Genetic load and extinction in peripheral populations: The roles of migration, drift and demographic stochasticity

We analyse how migration from a large mainland influences genetic load and population numbers on an island, in a scenario where fitness-affecting variants are unconditionally deleterious, and where numbers decline with increasing load. Our analysis shows that migration can have qualitatively different effects, depending on the total mutation target and fitness effects of deleterious variants. In particular, we find that populations exhibit a genetic Allee effect across a wide range of parameter combinations, when variants are partially recessive, cycling between low-load (large-population) and high-load (sink) states. Increased migration reduces load in the sink state (by increasing heterozygosity) but further inflates load in the large-population state (by hindering purging). We identify various critical parameter thresholds at which one or other stable state collapses, and discuss how these thresholds are influenced by the genetic versus demographic effects of migration. Our analysis is based on a ‘semi-deterministic’ analysis, which accounts for genetic drift but neglects demographic stochasticity. We also compare against simulations which account for both demographic stochasticity and drift. Our results clarify the importance of gene flow as a key determinant of extinction risk in peripheral populations, even in the absence of ecological gradients. This article is part of the theme issue ‘Species’ ranges in the face of changing environments (part I)’

ISTA Thesis

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. For 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 as well as in highly fragmented populations. In 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. Chapter 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. In 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. The 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. Chapter 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. Overall 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

The response of a metapopulation to a changing environment

A species distributed across diverse environments may adapt to local conditions. We ask how quickly such a species changes its range in response to changed conditions. Szép et al. (Szép E, Sachdeva H, Barton NH. 2021 Polygenic local adaptation in metapopulations: a stochastic eco-evolutionary model. Evolution75, 1030–1045 (doi:10.1111/evo.14210)) used the infinite island model to find the stationary distribution of allele frequencies and deme sizes. We extend this to find how a metapopulation responds to changes in carrying capacity, selection strength, or migration rate when deme sizes are fixed. We further develop a ‘fixed-state’ approximation. Under this approximation, polymorphism is only possible for a narrow range of habitat proportions when selection is weak compared to drift, but for a much wider range otherwise. When rates of selection or migration relative to drift change in a single deme of the metapopulation, the population takes a time of order m−1 to reach the new equilibrium. However, even with many loci, there can be substantial fluctuations in net adaptation, because at each locus, alleles randomly get lost or fixed. Thus, in a finite metapopulation, variation may gradually be lost by chance, even if it would persist in an infinite metapopulation. When conditions change across the whole metapopulation, there can be rapid change, which is predicted well by the fixed-state approximation. This work helps towards an understanding of how metapopulations extend their range across diverse environments. This article is part of the theme issue ‘Species’ ranges in the face of changing environments (Part II)’

Genetic load, eco-evolutionary feedback and extinction in a metapopulation

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