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1. 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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2. Detecting deviations from Kingman coalescence using 2-site frequency spectra

   https://doi.org/10.1093/genetics/iyaf023  

   Fenton, Eliot_F; Rice, Daniel_P; Novembre, John; Desai, Michael_M; Lohse, ed., K. (February 2025, GENETICS)

   Abstract Demographic inference methods in population genetics typically assume that the ancestry of a sample can be modeled by the Kingman coalescent. A defining feature of this stochastic process is that it generates genealogies that are binary trees: no more than 2 ancestral lineages may coalesce at the same time. However, this assumption breaks down under several scenarios. For example, pervasive natural selection and extreme variation in offspring number can both generate genealogies with “multiple-merger” events in which more than 2 lineages coalesce instantaneously. Therefore, detecting violations of the Kingman assumptions (e.g. due to multiple mergers) is important both for understanding which forces have shaped the diversity of a population and for avoiding fitting misspecified models to data. Current methods to detect deviations from Kingman coalescence in genomic data rely primarily on the site frequency spectrum (SFS). However, the signatures of some non-Kingman processes (e.g. multiple mergers) in the SFS are also consistent with a Kingman coalescent with a time-varying population size. Here, we present a new statistical test for determining whether the Kingman coalescent with any population size history is consistent with population data. Our approach is based on information contained in the 2-site joint frequency spectrum (2-SFS) for pairs of linked sites, which has a different dependence on the topologies of genealogies than the SFS. Our statistical test is global in the sense that it can detect when the genome-wide genetic diversity is inconsistent with the Kingman model, rather than detecting outlier regions, as in selection scan methods. We validate this test using simulations and then apply it to demonstrate that genomic diversity data from Drosophila melanogaster is inconsistent with the Kingman coalescent. 

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3. Conservation Genomics in the Sagebrush Sea: Population Divergence, Demographic History, and Local Adaptation in Sage-Grouse (Centrocercus spp.)

   https://doi.org/10.1093/gbe/evz112  

   Oh, Kevin P; Aldridge, Cameron L; Forbey, Jennifer S; Dadabay, Carolyn Y; Oyler-McCance, Sara J; Baer, Charles (July 2019, Genome Biology and Evolution)

   Abstract Sage-grouse are two closely related iconic species of the North American West, with historically broad distributions across sagebrush-steppe habitat. Both species are dietary specialists on sagebrush during winter, with presumed adaptations to tolerate the high concentrations of toxic secondary metabolites that function as plant chemical defenses. Marked range contraction and declining population sizes since European settlement have motivated efforts to identify distinct population genetic variation, particularly that which might be associated with local genetic adaptation and dietary specialization of sage-grouse. We assembled a reference genome and performed whole-genome sequencing across sage-grouse from six populations, encompassing both species and including several populations on the periphery of the species ranges. Population genomic analyses reaffirmed genome-wide differentiation between greater and Gunnison sage-grouse, revealed pronounced intraspecific population structure, and highlighted important differentiation of a small isolated population of greater sage-grouse in the northwest of the range. Patterns of genome-wide differentiation were largely consistent with a hypothesized role of genetic drift due to limited gene flow among populations. Inferred ancient population demography suggested persistent declines in effective population sizes that have likely contributed to differentiation within and among species. Several genomic regions with single-nucleotide polymorphisms exhibiting extreme population differentiation were associated with candidate genes linked to metabolism of xenobiotic compounds. In vitro activity of enzymes isolated from sage-grouse livers supported a role for these genes in detoxification of sagebrush, suggesting that the observed interpopulation variation may underlie important local dietary adaptations, warranting close consideration for conservation strategies that link sage-grouse to the chemistry of local sagebrush. 

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4. Seasonally migratory songbirds have different historic population size characteristics than resident relatives

   https://doi.org/10.7554/eLife.90848.2  

   Winker, Kevin; Delmore, Kira (February 2025, elife)

   Modern genomic methods enable estimation of a lineage’s long-term effective population sizes back to its origins. This ability allows unprecedented opportunities to determine how adoption of a major life-history trait affects lineages’ populations relative to those without the trait. We used this novel approach to study the population effects of the life-history trait of seasonal migration across evolutionary time. Seasonal migration is a common life-history strategy, but its effects on long-term population sizes relative to lineages that don’t migrate are largely unknown. Using whole-genome data, we estimated effective population sizes over millions of years in closely related seasonally migratory and resident lineages in a group of songbirds. Our main predictions were borne out: Seasonal migration is associated with larger effective population sizes (Ne), greater long-term variation in Ne, and a greater degree of initial population growth than among resident lineages. Initial growth periods were remarkably long (0.63-4.29 Myr), paralleling the expansion and adaptation phases of taxon cycles, a framework of lineage expansion and eventual contraction over time encompassing biogeography and evolutionary ecology. Heterogeneity among lineages is noteworthy, despite geographic proximity (including overlap) and close relatedness. Seasonal migration imbues these lineages with fundamentally different population size attributes through evolutionary time compared to closely related resident lineages. 

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5. Genetic decline and recovery of a demographically rebuilt fishery species

   https://doi.org/10.1111/mec.16697  

   Hoey, Jennifer A.; Able, Kenneth W.; Pinsky, Malin L. (November 2022, Molecular Ecology)

   Abstract The demographic history of a population is important for conservation and evolution, but this history is unknown for many populations. Methods that use genomic data have been developed to infer demography, but they can be challenging to implement and interpret, particularly for large populations. Thus, understanding if and when genetic estimates of demography correspond to true population history is important for assessing the performance of these genetic methods. Here, we used double‐digest restriction‐site associated DNA (ddRAD) sequencing data from archived collections of larval summer flounder (Paralichthys dentatus,n = 279) from three cohorts (1994–1995, 1997–1998 and 2008–2009) along the U.S. East coast to examine how contemporary effective population size and genetic diversity responded to changes in abundance in a natural population. Despite little to no detectable change in genetic diversity, coalescent‐based demographic modelling from site frequency spectra revealed that summer flounder effective population size declined dramatically in the early 1980s. The timing and direction of change corresponded well with the observed decline in spawning stock census abundance in the late 1980s from independent fish surveys. Census abundance subsequently recovered and achieved the prebottleneck size. Effective population size also grew following the bottleneck. Our results for summer flounder demonstrate that genetic sampling and site frequency spectra can be useful for detecting population dynamics, even in species with large effective sizes. 

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