The allopatric model of speciation has dominated our understanding of speciation biology and biogeography since the Modern Synthesis. It is uncontroversial because reproductive isolation may readily emerge as a by-product of evolutionary divergence during allopatry unopposed by gene flow. Recent genomic studies have found that gene flow between species is common, but whether allopatric speciation is common has rarely been systematically tested across a continuum of closely related species. Here, we fit a range of demographic models of evolutionary divergence to whole-genome sequence data from 93 pairs of Drosophila species to infer speciation histories and levels of post-divergence gene flow. We find that speciation with gene flow is common, even between currently allopatric pairs of species. Estimates of historical gene flow are not predicted by current range overlap. Whilst evidence for secondary contact is generally limited, a few sympatric pairs showed strong support for a secondary contact model. Our analyses suggest that most speciation processes involve some long-term gene flow, perhaps due to repeated cycles of allopatry and contact, without requiring an extensive allopatric phase.

The evolution of novel animal signals is critical to the generation of biodiversity. Here, we explore how new sexual signals become established. This process is challenging to explain because if receiver preferences are coupled with existing signals, then most receivers should discriminate against new signals. We investigated an underappreciated hypothesis: relaxed receiver preferences facilitate novel signal evolution by allowing new signals to establish a foothold. Further, we probed the mechanistic underpinnings of relaxed preferences by combining field-based and common garden approaches, allowing us to investigate evolution and plasticity as mechanisms. We capitalized on the Pacific field cricket, Teleogryllus oceanicus, a species that has recently evolved multiple novel acoustic signals (e.g., purring and rattling) in response to an eavesdropping parasitoid fly only found in the crickets' introduced range in Hawaii. To test the hypothesis that selection associated with high search costs in introduced populations leads to relaxed mating preferences and determine whether such relaxation is plastic, we conducted sound preference (phonotaxis) trials with females from the cricket's native range (Australia and French Polynesia, where the fly is absent) and its introduced range (Hawaii, where the fly is present). We presented females with novel songs plus the typical, ancestral song. Differences in phonotactic behavior between the lab and field settings would indicate plasticity in preferences. We found that Australian and French Polynesian females were quite plastic; they discriminated strongly against most songs in the field, but were much more phonotactic to rattling and the typical song in the lab. However, Hawaiian females exhibited little plasticity and were consistently highly responsive to the rattling and typical songs in the lab and field. This pattern points to a loss of ancestral plasticity in female preferences sometime after colonizing Hawaii, resulting in heightened responsiveness to all songs-allowing novel signals to establish.

Changes in gene expression levels are central to adaptation, yet predicting and understanding their evolution remains challenging. Here, we used transcriptome-wide variation in the red flour beetle Tribolium castaneum to identify genes under selection for expression changes during adaptation to heat and drought stress and to uncover the mechanisms driving these changes. We found that estimates of genetic selection on expression levels were predictive of their evolutionary changes after 20 generations across seven independent selection lines. Evolution was largely caused by indirect selection acting on genetically correlated genes rather than by direct selection on individual genes. Consequently, central genes in co-expression networks experienced stronger selection and larger expression changes. Our genomic analysis revealed that selection on expression levels is associated with parallel allele frequency changes in the respective genes, especially in pleiotropic genes and those carrying expression quantitative trait loci, with stronger genetic selection corresponding to greater parallelism. Contrary to previous evidence of constrained evolution at more connected genes, adaptation was driven by selection acting disproportionately on genes central to co-expression gene networks. Overall, our results demonstrated that selection measured at the transcriptome level not only predicts future gene expression evolution but also provides mechanistic insight into the genetic architecture of adaptation.

The evolution of eusociality, characterized by cooperative brood care, reproductive division of labor, and overlapping generations, represents a major evolutionary transition. A central paradox is that early models suggested diminishing returns to helping, making solitary reproduction seemingly more efficient. Here, we experimentally demonstrate increasing returns to scale from early-season helping in the primitively eusocial wasp Polistes gallicus. By manipulating the proportion of females allowed to remain as helpers, we show that while reproductive output scales linearly with worker numbers, total sexual productivity increases convexly with helper probability, thereby showing that early-season helping leads to compounding effects on reproductive output. Using these data, we parameterize a dynamic population genetic model and show that this convex relationship facilitates the spread of eusociality alleles more readily under monandry than polyandry, contrary to the conclusions of some prior models. Importantly, we show that compounding effects can cause eusociality to evolve even when helpers are no more efficient at rearing brood than solitary breeders. Our findings emphasize the value of integrating experimental data with mechanistically motivated theoretical models to study social evolution.

Natural populations often experience heterogeneity in the quality and abundance of environmentally acquired resources across both space and time, and this variation can influence population demographics and evolutionary dynamics. In this study, we directly manipulated diet in replicate populations of Drosophila melanogaster cultured in experimental mesocosms in the field. We found no significant effect of resource variation on estimates of adult census size. Resource variation altered patterns of phenotypic and genomic evolution across replicate populations; however, we find that this effect is secondary to selection driven by the fluctuating seasonal environment. Seasonal adaptation was observed for all traits assayed and elicited genome-wide signatures of selection. In contrast, adaptation to the resource environment was trait-specific and exhibited an oligogenic architecture. This illustrates the capacity of populations to adapt to a specific axis of variation (the resource environment) without hindering the adaptive response to seasonal change. This, in turn, suggests that resource variation may be an important force driving fluctuating selection across natural populations, ultimately contributing to the maintenance of genetic and phenotypic variation.

Understanding the structural changes that enable enzymes to remain active in extreme thermal conditions is of broad scientific interest for both fundamental and applied biological research. Three key mechanisms that underlie the thermal adaptation of enzymes are modifications in structural flexibility, compactness, and the contacts formed among amino acids. However, most previous studies on these topics have been limited to small sample sizes or a narrow taxonomic focus, and the importance of these factors to thermal adaptation remains poorly understood. In this study, we combined molecular dynamics simulations and phylogenetic comparative analyses to thoroughly analyze the structural factors underlying thermal adaptation in adenylate kinase—a key enzyme involved in cellular energy balance and homeostasis—across 70 prokaryotic species. We detect systematic increases in the flexibility of the enzyme with temperature, both across and within species. In contrast, structural compactness appears to be almost completely independent of temperature. Finally, we uncover a remarkable diversity in the number and types of amino acid contacts observed in different adenylate kinases that cannot be explained solely by temperature. Our results suggest that there are multiple paths toward the adaptation of prokaryotic adenylate kinases to extreme thermal environments and that these paths are generally accessible through changes in flexibility.

A particularly well-studied evolutionary model is the vinegar fly Drosophila melanogaster, a cosmopolitan insect of ancestral southern-central African origin. Recent work suggests that it expanded out of Africa ∼9,000 years ago, and spread from the Middle East into Europe ∼1,800 years ago. During its global expansion, this human commensal adapted to novel climate zones and habitats. Despite much work on phenotypic differentiation and adaptation on several continents (especially North America and Australia), typically in the context of latitudinal clines, little is known about phenotypic divergence among European populations. Here, we sought to provide a continent-wide study of phenotypic differentiation among European populations of D. melanogaster. In a consortium-wide phenomics effort, we assayed 16 fitness-related traits on a panel of 173 isofemale lines from 9 European populations, with the majority of traits measured by several groups using semi-standardized protocols. For most fitness-related traits, we found significant differentiation among populations on a continental scale. Despite inevitable differences in assay conditions among labs, the reproducibility and hence robustness of our measurements were overall remarkably good. Several fitness components (e.g., viability, development time) exhibited significant latitudinal or longitudinal clines, and populations differed markedly in multivariate trait structure. Notably, populations experiencing higher humidity/rainfall and lower maximum temperature showed higher viability, fertility, starvation resistance, and lifespan at the expense of lower heat-shock survival, suggesting a pattern of local adaptation. Our results indicate that derived populations of this tropical fly have been shaped by pervasive spatially varying multivariate selection and adaptation to different climates on the European continent.

Vision is a complex sensory system that requires coordination among cellular and morphological traits, and it remains unclear how functional relationships among traits interact with ecological selective pressures to shape the evolution of vision. Many species have specialized high visual acuity regions in the retina defined by patterns of ganglion cell density, which may evolve in response to ecological traits. For example, ganglion cell density can increase radially towards the center of the retina to form an area centralis, which is thought to improve acuity towards the center of the visual field in predators. Another example is the horizontal streak, where ganglion cells are dense in a horizontal pattern across the retina, which is thought to be beneficial in horizon-dominated habitats. At the morphological level, many have proposed that predation selects for high orbit convergence angles, or forward-facing eyes. We tested these hypotheses in a phylogenetic framework across eutherian mammals and found support for the association between the horizontal streak and horizon-dominated habitats. However, we did not find a significant association between orbit convergence and predation. We also tested if retinal specializations evolve in response to orbit convergence angles. We found that horizontal streaks were associated with side-facing eyes, potentially facilitating panoramic vision. Previous studies observed that some species with side-facing eyes have an area centralis shifted towards the temporal side of the retina, such that the high acuity region would project forward, but this relationship had not been tested quantitatively. We found that the temporal distance of the area centralis from the center of the retina was inversely correlated with orbit convergence, as predicted. Our work shows a strong relationship between orbit convergence and retinal specializations. We find support that both visual ecology and functional interactions among traits play important roles in the evolution of ocular traits across mammals.

Organism responses to environmental change require coordinated changes across correlated traits, so-called syndromes. For example, animals differ in their "pace-of-life syndrome" (POLS); suites of correlated life-history, behavioral and physiological traits. But standard "gene-centric" evolutionary theory cannot explain why POLSs exist because it assumes that the expression of phenotypic traits of animals is determined by genotype-specified reaction norms; it ignores that developmental processes can bias the direction of evolution so that phenotypes no longer match genotype-by-environment interactions. Here we apply a development-centric perspective to derive new POLS hypotheses that can resolve the conflict that current POLS predictions fail to explain which species/populations are resilient to environmental change.