that the taxonomic diversity positively correlated with the morphometric diversity and negatively correlated with the size of the holes. We also found that forest communities had higher values of morphometric diversity and smaller holes in the hypervolume than the maize cultivation communities, suggesting that local extinction may reduce community body shape spaces.     

Similarity of mammalian body size across the taxonomic hierarchy and across space and time

Although it is commonly assumed that closely related animals are similar in body size, the degree of similarity has not been examined across the taxonomic hierarchy. Moreover, little is known about the variation or consistency of body size patterns across geographic space or evolutionary time. Here, we draw from a data set of terrestrial, nonvolant mammals to quantify and compare patterns across the body size spectrum, the taxonomic hierarchy, continental space, and evolutionary time. We employ a variety of statistical techniques including "sib-sib" regression, phylogenetic autocorrelation, and nested ANOVA. We find an extremely high resemblance (heritability) of size among congeneric species for mammals over approximately 18 g; the result is consistent across the size spectrum. However, there is no significant relationship among the body sizes of congeneric species for mammals under approximately 18 g. We suspect that life-history and ecological parameters are so tightly constrained by allometry at diminutive size that animals can only adapt to novel ecological conditions by modifying body size. The overall distributions of size for each continental fauna and for the most diverse orders are quantitatively similar for North America, South America, and Africa, despite virtually no overlap in species composition. Differences in ordinal composition appear to account for quantitative differences between continents. For most mammalian orders, body size is highly conserved, although there is extensive overlap at all levels of the taxonomic hierarchy. The body size distribution for terrestrial mammals apparently was established early in the Tertiary, and it has remained remarkably constant over the past 50 Ma and across the major continents. Lineages have diversified in size to exploit environmental opportunities but only within limits set by allometric, ecological, and evolutionary constraints.     

Cryptic lineage diversity,body size divergence,and sympatry in a species complex of Australian lizards (Gehyra)

Understanding the joint evolutionary and ecological underpinnings of sympatry among close relatives remains a key challenge in biology. This problem can be addressed through joint phylogenomic and phenotypic analysis of complexes of closely related lineages within, and across, species and hence representing the speciation continuum. For a complex of tropical geckos from northern Australia—Gehyra nana and close relatives—we combine mtDNA phylogeography, exon‐capture sequencing, and morphological data to resolve independently evolving lineages and infer their divergence history and patterns of morphological evolution. Gehyra nana is found to include nine divergent lineages and is paraphyletic with four other species from the Kimberley region of north‐west Australia. Across these 13 taxa, 12 of which are restricted to rocky habitats, several lineages overlap geographically, including on the diverse Kimberley islands. Morphological evolution is dominated by body size shifts, and both body size and shape have evolved gradually across the group. However, larger body size shifts are observed among overlapping taxa than among closely related parapatric lineages of G. nana, and sympatric lineages are more divergent than expected at random. Whether elevated body size differences among sympatric lineages are due to ecological sorting or character displacement remains to be determined.     

Extinctions,traits and phylogenetic community structure: insights from primate assemblages in Madagascar

Understanding the origin and maintenance of community composition through ecological and evolutionary time has been a central challenge in ecology. However little is known about how extinction may alter patterns of phylogenetic and phenotypic structure within communities. To address this, we used past and present primate communities in Madagascar as our model system to explore how a large extinction event within a taxon may alter evolutionary relationships and phenotypic distributions within communities. We also explored the influence of environment on the structure of present‐day lemur communities. We found a phylogenetic pattern of overdispersion in both past and present‐day communities. However, trait structures, including relative dispersion of body masses and trophic niches were altered following extinction. We posit that the overdispersed phylogenetic patterns have resulted from the unique ecological and evolutionary history of Madagascar's primates including a rapid adaptive radiation in the presence of a broad niche‐space available during colonization. Differences in trait structures between present and past primate communities may be reflective of the selective extinction process that eliminated the largest primates from the island. Habitat also appeared to influence the structure of present‐day lemur communities. Lower divergence in patterns of phylogeny, body mass and activity rhythms were found in dry relative to wet habitats. This may be due to potential advantages of being small and nocturnal in environments with low productivity and hot dry climates. We suggest current studies exploring community processes should consider potential effects of past extinction events. Such work is important for understanding community assembly, coexistence, and mechanisms driving extinctions, particularly given the current extinction crisis facing ecosystems globally.     

Evolutionary trends in body size of parasitic flatworms

Evolutionary trends in body size have been identified within several lineages, but not all have followed Cope's rule, which states that average body size within a taxon tends to increase over time. In organisms such as parasites, space constraints may have shaped the evolution of body sizes, favouring small-bodied taxa capable of exploiting new niches. Here, the average adult body sizes of families in three groups of parasitic flatworms, the Digenea and two clades of Monogenea (Monopisthocotylea and Polyopisthocotylea), are related to their clade rank. Clade rank reflects the number of branching events, and thus the total path length, between an extant family and the root of the phylogenetic tree. Among families of Digenea, all of which are endoparasites of vertebrates, there was no trend in body size evolution. In contrast, the Monopisthocotylea and Polyopisthocotylea, which are (with the exception of Polystomatidae and Sphyranuridae) ectoparasites of fish, revealed significant negative relationships between family body size and clade rank, suggesting an evolutionary trend of decreasing size. In addition, an analysis of body size distributions in monogenean families also provides support, albeit weak, for this trend. From an ancestor parasitic on the skin of fishes, monogeneans have diversified by colonizing other microhabitats on their hosts, including such space-limited sites as the gaps between secondary gill lamellae. Using a conservative likelihood ratio test, however, a random walk, or null model of evolution could not be discarded in favour of the directional trends mentioned above. Nevertheless, these results suggest that body size has taken different evolutionary paths in endo- and ectoparasitic flatworms.  © 2005 The Linnean Society of London, Biological Journal of the Linnean Society , 2005, 85 , 181–189.     

Eco‐evolutionary dynamics in restored communities and ecosystems

Recent ecological studies have revealed that rapid evolution within populations can have significant impacts on the ecological dynamics of communities and ecosystems. These eco‐evolutionary dynamics (EED) are likely to have substantial and quantifiable effects in restored habitats over timescales that are relevant for the conservation and restoration of small populations and threatened communities. Restored habitats may serve as “hotspots” for EED due to mismatches between transplanted genotypes and the restored environment, and novel interactions among lineages that do not share a coevolutionary history, both of which can generate strong selection for rapid evolutionary change that has immediate demographic consequences. Rapid evolution that influences population dynamics and community processes is likely to have particularly large effects during the establishment phase of restoration efforts. Finally, restoration activities and their associated long‐term monitoring programs provide outstanding opportunities for using eco‐evolutionary experimental approaches. Results from such studies will address questions about the effects of rapid evolutionary change on the ecological dynamics of populations and interacting species, while simultaneously providing critical, but currently overlooked, information for conservation practices.     

Effects of climate change on species turnover and body mass frequency distributions of South African bird communities

Climate change will lead to substantial shifts in species distributions. Most of the predictions of shifting distributions rely on modelling future distributions with ecological niche models. We used these models to investigate (i) the expected species turnover, loss and gain within bird communities of four South African biomes and (ii) the expected changes in the body mass frequency distributions of these communities. We used distributional data of the Southern African Bird Atlas Project, current climate data and two scenarios of future climate change for 2050 to build ensemble models of bird distributions. Our results indicate that future species loss, gain and turnover within the four biomes will be considerable. Climate change will also have statistically significant effects on body mass frequency distributions, and these effects differ substantially depending on the severity of future climate change. We discuss the possible ecological effects of these predicted changes on ecosystem interactions and functions.     

Temperature-mediated changes in zooplankton body size: large scale temporal and spatial analysis

Climate warming has been linked with changes in the spatiotemporal distribution of species and the body size structure of ecological communities. Body size is a master trait underlying a host of physiological, ecological and evolutionary processes. However, the relative importance of environmental drivers and life history strategies on community body size structure across large spatial and temporal scales is poorly understood. We used detailed data of 83 copepod species, monitored over a 57-year period across the North Atlantic, to test how sea surface temperature, thermal and day length seasonality relate to observed latitudinal-size clines of the zooplankton community. The genus Calanus includes dominant taxa in the North Atlantic that overwinter at ocean depth. Thus we compared the copepod community size structure with and without Calanus species, to partition the influence of this life history strategy. The mean community body size of copepods was positively associated with latitude and negatively associated with temperature, suggesting that these communities follow Bergmann's rule. Including Calanus species strengthens these relationships due to their larger than average body sizes and high seasonal abundances, indicating that the latitudinal-size cline may be adaptive. We suggest that seasonal food availability prevents high abundance of smaller-sized copepods at higher latitudes, and that active vertical migration of dominant pelagic species can increase their survival rate over the resource-poor seasons. These findings improve our understanding of the impacts that climate warming has on ecological communities, with potential consequences for trophic interactions and biogeochemical processes that are well known to be size dependent.     

Fine-scale phenotypic change across a species transition zone in the genus neotoma: disentangling independent evolution from phylogenetic history

Zones of secondary contact between closely related species provide a rare opportunity to examine evidence of evolutionary processes that reinforce species boundaries and/or promote diversification. Here, we report on genetic and morphological variation in two sister species of woodrats, Neotoma fuscipes and N. macrotis, across a 30-km transition zone in the Sierra Nevada of California. We assessed whether these lineages readily hybridize, and whether their morphology suggests ecological interactions favoring phenotypic diversification. We combined measurements of body size and 11 craniodental traits from nine populations with genetic data to examine patterns of variation within and between species. We used phylogenetic autocorrelation methods to estimate the degree to which phenotypic variation in our dataset arose from independent evolution within populations versus phylogenetic history. Although no current sympatry or hybridization was evident, craniodental morphology diverged in both lineages near their distributional limits, whereas body size converged. The shift in craniodental morphology arose independently within populations whereas body size retained a strong phylogenetic signal, yet both patterns are consistent with expectations of phenotypic change based on different models of resource competition. Our findings demonstrate the importance of examining a suite of morphological traits across contact zones to provide a more complete picture of potential ecological interactions: competition may drive both diversification and convergence in different phenotypic traits.     

Asynchronous demographic responses to Pleistocene climate change in Eastern Nearctic vertebrates

Pleistocene climatic cycles altered species distributions in the Eastern Nearctic of North America, yet the degree of congruent demographic response to the Pleistocene among codistributed taxa remains unknown. We use a hierarchical approximate Bayesian computational approach to test if population sizes across lineages of snakes, lizards, turtles, mammals, birds, salamanders and frogs in this region expanded synchronously to Late Pleistocene climate changes. Expansion occurred in 75% of 74 lineages, and of these, population size trajectories across the community were partially synchronous, with coexpansion found in at least 50% of lineages in each taxonomic group. For those taxa expanding outside of these synchronous pulses, factors related to when they entered the community, ecological thresholds or biotic interactions likely condition their timing of response to Pleistocene climate change. Unified timing of population size change across communities in response to Pleistocene climate cycles is likely rare in North America.     

Body size distributions of large Costa Rican dry forest moths and the underlying relationship between plant and pollinator morphology

There has been much recent interest in explaining patterns of body size variation within species assemblages. One observation is that frequency distributions of species' body size commonly exhibit a right-skew, even on a logarithmic scale. Here we examine the species' body size distributions in two assemblages of large Costa Rican moths. We find that neither adult Sphingidae or Saturniidae exhibit the classic log right-skewed pattern. Furthermore, the species' body size distributions in these two groups are markedly different, which we suggest is a result of differential selective pressures related to resource and mate acquisition. For Sphingidae, we show (1) that body size is positively correlated with tongue length, and (2) that the distribution of sphingid body sizes/tongue lengths closely matches the distribution of flower corolla tube depths in sphingid-pollinated plants. Thus, morphological fitting between plants and pollinators seems to underlie the species' body size distribution of this sphingid assemblage. We discuss the significance of these results in the context of current theory on mechanisms driving species' body size distributions. Finally, we present an evolutionary hypothesis for the diversity of body sizes seen in this sphingid assemblage related to reciprocal interactions between plants and pollinators. This hypothesis can be tested within a rigorous phylogenetic framework, although a systematic phylogenetic analysis of Neotropical Sphingidae does not currently exist.