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1. A Synthesis of Game Theory and Quantitative Genetic Models of Social Evolution

   https://doi.org/10.1093/jhered/esab064  

   McGlothlin, Joel W.; Akçay, Erol; Brodie, III, Edmund D.; Moore, Allen J.; Van Cleve, Jeremy; Hughes, ed., Kimberly (February 2022, Journal of Heredity)

   Abstract Two popular approaches for modeling social evolution, evolutionary game theory and quantitative genetics, ask complementary questions but are rarely integrated. Game theory focuses on evolutionary outcomes, with models solving for evolutionarily stable equilibria, whereas quantitative genetics provides insight into evolutionary processes, with models predicting short-term responses to selection. Here we draw parallels between evolutionary game theory and interacting phenotypes theory, which is a quantitative genetic framework for understanding social evolution. First, we show how any evolutionary game may be translated into two quantitative genetic selection gradients, nonsocial and social selection, which may be used to predict evolutionary change from a single round of the game. We show that synergistic fitness effects may alter predicted selection gradients, causing changes in magnitude and sign as the population mean evolves. Second, we show how evolutionary games involving plastic behavioral responses to partners can be modeled using indirect genetic effects, which describe how trait expression changes in response to genes in the social environment. We demonstrate that repeated social interactions in models of reciprocity generate indirect effects and conversely, that estimates of parameters from indirect genetic effect models may be used to predict the evolution of reciprocity. We argue that a pluralistic view incorporating both theoretical approaches will benefit empiricists and theorists studying social evolution. We advocate the measurement of social selection and indirect genetic effects in natural populations to test the predictions from game theory and, in turn, the use of game theory models to aid in the interpretation of quantitative genetic estimates. 

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2. Sorting of persistent morphological polymorphisms links paleobiological pattern to population process

   https://doi.org/10.1017/pab.2023.27  

   Parins-Fukuchi, C. Tomomi (October 2023, Paleobiology)

   Biological variation fuels evolutionary change. Across longer timescales, however, polymorphisms at both the genomic and phenotypic levels often persist longer than would be expected under standard population genetic models such as positive selection or genetic drift. Explaining the maintenance of this variation within populations across long time spans via balancing selection has been a major triumph of theoretical population genetics and ecology. Although persistent polymorphisms can often be traced in fossil lineages over long periods through the rock record, paleobiology has had little to say about either the long-term maintenance of phenotypic variation or its macroevolutionary consequences. I explore the dynamics that occur when persistent polymorphisms maintained over long lineage durations are filtered into descendant lineages during periods of demographic upheaval that occur at speciation. I evaluate these patterns in two lineages:Ectocion, a genus of Eocene mammals, and botryocrinids, a Mississippian cladid crinoid family. Following origination, descendants are less variable than their ancestors. The patterns by which ancestral variation is sorted cannot be distinguished from drift. Maintained and accumulated polymorphisms in highly variable ancestral lineages such asBarycrinus rhombiferusOwen and Shumard, 1852 may fuel radiations as character states are sorted into multiple descendant lineages. Interrogating the conditions under which trans-specific polymorphism is either maintained or lost during periods of demographic and ecological upheaval can explain how population-level processes contribute to the emergent macroevolutionary dynamics that shape the history of life as preserved in the fossil record. 

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3. Linking pathogen–microbiome–host interactions to explain amphibian population dynamics

   https://doi.org/10.1111/mec.16701  

   Torres‐Sánchez, María; Longo, Ana V (November 2022, Molecular Ecology)

   Abstract Symbiotic interactions can determine the evolutionary trajectories of host species, influencing genetic variation through selection and changes in demography. In the context of strong selective pressures such as those imposed by infectious diseases, symbionts providing defences could contribute to increase host fitness upon pathogen emergence. Here, we generated genome‐wide data of an amphibian species to find evidence of evolutionary pressures driven by two skin symbionts: a batrachochytrid fungal pathogen and an antifungal bacterium. Using demographic modelling, we found evidence of decreased effective population size, probably due to pathogen infections. Additionally, we investigated host genetic associations with infection status, antifungal bacterium abundance and overall microbiome diversity using structural equation models. We uncovered relatively lower nucleotide diversity in infected frogs and potential heterozygote advantage to recruit the candidate beneficial symbiont and fight infections. Our models indicate that environmental conditions have indirect effects on symbiont abundance through both host body traits and microbiome diversity. Likewise, we uncovered a potential offsetting effect among host heterozygosity–fitness correlations, plausibly pointing to different ecological and evolutionary processes among the three species due to dynamic interactions. Our findings revealed that evolutionary pressures not only arise from the pathogen but also from the candidate beneficial symbiont, and both interactions shape the genetics of the host. Our results advance knowledge about multipartite symbiotic relationships and provide a framework to model ecological and evolutionary dynamics in wild populations. Finally, our study approach can be applied to inform conservation actions such as bioaugmentation strategies for other imperilled amphibians affected by infectious diseases. 

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4. Genomic and fitness consequences of a near-extinction event in the northern elephant seal

   https://doi.org/10.1038/s41559-024-02533-2  

   Hoffman, Joseph I; Vendrami, David_L J; Hench, Kosmas; Chen, Rebecca S; Stoffel, Martin A; Kardos, Marty; Amos, William; Kalinowski, Jörn; Rickert, Daniel; Köhrer, Karl; et al (December 2024, Nature Ecology & Evolution)

   Abstract Understanding the genetic and fitness consequences of anthropogenic bottlenecks is crucial for biodiversity conservation. However, studies of bottlenecked populations combining genomic approaches with fitness data are rare. Theory predicts that severe bottlenecks deplete genetic diversity, exacerbate inbreeding depression and decrease population viability. However, actual outcomes are complex and depend on how a species’ unique demography affects its genetic load. We used population genetic and veterinary pathology data, demographic modelling, whole-genome resequencing and forward genetic simulations to investigate the genomic and fitness consequences of a near-extinction event in the northern elephant seal. We found no evidence of inbreeding depression within the contemporary population for key fitness components, including body mass, blubber thickness and susceptibility to parasites and disease. However, we detected a genomic signature of a recent extreme bottleneck (effective population size = 6; 95% confidence interval = 5.0–7.5) that will have purged much of the genetic load, potentially leading to the lack of observed inbreeding depression in our study. Our results further suggest that deleterious genetic variation strongly impacted the post-bottleneck population dynamics of the northern elephant seal. Our study provides comprehensive empirical insights into the intricate dynamics underlying species-specific responses to anthropogenic bottlenecks. 

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5. Museum Genomics Reveals Temporal Genetic Stasis and Global Genetic Diversity in Arabidopsis thaliana

   https://doi.org/10.1111/mec.70081  

   Lopez, Lua; Lang, Patricia_L M; Marciniak, Stephanie; Kistler, Logan; Latorre, Sergio M; Haile, Asnake; Vasquez_Cerda, Eleanna; Gamba, Diana; Xu, Yuxing; Woods, Patrick; et al (October 2025, Molecular Ecology)

   Global patterns of population genetic variation through time offer a window into evolutionary processes that maintain diversity. Over time, lineages may expand or contract their distribution, causing turnover in population genetic composition. At individual loci, migration, drift and selection (among other processes) may affect allele frequencies. Museum specimens of widely distributed species offer a unique window into the genetics of understudied populations and changes over time. Here, we sequenced genomes of 130 herbarium specimens and 91 new field collections of Arabidopsis thaliana and combined these with published genomes. We sought a broader view of genomic diversity across the species and to test if population genomic composition is changing through time. We documented extensive and previously uncharacterised diversity in a range of populations in Africa, populations that are under threat from anthropogenic climate change. Through time, we did not find dramatic changes in genomic composition of populations. Instead, we found a pattern of genetic change every 100 years of the same magnitude seen when comparing Eurasian populations that are 185 km apart, potentially due to a combination of drift and changing selection. We found only mixed signals of polygenic adaptation at phenology and physiology QTL. We did find that genes conserved across eudicots show altered levels of directional allele frequency change, potentially due to variable purifying and background selection. Our study highlights how museum specimens can reveal new dimensions of population diversity and show how wild populations are evolving in recent history. 

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