Geogenomic predictors of genetree heterogeneity explain phylogeographic and introgression history: a case study in an Amazonian bird (Thamnophilus aethiops).

Can knowledge about genome architecture inform biogeographic and phylogenetic inference? Selection, drift, recombination, and gene flow interact to produce a genomic landscape of divergence wherein patterns of differentiation and genealogy vary nonrandomly across the genomes of diverging populations. For instance, genealogical patterns that arise due to gene flow should be more likely to occur on smaller chromosomes, which experience high recombination, whereas those tracking histories of geographic isolation (reduced gene flow caused by a barrier) and divergence should be more likely to occur on larger and sex chromosomes. In Amazonia, populations of many bird species diverge and introgress across rivers, resulting in reticulated genomic signals. Herein, we used reduced representation genomic data to disentangle the evolutionary history of four populations of an Amazonian antbird, Thamnophilus aethiops, whose biogeographic history was associated with the dynamic evolution of the Madeira River Basin. Specifically, we evaluate whether a large river capture event ca. 200 Ka, gave rise to reticulated genealogies in the genome by making spatially explicit predictions about isolation and gene flow based on knowledge about genomic processes. We first estimated chromosome-level phylogenies and recovered two primary topologies across the genome. The first topology (T1) was most consistent with predictions about population divergence and was recovered for the Z chromosome. The second (T2), was consistent with predictions about gene flow upon secondary contact. To evaluate support for these topologies, we trained a convolutional neural network to classify our data into alternative diversification models and estimate demographic parameters. The best-fit model was concordant with T1 and included gene flow between non-sister taxa. Finally, we modeled levels of divergence and introgression as functions of chromosome length and found that smaller chromosomes experienced higher gene flow. Given that (1) gene-trees supporting T2 were more likely to occur on smaller chromosomes and (2) we found lower levels of introgression on larger chromosomes (and especially the Z-chromosome), we argue that T1 represents the history of population divergence across rivers and T2 the history of secondary contact due to barrier loss. Our results suggest that a significant portion of genomic heterogeneity arises due to extrinsic biogeographic processes such as river capture interacting with intrinsic processes associated with genome architecture. Future phylogeographic studies would benefit from accounting for genomic processes, as different parts of the genome reveal contrasting, albeit complementary histories, all of which are relevant for disentangling the intricate geogenomic mechanisms of biotic diversification.

Rethinking Gloger's Rule: Climate, Light Environments, and Color in a Large Family of Tropical Birds (Furnariidae).

AbstractEcogeographic rules provide a framework within which to test evolutionary hypotheses of adaptation. Gloger's rule predicts that endothermic animals should have darker colors in warm/rainy climates. This rule also predicts that animals should be more rufous in warm/dry climates, the so-called complex Gloger's rule. Empirical studies frequently demonstrate that animals are darker in cool/wet climates rather than in warm/wet climates. Furthermore, sensory ecology predicts that, to enhance crypsis, animals should be darker in darker light environments. We aimed to disentangle the effects of climate and light environments on plumage color in the large Neotropical passerine family Furnariidae. We found that birds in cooler and rainier climates had darker plumage even after controlling for habitat type. Birds in darker habitats had darker plumage even after controlling for climate. The effects of temperature and precipitation interact so that the negative effect of precipitation on brightness is strongest in cool temperatures. Finally, birds tended to be more rufous in warm/dry habitats but also, surprisingly, in cool/wet locales. We suggest that Gloger's rule results from complementary selective pressures arising from myriad ecological factors, including crypsis, thermoregulation, parasite deterrence, and resistance to feather abrasion.

Digest: When sexual selection hits the wall of natural selection.

Sexual selection often drives traits in a direction that is disfavored by natural selection. The balance between these two types of selection can shift rapidly in response to environmental changes. Gallagher et al. (2024) report such a shift in the cricket population following the introduction of a parasitoid fly. The ancestral male morph, though still preferred by females, has been supplanted by multiple novel morphs that are more difficult for the parasitoid to detect.

The evolution of sex similarities in social signals: Climatic seasonality is associated with lower sexual dimorphism and greater elaboration of female and male signals in antbirds (Thamnophilidae).

Selection on signals that mediate social competition varies with resource availability. Climate regulates resource availability, which may affect the strength of competition and selection on signals. Traditionally, this meant that more seasonal, colder, or dryer-overall harsher-environments should favor the elaboration of male signals under stronger male-male competition, increasing sexual dimorphism. However, females also use signals to compete; thus, harsher environments could strengthen competition and favor elaboration of signals in both sexes, decreasing sexual dimorphism. Alternatively, harsher environments could decrease sexual dimorphism due to scarcer resources to invest in signal elaboration in both sexes. We evaluated these contrasting hypotheses in antbirds, a family of Neotropical passerines that varies in female and male signals and occurs across diverse climatic regimes. We tested the association of sexual dimorphism of plumage coloration and songs with temperature, precipitation, and their seasonality. We found that greater seasonality is associated with lower sexual dimorphism in plumage coloration and greater elaboration of visual signals in both sexes, but not acoustic signals. Our results suggest that greater seasonality may be associated with convergent elaboration of female and male visual signals, highlighting the role of signals of both sexes in the evolution of sexual dimorphism.

Realistic scenarios of missing taxa in phylogenetic comparative methods and their effects on model selection and parameter estimation.

Model-based analyses of continuous trait evolution enable rich evolutionary insight. These analyses require a phylogenetic tree and a vector of trait values for the tree's terminal taxa, but rarely do a tree and dataset include all taxa within a clade. Because the probability that a taxon is included in a dataset depends on ecological traits that have phylogenetic signal, missing taxa in real datasets should be expected to be phylogenetically clumped or correlated to the modelled trait. I examined whether those types of missing taxa represent a problem for model selection and parameter estimation. I simulated univariate traits under a suite of Brownian Motion and Ornstein-Uhlenbeck models, and assessed the performance of model selection and parameter estimation under absent, random, clumped or correlated missing taxa. I found that those analyses perform well under almost all scenarios, including situations with very sparsely sampled phylogenies. The only notable biases I detected were in parameter estimation under a very high percentage (90%) of correlated missing taxa. My results offer a degree of reassurance for studies of continuous trait evolution with missing taxa, but the problem of missing taxa in phylogenetic comparative methods still demands much further investigation. The framework I have described here might provide a starting point for future work.

Fifty shades of brown: Macroevolution of plumage brightness in the Furnariida, a large clade of drab Neotropical passerines.

Both natural and sexual selection are thought to affect the evolution of bird color. Most studies of the topic have focused on sexually dichromatic taxa and showy plumages, which are expected to be more influenced by social selection and usually result in increased conspicuousness. However, many bird clades display dull brown or gray plumages that vary greatly in brightness (lightness), but little in hue (shade). Here, we examine the macroevolution of brightness in one such clade, the Furnariida. We make comparisons across light environments, body parts, monochromatic lineages, and each sex of dichromatic lineages. We found that support for models including light environments is greater for the dorsum than for the venter, and that brightness evolution is more constrained in the former than in the latter. Plumages in this clade have evolved to be darker in darker habitats, consistent with natural selection for increased crypsis. Finally, the features of brightness macroevolution are broadly similar across the sexes of the dichromatic clade, challenging the view that sexual dichromatism is driven by different evolutionary processes acting in each sex. We conclude that, in the Furnariida, light environments and dorsal-ventral variation are more important than sex as axes of color evolution.