[{"OA_type":"green","oa_version":"Preprint","title":"Genetic load, eco-evolutionary feedback, and extinction in metapopulations","date_created":"2026-02-18T10:47:18Z","publication_identifier":{"eissn":["1537-5323"],"issn":["0003-0147"]},"publication_status":"published","related_material":{"record":[{"relation":"earlier_version","status":"public","id":"14732"}]},"pmid":1,"publisher":"University of Chicago Press","article_processing_charge":"No","corr_author":"1","department":[{"_id":"JaMa"},{"_id":"NiBa"}],"month":"06","project":[{"name":"Causes and consequences of population fragmentation","grant_number":"P32896","_id":"c08d3278-5a5b-11eb-8a69-fdb09b55f4b8"},{"_id":"34c872fe-11ca-11ed-8bc3-8534b82131e6","grant_number":"26380","name":"Polygenic Adaptation in a Metapopulation"},{"grant_number":"26293","_id":"34d33d68-11ca-11ed-8bc3-ec13763c0ca8","name":"The impact of deleterious mutations on small populations"}],"article_type":"original","author":[{"full_name":"Olusanya, Oluwafunmilola O","last_name":"Olusanya","id":"41AD96DC-F248-11E8-B48F-1D18A9856A87","first_name":"Oluwafunmilola O","orcid":"0000-0003-1971-8314"},{"last_name":"Khudiakova","full_name":"Khudiakova, Kseniia","orcid":"0000-0002-6246-1465","first_name":"Kseniia","id":"4E6DC800-AE37-11E9-AC72-31CAE5697425"},{"first_name":"Himani","id":"42377A0A-F248-11E8-B48F-1D18A9856A87","full_name":"Sachdeva, Himani","last_name":"Sachdeva"}],"volume":205,"oa":1,"doi":"10.1086/735562","acknowledgement":"This research was partially funded by the Austrian Science Fund (FWF P-32896B) and DOC Fellowships of the Austrian Academy of Sciences: grants 26380 (O.O.) and 26293 (K.K.). We thank Nick Barton for useful comments on the chapter in O.O.’s thesis that led to this article.","main_file_link":[{"open_access":"1","url":"https://doi.org/10.1101/2023.12.02.569702"}],"OA_place":"repository","date_published":"2025-06-01T00:00:00Z","user_id":"ba8df636-2132-11f1-aed0-ed93e2281fdd","year":"2025","intvolume":"       205","day":"01","citation":{"ama":"Olusanya OO, Khudiakova K, Sachdeva H. Genetic load, eco-evolutionary feedback, and extinction in metapopulations. <i>The American Naturalist</i>. 2025;205(6):617-636. doi:<a href=\"https://doi.org/10.1086/735562\">10.1086/735562</a>","ista":"Olusanya OO, Khudiakova K, Sachdeva H. 2025. Genetic load, eco-evolutionary feedback, and extinction in metapopulations. The American Naturalist. 205(6), 617–636.","chicago":"Olusanya, Oluwafunmilola O, Kseniia Khudiakova, and Himani Sachdeva. “Genetic Load, Eco-Evolutionary Feedback, and Extinction in Metapopulations.” <i>The American Naturalist</i>. University of Chicago Press, 2025. <a href=\"https://doi.org/10.1086/735562\">https://doi.org/10.1086/735562</a>.","mla":"Olusanya, Oluwafunmilola O., et al. “Genetic Load, Eco-Evolutionary Feedback, and Extinction in Metapopulations.” <i>The American Naturalist</i>, vol. 205, no. 6, University of Chicago Press, 2025, pp. 617–36, doi:<a href=\"https://doi.org/10.1086/735562\">10.1086/735562</a>.","short":"O.O. Olusanya, K. Khudiakova, H. Sachdeva, The American Naturalist 205 (2025) 617–636.","ieee":"O. O. Olusanya, K. Khudiakova, and H. Sachdeva, “Genetic load, eco-evolutionary feedback, and extinction in metapopulations,” <i>The American Naturalist</i>, vol. 205, no. 6. University of Chicago Press, pp. 617–636, 2025.","apa":"Olusanya, O. O., Khudiakova, K., &#38; Sachdeva, H. (2025). Genetic load, eco-evolutionary feedback, and extinction in metapopulations. <i>The American Naturalist</i>. University of Chicago Press. <a href=\"https://doi.org/10.1086/735562\">https://doi.org/10.1086/735562</a>"},"quality_controlled":"1","type":"journal_article","external_id":{"pmid":["40446297 "]},"language":[{"iso":"eng"}],"_id":"21322","abstract":[{"text":"Habitat fragmentation poses a significant risk to population survival, causing both demographic stochasticity and genetic drift within local populations to increase, thereby increasing genetic load. Higher load causes population numbers to decline, which reduces the efficiency of selection and further increases load, resulting in a positive feedback that may drive entire populations to extinction. Here, we investigate this eco-evolutionary feedback in a metapopulation consisting of local demes connected via migration, with individuals subject to deleterious mutation at a large number of loci. We first analyze the determinants of load under soft selection, where population sizes are fixed, and then build on this to understand hard selection, where population sizes and load coevolve. We show that under soft selection, very little gene flow (less than one migrant per generation) is enough to prevent fixation of deleterious alleles. By contrast, much higher levels of migration are required to mitigate load and prevent extinction when selection is hard, with critical migration thresholds for metapopulation persistence increasing sharply as the genome-wide deleterious mutation rate becomes comparable to the baseline population growth rate. Moreover, critical migration thresholds are highest if deleterious mutations have intermediate selection coefficients but lower if alleles are predominantly recessive rather than additive (due to more efficient purging of recessive load within local populations). Our analysis is based on a combination of analytical approximations and simulations, allowing for a more comprehensive understanding of the factors influencing load and extinction in fragmented populations.","lang":"eng"}],"scopus_import":"1","issue":"6","status":"public","page":"617-636","date_updated":"2026-04-07T08:45:14Z","publication":"The American Naturalist"},{"acknowledged_ssus":[{"_id":"SSU"}],"date_updated":"2026-04-07T12:54:29Z","file_date_updated":"2024-01-03T18:31:34Z","license":"https://creativecommons.org/licenses/by-nc-sa/4.0/","ec_funded":1,"status":"public","page":"183","citation":{"ama":"Olusanya OO. Local adaptation, genetic load and extinction in metapopulations. 2024. doi:<a href=\"https://doi.org/10.15479/at:ista:14711\">10.15479/at:ista:14711</a>","ista":"Olusanya OO. 2024. Local adaptation, genetic load and extinction in metapopulations. Institute of Science and Technology Austria.","chicago":"Olusanya, Oluwafunmilola O. “Local Adaptation, Genetic Load and Extinction in Metapopulations.” Institute of Science and Technology Austria, 2024. <a href=\"https://doi.org/10.15479/at:ista:14711\">https://doi.org/10.15479/at:ista:14711</a>.","mla":"Olusanya, Oluwafunmilola O. <i>Local Adaptation, Genetic Load and Extinction in Metapopulations</i>. Institute of Science and Technology Austria, 2024, doi:<a href=\"https://doi.org/10.15479/at:ista:14711\">10.15479/at:ista:14711</a>.","short":"O.O. Olusanya, Local Adaptation, Genetic Load and Extinction in Metapopulations, Institute of Science and Technology Austria, 2024.","ieee":"O. O. Olusanya, “Local adaptation, genetic load and extinction in metapopulations,” Institute of Science and Technology Austria, 2024.","apa":"Olusanya, O. O. (2024). <i>Local adaptation, genetic load and extinction in metapopulations</i>. Institute of Science and Technology Austria. <a href=\"https://doi.org/10.15479/at:ista:14711\">https://doi.org/10.15479/at:ista:14711</a>"},"day":"19","has_accepted_license":"1","type":"dissertation","_id":"14711","language":[{"iso":"eng"}],"abstract":[{"lang":"eng","text":"In nature, different species find their niche in a range of environments, each with its unique characteristics. While some thrive in uniform (homogeneous) landscapes where environmental conditions stay relatively consistent across space, others traverse the complexities of spatially heterogeneous terrains. Comprehending how species are distributed and how they interact within these landscapes holds the key to gaining insights into their evolutionary dynamics while also informing conservation and management strategies.\r\n\r\nFor species inhabiting heterogeneous landscapes, when the rate of dispersal is low compared to spatial fluctuations in selection pressure, localized adaptations may emerge. Such adaptation in response to varying selection strengths plays an important role in the persistence of populations in our rapidly changing world. Hence, species in nature are continuously in a struggle to adapt to local environmental conditions, to ensure their continued survival. Natural populations can often adapt in time scales short enough for evolutionary changes to influence ecological dynamics and vice versa, thereby creating a feedback between evolution and demography. The analysis of this feedback and the relative contributions of gene flow, demography, drift, and natural selection to genetic variation and differentiation has remained a recurring theme in evolutionary biology. Nevertheless, the effective role of these forces in maintaining variation and shaping patterns of diversity is not fully understood. Even in homogeneous environments devoid of local adaptations, such understanding remains elusive. Understanding this feedback is crucial, for example in determining the conditions under which extinction risk can be mitigated in peripheral populations subject to deleterious mutation accumulation at the edges of species’ ranges\r\nas well as in highly fragmented populations.\r\n\r\nIn this thesis we explore both uniform and spatially heterogeneous metapopulations, investigating and providing theoretical insights into the dynamics of local adaptation in the latter and examining the dynamics of load and extinction as well as the impact of joint ecological and evolutionary (eco-evolutionary) dynamics in the former. The thesis is divided into 5 chapters.\r\n\r\nChapter 1 provides a general introduction into the subject matter, clarifying concepts and ideas used throughout the thesis. In chapter 2, we explore how fast a species distributed across a heterogeneous landscape adapts to changing conditions marked by alterations in carrying capacity, selection pressure, and migration rate.\r\n\r\nIn chapter 3, we investigate how migration selection and drift influences adaptation and the maintenance of variation in a metapopulation with three habitats, an extension of previous models of adaptation in two habitats. We further develop analytical approximations for the critical threshold required for polymorphism to persist.\r\n\r\nThe focus of chapter 4 of the thesis is on understanding the interplay between ecology and evolution as coupled processes. We investigate how eco-evolutionary feedback between migration, selection, drift, and demography influences eco-evolutionary outcomes in marginal populations subject to deleterious mutation accumulation. Using simulations as well as theoretical approximations of the coupled dynamics of population size and allele frequency, we analyze how gene flow from a large mainland source influences genetic load and population size on an island (i.e., in a marginal population) under genetically realistic assumptions. Analyses of this sort are important because small isolated populations, are repeatedly affected by complex interactions between ecological and evolutionary processes, which can lead to their death. Understanding these interactions can therefore provide an insight into the conditions under which extinction risk can be mitigated in peripheral populations thus, contributing to conservation and restoration efforts.\r\n\r\nChapter 5 extends the analysis in chapter 4 to consider the dynamics of load (due to deleterious mutation accumulation) and extinction risk in a metapopulation. We explore the role of gene flow, selection, and dominance on load and extinction risk and further pinpoint critical thresholds required for metapopulation persistence.\r\n\r\nOverall this research contributes to our understanding of ecological and evolutionary mechanisms that shape species’ persistence in fragmented landscapes, a crucial foundation for successful conservation efforts and biodiversity management."}],"OA_place":"publisher","date_published":"2024-01-19T00:00:00Z","ddc":["576"],"user_id":"ba8df636-2132-11f1-aed0-ed93e2281fdd","year":"2024","month":"01","department":[{"_id":"NiBa"},{"_id":"GradSch"}],"project":[{"name":"International IST Doctoral Program","grant_number":"665385","_id":"2564DBCA-B435-11E9-9278-68D0E5697425","call_identifier":"H2020"},{"name":"Causes and consequences of population fragmentation","_id":"c08d3278-5a5b-11eb-8a69-fdb09b55f4b8","grant_number":"P32896"},{"grant_number":"26380","_id":"34c872fe-11ca-11ed-8bc3-8534b82131e6","name":"Polygenic Adaptation in a Metapopulation"}],"author":[{"orcid":"0000-0003-1971-8314","id":"41AD96DC-F248-11E8-B48F-1D18A9856A87","first_name":"Oluwafunmilola O","full_name":"Olusanya, Oluwafunmilola O","last_name":"Olusanya"}],"doi":"10.15479/at:ista:14711","oa":1,"degree_awarded":"PhD","related_material":{"record":[{"id":"10787","status":"public","relation":"part_of_dissertation"},{"status":"public","id":"10658","relation":"part_of_dissertation"},{"id":"14732","status":"public","relation":"part_of_dissertation"}]},"publisher":"Institute of Science and Technology Austria","article_processing_charge":"No","corr_author":"1","tmp":{"short":"CC BY-NC-SA (4.0)","image":"/images/cc_by_nc_sa.png","legal_code_url":"https://creativecommons.org/licenses/by-nc-sa/4.0/legalcode","name":"Creative Commons Attribution-NonCommercial-ShareAlike 4.0 International (CC BY-NC-SA 4.0)"},"file":[{"access_level":"closed","date_created":"2024-01-03T18:30:13Z","file_size":16986244,"content_type":"application/zip","file_name":"FinalSubmission_Thesis_OLUSANYA.zip","checksum":"de179b1c6758f182ff0c70d8b38c1501","file_id":"14730","date_updated":"2024-01-03T18:30:13Z","creator":"oolusany","relation":"source_file"},{"checksum":"0e331585e3cd4823320aab4e69e64ccf","file_name":"FinalSubmission2_Thesis_OLUSANYA.pdf","file_id":"14731","creator":"oolusany","relation":"main_file","date_updated":"2024-01-03T18:31:34Z","access_level":"open_access","content_type":"application/pdf","success":1,"file_size":6460403,"date_created":"2024-01-03T18:31:34Z"}],"publication_status":"published","supervisor":[{"last_name":"Barton","full_name":"Barton, Nicholas H","orcid":"0000-0002-8548-5240","id":"4880FE40-F248-11E8-B48F-1D18A9856A87","first_name":"Nicholas H"},{"first_name":"Jitka","full_name":"Polechova, Jitka","last_name":"Polechova"},{"first_name":"Himani","full_name":"Sachdeva, Himani","last_name":"Sachdeva"}],"oa_version":"Published Version","alternative_title":["ISTA Thesis"],"date_created":"2023-12-26T22:49:53Z","title":"Local adaptation, genetic load and extinction in metapopulations","publication_identifier":{"issn":["2663-337X"]}},{"date_published":"2023-12-04T00:00:00Z","OA_place":"repository","date_created":"2024-01-04T09:35:54Z","title":"Genetic load, eco-evolutionary feedback and extinction in a metapopulation","oa_version":"Preprint","main_file_link":[{"open_access":"1","url":"https://www.biorxiv.org/content/10.1101/2023.12.02.569702v1"}],"year":"2023","user_id":"2DF688A6-F248-11E8-B48F-1D18A9856A87","citation":{"ama":"Olusanya OO, Khudiakova K, Sachdeva H. Genetic load, eco-evolutionary feedback and extinction in a metapopulation. <i>bioRxiv</i>. doi:<a href=\"https://doi.org/10.1101/2023.12.02.569702\">10.1101/2023.12.02.569702</a>","ista":"Olusanya OO, Khudiakova K, Sachdeva H. Genetic load, eco-evolutionary feedback and extinction in a metapopulation. bioRxiv, <a href=\"https://doi.org/10.1101/2023.12.02.569702\">10.1101/2023.12.02.569702</a>.","chicago":"Olusanya, Oluwafunmilola O, Kseniia Khudiakova, and Himani Sachdeva. “Genetic Load, Eco-Evolutionary Feedback and Extinction in a Metapopulation.” <i>BioRxiv</i>, n.d. <a href=\"https://doi.org/10.1101/2023.12.02.569702\">https://doi.org/10.1101/2023.12.02.569702</a>.","mla":"Olusanya, Oluwafunmilola O., et al. “Genetic Load, Eco-Evolutionary Feedback and Extinction in a Metapopulation.” <i>BioRxiv</i>, doi:<a href=\"https://doi.org/10.1101/2023.12.02.569702\">10.1101/2023.12.02.569702</a>.","short":"O.O. Olusanya, K. Khudiakova, H. Sachdeva, BioRxiv (n.d.).","ieee":"O. O. Olusanya, K. Khudiakova, and H. Sachdeva, “Genetic load, eco-evolutionary feedback and extinction in a metapopulation,” <i>bioRxiv</i>. .","apa":"Olusanya, O. O., Khudiakova, K., &#38; Sachdeva, H. (n.d.). Genetic load, eco-evolutionary feedback and extinction in a metapopulation. <i>bioRxiv</i>. <a href=\"https://doi.org/10.1101/2023.12.02.569702\">https://doi.org/10.1101/2023.12.02.569702</a>"},"day":"04","language":[{"iso":"eng"}],"_id":"14732","abstract":[{"text":"Fragmented landscapes pose a significant threat to the persistence of species as they are highly susceptible to heightened risk of extinction due to the combined effects of genetic and demographic factors such as genetic drift and demographic stochasticity. This paper explores the intricate interplay between genetic load and extinction risk within metapopulations with a focus on understanding the impact of eco-evolutionary feedback mechanisms. We distinguish between two models of selection: soft selection, characterised by subpopulations maintaining carrying capacity despite load, and hard selection, where load can significantly affect population size. Within the soft selection framework, we investigate the impact of gene flow on genetic load at a single locus, while also considering the effect of selection strength and dominance coefficient. We subsequently build on this to examine how gene flow influences both population size and load under hard selection as well as identify critical thresholds for metapopulation persistence. Our analysis employs the diffusion, semi-deterministic and effective migration approximations. Our findings reveal that under soft selection, even modest levels of migration can significantly alleviate the burden of load. In sharp contrast, with hard selection, a much higher degree of gene flow is required to mitigate load and prevent the collapse of the metapopulation. Overall, this study sheds light into the crucial role migration plays in shaping the dynamics of genetic load and extinction risk in fragmented landscapes, offering valuable insights for conservation strategies and the preservation of diversity in a changing world.","lang":"eng"}],"type":"preprint","publication_status":"draft","license":"https://creativecommons.org/licenses/by-nc-nd/4.0/","related_material":{"record":[{"relation":"later_version","id":"21322","status":"public"},{"status":"public","id":"14711","relation":"dissertation_contains"}]},"corr_author":"1","tmp":{"image":"/images/cc_by_nc_nd.png","short":"CC BY-NC-ND (4.0)","name":"Creative Commons Attribution-NonCommercial-NoDerivatives 4.0 International (CC BY-NC-ND 4.0)","legal_code_url":"https://creativecommons.org/licenses/by-nc-nd/4.0/legalcode"},"article_processing_charge":"No","status":"public","date_updated":"2026-04-07T12:54:28Z","publication":"bioRxiv","author":[{"orcid":"0000-0003-1971-8314","first_name":"Oluwafunmilola O","id":"41AD96DC-F248-11E8-B48F-1D18A9856A87","full_name":"Olusanya, Oluwafunmilola O","last_name":"Olusanya"},{"first_name":"Kseniia","id":"4E6DC800-AE37-11E9-AC72-31CAE5697425","orcid":"0000-0002-6246-1465","full_name":"Khudiakova, Kseniia","last_name":"Khudiakova"},{"last_name":"Sachdeva","full_name":"Sachdeva, Himani","first_name":"Himani","id":"42377A0A-F248-11E8-B48F-1D18A9856A87"}],"project":[{"_id":"c08d3278-5a5b-11eb-8a69-fdb09b55f4b8","grant_number":"P32896","name":"Causes and consequences of population fragmentation"},{"name":"The impact of deleterious mutations on small populations","_id":"34d33d68-11ca-11ed-8bc3-ec13763c0ca8","grant_number":"26293"},{"_id":"34c872fe-11ca-11ed-8bc3-8534b82131e6","grant_number":"26380","name":"Polygenic Adaptation in a Metapopulation"}],"department":[{"_id":"NiBa"},{"_id":"JaMa"}],"month":"12","doi":"10.1101/2023.12.02.569702","oa":1}]
