Heterogeneous relationships between rates of speciation and body size evolution across vertebrate clades

Several theories predict that rates of phenotypic evolution should be related to the rate at which new lineages arise. However, drawing general conclusions regarding the coupling between these fundamental evolutionary rates has been difficult due to the inconsistent nature of previous results combined with uncertainty over the most appropriate methodology with which to investigate such relationships. Here we propose and compare the performance of several different approaches for testing associations between lineage-specific rates of speciation and phenotypic evolution using phylogenetic data. We then use the best-performing method to test relationships between rates of speciation and body size evolution in five major vertebrate clades (amphibians, birds, mammals, ray-finned fish and squamate reptiles) at two phylogenetic scales. Our results provide support for the long-standing view that rates of speciation and morphological evolution are generally positively related at broad macroevolutionary scales, but they also reveal a substantial degree of heterogeneity in the strength and direction of these associations at finer scales across the vertebrate tree of life

Sociality, ecology and developmental constraints predict variation in brain size across birds

Conflicting theories have been proposed to explain variation in relative brain size across the animal kingdom. Ecological theories argue that the cognitive demands of seasonal or unpredictable environments have selected for increases in relative brain size, whereas the ‘social brain hypothesis’ argues that social complexity is the primary driver of brain size evolution. Here, we use a comparative approach to test the relative importance of ecology (diet, foraging niche and migration), sociality (social bond, cooperative breeding and territoriality) and developmental mode in shaping brain size across 1886 bird species. Across all birds, we find a highly significant effect of developmental mode and foraging niche on brain size, suggesting that developmental constraints and selection for complex motor skills whilst foraging generally imposes important selection on brain size in birds. We also find effects of social bonding and territoriality on brain size, but the direction of these effects do not support the social brain hypothesis. At the same time, we find extensive heterogeneity among major avian clades in the relative importance of different variables, implying that the significance of particular ecological and social factors for driving brain size evolution is often clade- and context-specific. Overall, our results reveal the important and complex ways in which ecological and social selection pressures and developmental constraints shape brain size evolution across birds

Phenotypic sexual dimorphism is associated with genomic signatures of resolved sexual conflict

Intra‐locus sexual conflict, where an allele benefits one sex at the expense of the other, has an important role in shaping genetic diversity of populations through balancing selection. However, the potential for mating systems to exert balancing selection through sexual conflict on the genome remains unclear. Furthermore, the nature and potential for resolution of sexual conflict across the genome has been hotly debated. To address this, we analysed de novo transcriptomes from six avian species, chosen to reflect the full range of sexual dimorphism and mating systems. Our analyses combine expression and population genomic statistics across reproductive and somatic tissue, with measures of sperm competition and promiscuity. Our results reveal that balancing selection is weakest in the gonad, consistent with the resolution of sexual conflict and evolutionary theory that phenotypic sex differences are associated with lower levels of ongoing conflict. We also demonstrate a clear link between variation in sexual conflict and levels of genetic variation across phylogenetic space in a comparative framework. Our observations suggest that this conflict is short‐lived, and is resolved via the decoupling of male and female gene expression patterns, with important implications for the role of sexual selection in adaptive potential and role of dimorphism in facilitating sex‐specific fitness optima

Adaptive radiation and the evolution of nectarivory in a large songbird clade

The accumulation of exceptional ecological diversity within a lineage is a key feature of adaptive radiation resulting from diversification associated with the subdivision of previously underutilized resources. The invasion of unoccupied niche space is predicted to be a key determinant of adaptive diversification, and this process may be particularly important if the diversity of competing lineages within the area, in which the radiation unfolds, is already high. Here, we test whether the evolution of nectarivory resulted in significantly higher rates of morphological evolution, more extensive morphological disparity, and a heightened build‐up of sympatric species diversity in a large adaptive radiation of passerine birds (the honeyeaters, about 190 species) that have diversified extensively throughout continental and insular settings. We find that a large increase in rates of body size evolution and general expansion in morphological space followed an ancestral shift to nectarivory, enabling the build‐up of large numbers of co‐occurring species that vary greatly in size, compared to related and co‐distributed nonnectarivorous clades. These results strongly support the idea that evolutionary shifts into novel areas of niche space play a key role in promoting adaptive radiation in the presence of likely competing lineages

Constraint and divergence in the evolution of male and female recombination rates in fishes

Recombination is a fundamental feature of sexual reproduction across eukaryotes, yet recombination rates are highly variable both within and between species. In particular, sex differences in recombination rate between males and females (heterochiasmy) is more often the rule than the exception, but despite its prevalence the ultimate causes of global patterns of heterochiasmy remain unclear. Here, we assemble a comprehensive dataset of sex-specific recombination rate estimates for 61 fish species, and combine this with information on sex determination, fertilisation mode and sexual dimorphism to test competing theories for the causes and evolution of heterochiasmy. We find that sex differences in recombination rate are evolutionary labile, with frequent shifts in the direction and magnitude of heterochiasmy. This rapid turnover does not appear to be driven by simple neutral processes and is inconsistent with non-adaptive explanations for heterochiasmy, including biological sex differences in meiosis. However, while patterns of heterochiasmy across the phylogeny indicate a potential role for adaptive processes, we are unable to directly link variation in heterochiasmy with proxies for sexual selection or sexual conflict across species, indicating that these effects – if present – are either subtle or complex. Finally, we show evidence for correlated rates of recombination rate evolution between males and females, indicating the potential for genetic constraints and sexual conflict over the recombination landscape

Allometric conservatism in the evolution of bird beaks

Evolution can involve periods of rapid divergent adaptation and expansion in the range of diversity, but evolution can also be relatively conservative over certain timescales due to functional, genetic-developmental, and ecological constraints. One way in which evolution may be conservative is in terms of allometry, the scaling relationship between the traits of organisms and body size. Here, we investigate patterns of allometric conservatism in the evolution of bird beaks with beak size and body size data for a representative sample of over 5000 extant bird species within a phylogenetic framework. We identify clades in which the allometric relationship between beak size and body size has remained relatively conserved across species over millions to tens of millions of years. We find that allometric conservatism is nonetheless punctuated by occasional shifts in the slopes and intercepts of allometric relationships. A steady accumulation of such shifts through time has given rise to the tremendous diversity of beak size relative to body size across birds today. Our findings are consistent with the Simpsonian vision of macroevolution, with evolutionary conservatism being the rule but with occasional shifts to new adaptive zones

Innovation and elaboration on the avian tree of life

Widely documented, megaevolutionary jumps in phenotypic diversity continue to perplex researchers because it remains unclear whether these marked changes can emerge from microevolutionary processes. Here, we tackle this question using new approaches for modeling multivariate traits to evaluate the magnitude and distribution of elaboration and innovation in the evolution of bird beaks. We find that elaboration, evolution along the major axis of phenotypic change, is common at both macro- and megaevolutionary scales, whereas innovation, evolution away from the major axis of phenotypic change, is more prominent at megaevolutionary scales. The major axis of phenotypic change among species beak shapes at megaevolutionary scales is an emergent property of innovation across clades. Our analyses suggest that the reorientation of phenotypes via innovation is a ubiquitous route for divergence that can arise through gradual change alone, opening up further avenues for evolution to explore

The signature of competition in ecomorphological traits across the avian radiation

Competition for shared resources represents a fundamental driver of biological diversity. However, the tempo and mode of phenotypic evolution in deep-time has been predominantly investigated using trait evolutionary models which assume that lineages evolve independently from each other. Consequently, the role of species interactions in driving macroevolutionary dynamics remains poorly understood. Here, we quantify the prevalence for signatures of competition between related species in the evolution of ecomorphological traits across the bird radiation. We find that mechanistic trait models accounting for the effect of species interactions on phenotypic divergence provide the best fit for the data on at least one trait axis in 27 out of 59 clades ranging between 21 and 195 species. Where it occurs, the signature of competition generally coincides with positive species diversity-dependence, driven by the accumulation of lineages with similar ecologies, and we find scarce evidence for trait-dependent or negative diversity-dependent phenotypic evolution. Overall, our results suggest that the footprint of interspecific competition is often eroded in long-term patterns of phenotypic diversification, and that other selection pressures may predominantly shape ecomorphological diversity among extant species at macroevolutionary scales

The signature of competition in ecomorphological traits across the avian radiation

Competition for shared resources represents a fundamental driver of biological diversity. However, the tempo and mode of phenotypic evolution in deep-time has been predominantly investigated using trait evolutionary models which assume that lineages evolve independently from each other. Consequently, the role of species interactions in driving macroevolutionary dynamics remains poorly understood. Here, we quantify the prevalence for signatures of competition between related species in the evolution of ecomorphological traits across the bird radiation. We find that mechanistic trait models accounting for the effect of species interactions on phenotypic divergence provide the best fit for the data on at least one trait axis in 27 out of 59 clades ranging between 21 and 195 species. Where it occurs, the signature of competition generally coincides with positive species diversity-dependence, driven by the accumulation of lineages with similar ecologies, and we find scarce evidence for trait-dependent or negative diversity-dependent phenotypic evolution. Overall, our results suggest that the footprint of interspecific competition is often eroded in long-term patterns of phenotypic diversification, and that other selection pressures may predominantly shape ecomorphological diversity among extant species at macroevolutionary scales

Using pose estimation to identify regions and points on natural history specimens

A key challenge in mobilising growing numbers of digitised biological specimens for scientific research is finding high-throughput methods to extract phenotypic measurements on these datasets. In this paper, we test a pose estimation approach based on Deep Learning capable of accurately placing point labels to identify key locations on specimen images. We then apply the approach to two distinct challenges that each requires identification of key features in a 2D image: (i) identifying body region-specific plumage colouration on avian specimens and (ii) measuring morphometric shape variation in Littorina snail shells. For the avian dataset, 95% of images are correctly labelled and colour measurements derived from these predicted points are highly correlated with human-based measurements. For the Littorina dataset, more than 95% of landmarks were accurately placed relative to expert-labelled landmarks and predicted landmarks reliably captured shape variation between two distinct shell ecotypes (‘crab’ vs ‘wave’). Overall, our study shows that pose estimation based on Deep Learning can generate high-quality and high-throughput point-based measurements for digitised image-based biodiversity datasets and could mark a step change in the mobilisation of such data. We also provide general guidelines for using pose estimation methods on large-scale biological datasets