Carlos A. Botero

Sexual selection accelerates signal evolution during speciation in birds

Sexual selection is proposed to be an important driver of diversification in animal systems, yet previous tests of this hypothesis have produced mixed results and the mechanisms involved remain unclear. Here, we use a novel phylogenetic approach to assess the influence of sexual selection on patterns of evolutionary change during 84 recent speciation events across 23 passerine bird families. We show that elevated levels of sexual selection are associated with more rapid phenotypic divergence between related lineages, and that this effect is restricted to male plumage traits proposed to function in mate choice and species recognition. Conversely, we found no evidence that sexual selection promoted divergence in female plumage traits, or in male traits related to foraging and locomotion. These results provide strong evidence that female choice and male–male competition are dominant mechanisms driving divergence during speciation in birds, potentially linking sexual selection to the accelerated evolution of pre-mating reproductive isolation.

Evolutionary tipping points in the capacity to adapt to environmental change

Significance Environmental variation is becoming more frequent and unpredictable as a consequence of climate change, yet we currently lack the tools to evaluate the extent to which organisms may adapt to this phenomenon. Here we develop a model that explores these issues and use it to study how changes in the timescale and predictability of environmental variation may ultimately affect population viability. Our model indicates that, although populations can often cope with fairly large changes in these environmental parameters, on occasion they will collapse abruptly and go extinct. We characterize the conditions under which these evolutionary tipping points occur and discuss how vulnerability to such cryptic threats may depend on the genetic architecture and life history of the organisms involved. In an era of rapid climate change, there is a pressing need to understand how organisms will cope with faster and less predictable variation in environmental conditions. Here we develop a unifying model that predicts evolutionary responses to environmentally driven fluctuating selection and use this theoretical framework to explore the potential consequences of altered environmental cycles. We first show that the parameter space determined by different combinations of predictability and timescale of environmental variation is partitioned into distinct regions where a single mode of response (reversible phenotypic plasticity, irreversible phenotypic plasticity, bet-hedging, or adaptive tracking) has a clear selective advantage over all others. We then demonstrate that, although significant environmental changes within these regions can be accommodated by evolution, most changes that involve transitions between regions result in rapid population collapse and often extinction. Thus, the boundaries between response mode regions in our model correspond to evolutionary tipping points, where even minor changes in environmental parameters can have dramatic and disproportionate consequences on population viability. Finally, we discuss how different life histories and genetic architectures may influence the location of tipping points in parameter space and the likelihood of extinction during such transitions. These insights can help identify and address some of the cryptic threats to natural populations that are likely to result from any natural or human-induced change in environmental conditions. They also demonstrate the potential value of evolutionary thinking in the study of global climate change.

The ecology of religious beliefs

Significance Here we show that the spatial prevalence of human societies that believe in moralizing high gods can be predicted with a high level of accuracy (91%) from historical, social, and ecological data. Using high-resolution datasets, we systematically estimate the relative effects of resource abundance, ecological risk, cultural diffusion, shared ancestry, and political complexity on the global distribution of beliefs in moralizing high gods. The methods presented in this paper provide a blueprint for how to leverage the increasing wealth of ecological, linguistic, and historical data to understand the forces that have shaped the behavior of our own species. Although ecological forces are known to shape the expression of sociality across a broad range of biological taxa, their role in shaping human behavior is currently disputed. Both comparative and experimental evidence indicate that beliefs in moralizing high gods promote cooperation among humans, a behavioral attribute known to correlate with environmental harshness in nonhuman animals. Here we combine fine-grained bioclimatic data with the latest statistical tools from ecology and the social sciences to evaluate the potential effects of environmental forces, language history, and culture on the global distribution of belief in moralizing high gods (n = 583 societies). After simultaneously accounting for potential nonindependence among societies because of shared ancestry and cultural diffusion, we find that these beliefs are more prevalent among societies that inhabit poorer environments and are more prone to ecological duress. In addition, we find that these beliefs are more likely in politically complex societies that recognize rights to movable property. Overall, our multimodel inference approach predicts the global distribution of beliefs in moralizing high gods with an accuracy of 91%, and estimates the relative importance of different potential mechanisms by which this spatial pattern may have arisen. The emerging picture is neither one of pure cultural transmission nor of simple ecological determinism, but rather a complex mixture of social, cultural, and environmental influences. Our methods and findings provide a blueprint for how the increasing wealth of ecological, linguistic, and historical data can be leveraged to understand the forces that have shaped the behavior of our own species.

Environmental harshness is positively correlated with intraspecific divergence in mammals and birds

Life on Earth is conspicuously more diverse in the tropics. Although this intriguing geographical pattern has been linked to many biotic and abiotic factors, their relative importance and potential interactions are still poorly understood. The way in which latitudinal changes in ecological conditions influence evolutionary processes is particularly controversial, as there is evidence for both a positive and a negative latitudinal gradient in speciation rates. Here, we identify and address some methodological issues (how patterns are analysed and how latitude is quantified) that could lead to such conflicting results. To address these issues, we assemble a comprehensive data set of the environmental correlates of latitude (including climate, net primary productivity and habitat heterogeneity) and combine it with biological, historical and molecular data to explore global patterns in recent divergence events (subspeciation). Surprisingly, we find that the harsher conditions that typify temperate habitats (lower primary productivity, decreased rainfall and more variable and unpredictable temperatures) are positively correlated with greater subspecies richness in terrestrial mammals and birds. Thus, our findings indicate that intraspecific divergence is greater in regions with lower biodiversity, a pattern that is robust to both sampling variation and latitudinal biases in taxonomic knowledge. We discuss possible causal mechanisms for the link between environmental harshness and subspecies richness (faster rates of evolution, greater likelihood of range discontinuities and more opportunities for divergence) and conclude that this pattern supports recent indications that latitudinal gradients of diversity are maintained by simultaneously higher potentials for both speciation and extinction in temperate than tropical regions.

Toward a Mechanistic Understanding of Linguistic Diversity

Our species displays remarkable linguistic diversity. Although the uneven distribution of this diversity demands explanation, the drivers of these patterns have not been conclusively determined. We address this issue in two steps: First, we review previous empirical studies whose authors have suggested environmental, geographical, and sociocultural drivers of linguistic diversification. However, contradictory results and methodological variation make it difficult to draw general conclusions. Second, we outline a program for future research. We suggest that future analyses should account for interactions among causal factors, the lack of spatial and phylogenetic independence of the data, and transitory patterns. Recent analytical advances in biogeography and evolutionary biology, such as simulation modeling of diversity patterns, hold promise for testing four key mechanisms of language diversification proposed here: neutral change, population movement, contact, and selection. Future modeling approaches should also evaluate how the outcomes of these processes are influenced by demography, environmental heterogeneity, and time.

D-PLACE: A Global Database of Cultural, Linguistic and Environmental Diversity

From the foods we eat and the houses we construct, to our religious practices and political organization, to who we can marry and the types of games we teach our children, the diversity of cultural practices in the world is astounding. Yet, our ability to visualize and understand this diversity is limited by the ways it has been documented and shared: on a culture-by-culture basis, in locally-told stories or difficult-to-access repositories. In this paper we introduce D-PLACE, the Database of Places, Language, Culture, and Environment. This expandable and open-access database (accessible at https://d-place.org) brings together a dispersed corpus of information on the geography, language, culture, and environment of over 1400 human societies. We aim to enable researchers to investigate the extent to which patterns in cultural diversity are shaped by different forces, including shared history, demographics, migration/diffusion, cultural innovations, and environmental and ecological conditions. We detail how D-PLACE helps to overcome four common barriers to understanding these forces: i) location of relevant cultural data, (ii) linking data from distinct sources using diverse ethnonyms, (iii) variable time and place foci for data, and (iv) spatial and historical dependencies among cultural groups that present challenges for analysis. D-PLACE facilitates the visualisation of relationships among cultural groups and between people and their environments, with results downloadable as tables, on a map, or on a linguistic tree. We also describe how D-PLACE can be used for exploratory, predictive, and evolutionary analyses of cultural diversity by a range of users, from members of the worldwide public interested in contrasting their own cultural practices with those of other societies, to researchers using large-scale computational phylogenetic analyses to study cultural evolution. In summary, we hope that D-PLACE will enable new lines of investigation into the major drivers of cultural change and global patterns of cultural diversity.

Different axes of environmental variation explain the presence vs. extent of cooperative nest founding associations in Polistes paper wasps

Ecological constraints on independent breeding are recognised as major drivers of cooperative breeding across diverse lineages. How the prevalence and degree of cooperative breeding relates to ecological variation remains unresolved. Using a large data set of cooperative nesting in Polistes wasps we demonstrate that different aspects of cooperative breeding are likely to be driven by different aspects of climate. Whether or not a species forms cooperative groups is associated with greater short-term temperature fluctuations. In contrast, the number of cooperative foundresses increases in more benign environments with warmer, wetter conditions. The same data set reveals that intraspecific responses to climate variation do not mirror genus-wide trends and instead are highly heterogeneous among species. Collectively these data suggest that the ecological drivers that lead to the origin or loss of cooperation are different from those that influence the extent of its expression within populations.

Family living sets the stage for cooperative breeding and ecological resilience in birds

Cooperative breeding is an extreme form of cooperation that evolved in a range of lineages, including arthropods, fish, birds, and mammals. Although cooperative breeding in birds is widespread and well-studied, the conditions that favored its evolution are still unclear. Based on phylogenetic comparative analyses on 3,005 bird species, we demonstrate here that family living acted as an essential stepping stone in the evolution of cooperative breeding in the vast majority of species. First, families formed by prolonging parent–offspring associations beyond nutritional independency, and second, retained offspring began helping at the nest. These findings suggest that assessment of the conditions that favor the evolution of cooperative breeding can be confounded if this process is not considered to include 2 steps. Specifically, phylogenetic linear mixed models show that the formation of families was associated with more productive and seasonal environments, where prolonged parent–offspring associations are likely to be less costly. However, our data show that the subsequent evolution of cooperative breeding was instead linked to environments with variable productivity, where helpers at the nest can buffer reproductive failure in harsh years. The proposed 2-step framework helps resolve current disagreements about the role of environmental forces in the evolution of cooperative breeding and better explains the geographic distribution of this trait. Many geographic hotspots of cooperative breeding have experienced a historical decline in productivity, suggesting that a higher proportion of family-living species could have been able to avoid extinction under harshening conditions through the evolution of cooperative breeding. These findings underscore the importance of considering the potentially different factors that drive different steps in the evolution of complex adaptations.

The promise and limits of eco-evolutionary studies of human culture

Extending genomics to natural communities and ecosystems. Science, 320, 492–495. Willig, M. R., Kaufman, D. M., & Stevens, R. D. (2003). Latitudinal gradients of biodiversity: Pattern, process, scale and synthesis. Annual Review of Ecology, Evolution, and Systematics, 34, 273–309. Wilson, D. S. (1980). The natural selection of populations and communities (p. 186). Menlo Park, CA: Benjamin/ Cummings. Wilson, D. S. (1997). Biological communities as functionally organized units. Ecology, 78(7), 2018–2024. Wilson, D. S. (2002). Darwin’s cathedral: Evolution, religion and the nature of society. Chicago: University of Chicago Press. Wilson, D. S. (2005a). Testing major evolutionary hypotheses about religion with a random sample. Human Nature, 16, 382–409. Wilson, D. S. (2005b). Evolutionary social constructivism. In J. Gottshcall & D. S. Wilson (Eds.), The literary animal: Evolution and the nature of narrative (pp. 20–37). Evanston, IL: Northwestern University Press. Wilson, D. S. (2011). The neighborhood project: Using evolution to improve my city, one block at a time. New York: Little, Brown. Wilson, D. S. (2012). Human cultures are primarily adaptive at the group level. Social Evolution Forum. Retrieved from https://evolution-institute.org/focus-article/david-sloan-wilson-human-cultures-are-primarily-adaptive-atthe-group-level/ Wilson, D. S. (2015). Does altruism exist? New Haven: Yale University Press. Wilson, D. S., & Wilson, E. O. (2007). Rethinking the theoretical foundation of sociobiology. Quarterly Review of Biology, 82, 327–348. Wilson, E. O. (2012). The social conquest of earth. New York: Norton. Yaworsky, W., Horowitz, M., & Kickham, K. (2015). Gender and politics among anthropologists in the units of selection debate. Biological Theory, 10(2), 145–155. doi:10.1007/s13752-014-0196-5

Big brains stabilize populations and facilitate colonization of variable habitats in birds

The cognitive buffer hypothesis posits that environmental variability can be a major driver of the evolution of cognition because an enhanced ability to produce flexible behavioural responses facilitates coping with the unexpected. Although comparative evidence supports different aspects of this hypothesis, a direct connection between cognition and the ability to survive a variable and unpredictable environment has yet to be demonstrated. Here, we use complementary demographic and evolutionary analyses to show that among birds, the mechanistic premise of this hypothesis is well supported but the implied direction of causality is not. Specifically, we show that although population dynamics are more stable and less affected by environmental variation in birds with larger relative brain sizes, the evolution of larger brains often pre-dated and facilitated the colonization of variable habitats rather than the other way around. Our findings highlight the importance of investigating the timeline of evolutionary events when interpreting patterns of phylogenetic correlation.The ability to cope with environmental variability is thought to be a major driver of brain-size evolution. Here, the authors show that cognitive capacity in birds may instead have pre-dated and facilitated the colonization of variable habitats.