Brain structure evolution in a basal vertebrate clade: evidence from phylogenetic comparative analysis of cichlid fishes

<p>Abstract</p> <p>Background</p> <p>The vertebrate brain is composed of several interconnected, functionally distinct structures and much debate has surrounded the basic question of how these structures evolve. On the one hand, according to the 'mosaic evolution hypothesis', because of the elevated metabolic cost of brain tissue, selection is expected to target specific structures mediating the cognitive abilities which are being favored. On the other hand, the 'concerted evolution hypothesis' argues that developmental constraints limit such mosaic evolution and instead the size of the entire brain varies in response to selection on any of its constituent parts. To date, analyses of these hypotheses of brain evolution have been limited to mammals and birds; excluding Actinopterygii, the basal and most diverse class of vertebrates. Using a combination of recently developed phylogenetic multivariate allometry analyses and comparative methods that can identify distinct rates of evolution, even in highly correlated traits, we studied brain structure evolution in a highly variable clade of ray-finned fishes; the Tanganyikan cichlids.</p> <p>Results</p> <p>Total brain size explained 86% of the variance in brain structure volume in cichlids, a lower proportion than what has previously been reported for mammals. Brain structures showed variation in pair-wise allometry suggesting some degree of independence in evolutionary changes in size. This result is supported by variation among structures on the strength of their loadings on the principal size axis of the allometric analysis. The rate of evolution analyses generally supported the results of the multivariate allometry analyses, showing variation among several structures in their evolutionary patterns. The olfactory bulbs and hypothalamus were found to evolve faster than other structures while the dorsal medulla presented the slowest evolutionary rate.</p> <p>Conclusion</p> <p>Our results favor a mosaic model of brain evolution, as certain structures are evolving in a modular fashion, with a small but non-negligible influence of concerted evolution in cichlid fishes. Interestingly, one of the structures presenting distinct evolutionary patterns within cichlids, the olfactory bulbs, has also been shown to evolve differently from other structures in mammals. Hence, our results for a basal vertebrate clade also point towards a conserved developmental plan for all vertebrates.</p

Sex ratios deviate across killifish species without clear links to life history

Sex ratios can differ from an expected equal proportion of males and females, carrying substantial implications for our understanding of how mating systems evolve. Typically, macro-evolutionary studies have been conducted without assessing how deviations from an equal sex ratio could be explained by sex-biased mortality or dispersal. Our understanding of sex ratio evolution independent of these confounds, in addition to any putative links between skewed sex ratios and other factors (e.g. life history), therefore remains largely unexplored. Here, we conducted an exploratory study investigating differences in sex ratios across closely related species while controlling for extrinsic mortality. We also tested two factors, non-overlapping/overlapping generations and the social environment, which have both been hypothesised to affect sex ratios. Specifically, we raised 15 species of killifish, which have either overlapping or discrete generations, under both solitary and social treatments. We found substantial divergences in sex ratios across closely related species, which exhibited both male and female biases. In conjunction with a low phylogenetic signal, our results suggest that sex ratios can evolve rapidly in this group. However, we found no evidence that overlapping generations or the social environment affected sex biases, suggesting that other factors drive the rapid evolution of sex ratios in killifishes

Carotenoid-dependent plumage coloration is associated with reduced male care in passerine birds

The immense diversity of plumage coloration exhibited by birds is the result of either pigments deposited in the feathers or microstructural arrangements of feather barbules. Some of the most common pigments are carotenoids, which produce bright yellow, orange, and red colors. Carotenoids differ from other pigments since birds cannot synthesize them de novo and must obtain them from the diet. Carotenoid pigments are usually associated with signaling and sexual selection, although they also have antioxidant properties and play a role in the immune response. Here, we hypothesize that carotenoid-dependent plumage coloration functions as a signal of a male’s tendency to invest in offspring care because they play an important role in self-maintenance and may provide key information about individual quality; allowing females to obtain information about a male’s tendency to invest in offspring care. Using phylogenetic comparative analyses across 349 passerine birds, we show that species that consume carotenoid-rich foods have more carotenoid-dependent plumage coloration than species with carotenoid-poor diets. In addition, carotenoid-dependent plumage coloration is associated with decreased male investment in offspring care. Our results suggest that investment in carotenoid-dependent plumage coloration trades off against male investment in offspring care and will likely have broad implications for our understanding of the ecological contexts that facilitate various evolutionary processes, such as sexual selection and signaling associated with plumage colors

Carotenoid-dependent plumage coloration is associated with reduced male care in passerine birds

The immense diversity of plumage coloration exhibited by birds is the result of either pigments deposited in the feathers or microstructural arrangements of feather barbules. Some of the most common pigments are carotenoids, which produce bright yellow, orange, and red colors. Carotenoids differ from other pigments since birds cannot synthesize them de novo and must obtain them from the diet. Carotenoid pigments are usually associated with signaling and sexual selection, although they also have antioxidant properties and play a role in the immune response. Here, we hypothesize that carotenoid-dependent plumage coloration functions as a signal of a male’s tendency to invest in offspring care because they play an important role in self-maintenance and may provide key information about individual quality; allowing females to obtain information about a male’s tendency to invest in offspring care. Using phylogenetic comparative analyses across 349 passerine birds, we show that species that consume carotenoid-rich foods have more carotenoid-dependent plumage coloration than species with carotenoid-poor diets. In addition, carotenoid-dependent plumage coloration is associated with decreased male investment in offspring care. Our results suggest that investment in carotenoid-dependent plumage coloration trades off against male investment in offspring care and will likely have broad implications for our understanding of the ecological contexts that facilitate various evolutionary processes, such as sexual selection and signaling associated with plumage colors

A comment on 'The adaptive value of gluttony: predators mediate the life history trade?offs of satiation threshold' by Pruitt & Krauel (2010)

Inspection of the data that accompany Pruitt and Krauel's study of individual variation in satiation threshold and a comparison of these data with the Materials and Methods and Results sections of the paper have revealed a number of issues that cast doubts on the reliability of the data and any results based on these data. In particular, we show that, following our analyses, the data are unlikely to have been obtained using the study design outlined in the publication and that statistical analyses of these data provide results that differ in important ways from those reported. These findings illustrate the importance of making raw data and analysis code available for the rigour and reproducibility of the scientific literature

Deconstructing heterostyly: The evolutionary role of incompatibility system, pollinators, and floral architecture. Evolution 67

Darwin&apos;s early work on heterostyly and related style polymorphisms (the presence of two or three style morphs within a population) generated much interest to understand how precise interactions between ecological and genetic mechanisms influence the evolution of floral diversity. Here we tested three key hypotheses proposed to explain the evolution of heterostyly: (i) the presence of self-incompatibility; (ii) the role of pollinators in promoting dissasortative mating; and (iii) floral architecture, which restricts pollinators&apos; movements and ensures more exact pollen deposition on their bodies. We combined data from experiments, field observations, and published studies to test whether evolution of style polymorphism in Narcissus is driven by the incompatibility system, pollinator guilds, or floral architecture, within a phylogenetic framework. Neither differences in pollinator environment nor the presence of genetic self-incompatibility were correlated with presence of style polymorphism. However, our results indicate that the evolution of style polymorphism was driven by the presence of a narrow and long floral tube. K E Y W O R D S : Evolutionary transitions, floral architecture, heterostyly, incompatibility system, pollinators. Heterostyly and related style polymorphisms have fascinated biologists since Darwin provided an evolutionary explanation of the mechanisms suggesting that they serve to promote outcrossing in hermaphroditic plants (Darwin 1877). Heterostyly is characterized by the presence of two (distyly) or three (tristyly) flower morphs with reciprocal displacement in the height of the stigmas and the anthers within a flower. Style dimorphism is a polymorphism related with heterostyly, where two stylar morphs exist without concomitant reciprocal variation in stamens. Evolutionary models suggest that stylar dimorphism is an intermediate step in the transition from style monomorphism to distyl

The phylogenetic limits to diversity-dependent diversification

While the theory of micro-evolution by natural selection assigns a crucial role to competition, its role in macroevolution is less clear. Phylogenetic evidence for a decelerating accumulation of lineages suggests a feedback of lineage diversity on diversification. However, does this feedback only occur between close relatives, or do distant relatives also influence their diversification? In other words: are there phylogenetic limits to this diversity-dependence? Islands form ideal systems to answer these questions, because their boundedness facilitates an overview of all potential competitors. The DAISIE (Dynamic Assembly of Island biota through Speciation Immigration and Extinction) framework allows for testing the presence of diversity-dependence on islands given phylogenetic data on colonization and branching times. The current inference models in DAISIE assume that this diversity-dependence only applies within a colonizing clade, i.e. all mainland species can colonize and diversify independently from one another. We term this clade-specific (CS) diversity-dependence. Here we introduce a new DAISIE model that assumes that diversity-dependence applies to all island species of a taxonomic group regardless of their mainland ancestry, i.e. diversity-dependence applies both to species within the same clade and between different clades established by different mainland species. We call this island-wide (IW) diversity-dependence. We present a method to compute a likelihood for this model given phylogenetic data on colonization and branching events and use likelihood ratio bootstrapping to compare it to the likelihood of the CS model in order to overcome biases known for standard model selection. We apply it to the diversification of Eleutherodactylus frogs on Hispaniola. Across the Greater Antilles archipelago, this radiation shows repeated patterns of diversification in ecotypes which are similar across clades. This could be suggestive of overlapping niche space and hence between-clade interactions, i.e. IW diversity-dependence. But it could also be suggestive of only within-clade interactions, because between-clade interactions would have blocked the same ecotype re-appearing. We find that the CS model fits the data much better than the IW model, indicating that different colonizations, while resulting in similar ecotypes, are sufficiently distinct to avoid interacting strongly. We argue that non-overlapping distributions between clades (both spatially and in terms of ecotypes) cannot be used as evidence of CS diversity-dependence, because this pattern may be a consequence of IW diversity-dependence. By contrast, by using phylogenetic data rather than distributional data our method does allow for inferring the phylogenetic limits to diversity-dependent diversification. We discuss possibilities for future extensions and applications of our modelling approach.</p

The limits to ecological limits to diversification

While the theory of micro-evolution by natural selection assigns a crucial role to competition, its role in macroevolution is less clear. Phylogenetic evidence for a decelerating accumulation of lineages suggests a feedback of lineage diversity on diversification, i.e., ecological limits to diversification. However, does this feedback only occur between close relatives, or do distant relatives also influence their diversification? In other words: are there phylogenetic limits to these ecological limits? Islands form ideal systems to answer these questions, because their boundedness facilitates an overview of all potential competitors. The DAISIE (Dynamic Assembly of Island biota through Speciation Immigration and Extinction) framework allows for testing the presence of diversity-dependence on islands given phylogenetic data on colonization and branching times. The current inference models in DAISIE assume that this diversity-dependence only applies within a colonizing clade, which we term clade-specific (CS) diversity-dependence. Here we introduce a new DAISIE model that assumes that diversity-dependence applies to all species regardless of their ancestry, i.e. diversity-dependence applies both to species within the same clade and between different clades. We call this island-wide (IW) diversity-dependence. Here we present a method to compute a likelihood for this model and develop a statistical procedure based on likelihood ratio bootstrapping to compare it to the likelihood of the CS model in order to overcome biases known for standard model selection. We apply it to the diversification of Eleutherodactylus frogs on Hispaniola. Across the Greater Antilles archipelago, this radiation shows repeated patterns of diversification in ecotypes which are similar across clades. This could be suggestive of overlapping niche space and hence between-clade interactions, i.e. IW diversity-dependence. But it could also be suggestive of only within-clade interactions, because between-clade interactions would have blocked the same ecotype re-appearing. We find that the CS model fits the data much better than the IW model, indicating that different colonizations, while resulting in similar ecotypes, are sufficiently distinct to avoid interacting strongly. We argue that non-overlapping distributions between clades (both spatially and in terms of ecotypes) cannot be used as evidence of CS diversity-dependence, because this pattern may be a consequence of IW diversity-dependence. By contrast, by using phylogenetic data rather than distributional data our method does allow for inferring the phylogenetic limits to ecological limits to diversification. We discuss how our new IW model advances our understanding also in other ways, ranging from identifying priority effects to modelling the spread of an epidemic in island-like systems, such as schools or hospitals

Fast life-histories are associated with larger brain size in killifishes

The high energetic demands associated with the vertebrate brain are proposed to result in a trade-off between the pace of life-history and relative brain size. However, because both life-history and brain size also have a strong relationship with body size, any associations between the pace of life-history and relative brain size may be confounded by coevolution with body size. Studies on systems where contrasts in the pace of life-history occur without concordant contrasts in body size could therefore add to our understanding of the potential coevolution between relative brain size and life-history. Using one such system - 21 species of killifish - we employed a common garden design across two ontogenetic stages to investigate the association between relative brain size and the pace of life-history. Contrary to predictions, we found that relative brain size was larger in adult fast-living killifishes, compared to slow-living species. Although we found no differences in relative brain size between juvenile killifishes. Our results suggest that fast- and slow-living killifishes do not exhibit the predicted trade-off between brain size and life-history. Instead, fast and slow-living killifishes could differ in the ontogenetic timing of somatic versus neural growth or inhabit environments that differ considerably in cognitive demands