Trophic niche shifts and phenotypic trait evolution are largely decoupled in Australasian parrots

Background Trophic shifts from one dietary niche to another have played major roles in reshaping the evolutionary trajectories of a wide range of vertebrate groups, yet their consequences for morphological disparity and species diversity differ among groups. Methods Here, we use phylogenetic comparative methods to examine whether the evolution of nectarivory and other trophic shifts have driven predictable evolutionary pathways in Australasian psittaculid parrots in terms of ecological traits such as body size, beak shape, and dispersal capacity. Results We found no evidence for an ‘early-burst’ scenario of lineage or morphological diversification. The best-fitting models indicate that trait evolution in this group is characterized by abrupt phenotypic shifts (evolutionary jumps), with no sign of multiple phenotypic optima correlating with different trophic strategies. Thus, our results point to the existence of weak directional selection and suggest that lineages may be evolving randomly or slowly toward adaptive peaks they have not yet reached. Conclusions This study adds to a growing body of evidence indicating that the relationship between avian morphology and feeding ecology may be more complex than usually assumed and highlights the importance of adding more flexible models to the macroevolutionary toolbox.

The relative impact of evolving pleiotropy and mutational correlation on trait divergence

Both pleiotropic connectivity and mutational correlations can restrict the decoupling of traits under divergent selection, but it is unknown which is more important in trait evolution. To address this question, we create a model that permits within-population variation in both pleiotropic connectivity and mutational correlation, and compare their relative importance to trait evolution. Specifically, we developed an individual-based stochastic model where mutations can affect whether a locus affects a trait and the extent of mutational correlations in a population. We find that traits can decouple whether there is evolution in pleiotropic connectivity or mutational correlation, but when both can evolve, then evolution in pleiotropic connectivity is more likely to allow for decoupling to occur. The most common genotype found in this case is characterized by having one locus that maintains connectivity to all traits and another that loses connectivity to the traits under stabilizing selection (subfunctionalization). This genotype is favored because it allows the subfunctionalized locus to accumulate greater effect size alleles, contributing to increasingly divergent trait values in the traits under divergent selection without changing the trait values of the other traits (genetic modularization). These results provide evidence that partial subfunctionalization of pleiotropic loci may be a common mechanism of trait decoupling under regimes of corridor selection.

The effects of introgression across thousands of quantitative traits revealed by gene expression in wild tomatoes

It is now understood that introgression can serve as powerful evolutionary force, providing genetic variation that can shape the course of trait evolution. Introgression also induces a shared evolutionary history that is not captured by the species phylogeny, potentially complicating evolutionary analyses that use a species tree. Such analyses are often carried out on gene expression data across species, where the measurement of thousands of trait values allows for powerful inferences while controlling for shared phylogeny. Here, we present a Brownian motion model for quantitative trait evolution under the multispecies network coalescent framework, demonstrating that introgression can generate apparently convergent patterns of evolution when averaged across thousands of quantitative traits. We test our theoretical predictions using whole-transcriptome expression data from ovules in the wild tomato genus Solanum. Examining two sub-clades that both have evidence for post-speciation introgression, but that differ substantially in its magnitude, we find patterns of evolution that are consistent with histories of introgression in both the sign and magnitude of ovule gene expression. Additionally, in the sub-clade with a higher rate of introgression, we observe a correlation between local gene tree topology and expression similarity, implicating a role for introgressed cis-regulatory variation in generating these broad-scale patterns. Our results reveal a general role for introgression in shaping patterns of variation across many thousands of quantitative traits, and provide a framework for testing for these effects using simple model-informed predictions.

Olfactory System Morphology Suggests Colony Size Drives Trait Evolution in Odorous Ants (Formicidae: Dolichoderinae)

In social insects colony fitness is determined in part by individual worker phenotypes. Across ant species, colony size varies greatly and is thought to affect worker trait variation in both proximate and ultimate ways. Little is known about the relationship between colony size and worker trait evolution, but hypotheses addressing the role of social structure in brain evolution suggest workers of small-colony species may have larger brains or larger brain regions necessary for complex behaviors. In previous work on odorous ants (Formicidae: Dolichoderinae) we found no correlation between colony size and these brain properties, but found that relative antennal lobe size scaled negatively with colony size. Therefore, we now test whether sensory systems scale with colony size, with particular attention to olfactory components thought to be involved in nestmate recognition. Across three species of odorous ants, Forelius mccooki, Dorymyrmex insanus, and D. bicolor, which overlap in habitat and foraging ecology but vary in colony size, we compare olfactory sensory structures, comparing those thought to be involved in nestmate recognition. We use the visual system, a sensory modality not as important in social communication in ants, as a control comparison. We find that body size scaling largely explains differences in eye size, antennal length, antennal sensilla density, and total number of olfactory glomeruli across these species. However, sensilla basiconica and olfactory glomeruli in the T6 cluster of the antennal lobe, structures known to be involved in nestmate recognition, do not follow body size scaling observed for other structures. Instead, we find evidence from the closely related Dorymyrmex species that the larger colony species, D. bicolor, invests more in structures implicated in nestmate recognition. To test for functional consequences, we compare nestmate and non-nestmate interactions between these two species and find D. bicolor pairs of either type engage in more interactions than D. insaus pairs. Thus, we do not find evidence supporting a universal pattern of sensory system scaling associated with changes in colony size, but hypothesize that observed differences in the olfactory components in two closely related Dorymyrmex species are evidence of a link between colony size and sensory trait evolution.

The role of evolutionary modes for trait-based cascades in mutualistic networks

The erosion of functional diversity may foster the collapse of ecological systems. Functional diversity is ultimately defined by the distribution of species traits and, as species traits are a legacy of species evolutionary history, one might expect that the mode of trait evolution influence community resistance under the loss of functional diversity. In this paper, we investigate the role of trait evolutionary dynamics on the robustness of mutualistic networks undergoing the following scenarios of species loss: i) random extinctions, ii) loss of functional distinctiveness and iii) biased towards larger trait values. We simulated networks defined by models of single trait complementary and evolutionary modes where traits can arise in recent diversification events with weak phylogenetic signal, in early diversification events with strong phylogenetic signal, or as a random walk through evolutionary time. Our simulations show that mutualistic networks are especially vulnerable to extinctions based on trait distinctiveness and more robust to random extinction dynamics. The networks show intermediate level of robustness against size-based extinctions. Despite the small range of variation in network robustness, our results show that the mode of trait evolution matters for network robustness in all three scenarios. Networks with low phylogenetic signal are more robust than networks with high phylogenetic signal across all scenarios. As a consequence, our results predict that mutualistic networks based upon current adaptations are more likely to cope with extinction dynamics than those networks that are based upon conserved traits.

Tempo and mode of morphological evolution are decoupled from latitude in birds

The latitudinal diversity gradient is one of the most striking patterns in nature, yet its implications for morphological evolution are poorly understood. In particular, it has been proposed that an increased intensity of species interactions in tropical biota may either promote or constrain trait evolution, but which of these outcomes predominates remains uncertain. Here, we develop tools for fitting phylogenetic models of phenotypic evolution in which the impact of species interactions—namely, competition—can vary across lineages. Deploying these models on a global avian trait dataset to explore differences in trait divergence between tropical and temperate lineages, we find that the effect of latitude on the mode and tempo of morphological evolution is weak and clade- or trait dependent. Our results indicate that species interactions do not disproportionately impact morphological evolution in tropical bird families and question the validity of previously reported patterns of slower trait evolution in the tropics.