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The Genetic Allee Effect: a Unified Framework for the Genetics and Demography of Small Populations Gloria M

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The Genetic Allee Effect: a Unified Framework for the Genetics and Demography of Small Populations Gloria M The genetic Allee effect: a unified framework for the genetics and demography of small populations Gloria M. Luque, Chloé Vayssade, Benoit Facon, Thomas Guillemaud, Franck Courchamp, Xavier Fauvergue To cite this version: Gloria M. Luque, Chloé Vayssade, Benoit Facon, Thomas Guillemaud, Franck Courchamp, et al.. The genetic Allee effect: a unified framework for the genetics and demography of small populations. Ecosphere, Ecological Society of America, 2016, 7 (7), pp.e01413. 10.1002/ecs2.1413. hal-01594603 HAL Id: hal-01594603 https://hal.archives-ouvertes.fr/hal-01594603 Submitted on 28 May 2021 HAL is a multi-disciplinary open access L’archive ouverte pluridisciplinaire HAL, est archive for the deposit and dissemination of sci- destinée au dépôt et à la diffusion de documents entific research documents, whether they are pub- scientifiques de niveau recherche, publiés ou non, lished or not. The documents may come from émanant des établissements d’enseignement et de teaching and research institutions in France or recherche français ou étrangers, des laboratoires abroad, or from public or private research centers. publics ou privés. Distributed under a Creative Commons Attribution| 4.0 International License SYNTHESIS & INTEGRATION The genetic Allee effect: a unified framework for the genetics and demography of small populations Gloria M. Luque,1 Chloé Vayssade,2 Benoît Facon,3 Thomas Guillemaud,2 Franck Courchamp,1,4 and Xavier Fauvergue2,† 1Ecologie Systématique Evolution, Univ. Paris-Sud, CNRS, AgroParisTech, Université Paris-Saclay, 91400, Orsay, France 2ISA, UMR INRA CNRS, Universite Nicé Côte d’Azur, 06903 Sophia-Antipolis, France 3CBGP, UMR INRA, CIRAD, IRD, SupAgro, 34988, Montferrier sur Lez, France 4Department of Ecology and Evolutionary Biology, Center for Tropical Research, Institute of the Environment and Sustainability, University of California Los Angeles, Los Angeles, California 90095 USA Citation: Luque, G. M., C. Vayssade, B. Facon, T. Guillemaud, F. Courchamp, and X. Fauvergue. 2016. The genetic Allee effect: a unified framework for the genetics and demography of small populations. Ecosphere 7(7):e01413. 10.1002/ ecs2.1413 Abstract. The Allee effect is a theoretical model predicting low growth rates and the possible extinction of small populations. Historically, studies of the Allee effect have focused on demography. As a result, underlying processes other than the direct effect of population density on fitness components are not generally taken into account. There has been heated debate about the potential of genetic processes to drive small populations to extinction, but recent studies have shown that such processes clearly impact small populations over short time scales, and some may generate Allee effects. However, as opposed to the ecological Allee effect, which is underpinned by cooperative interactions between individuals, genetically driven Allee effects require a change in genetic structure to link the decline in population size with a de- crease in fitness components. We therefore define the genetic Allee effect as a two-step process whereby a decrease in population size leads to a change in population genetic structure and, in turn, to a decrease in individual fitness. We describe potential underlying mechanisms and review the evidence for this original type of component Allee effect, using published examples from both plants and animals. The possibility of considering demogenetic feedback in light of genetic Allee effects clarifies the analysis and interpretation of demographic and genetic processes, and the interplay between them, in small populations. Key words: Allee effect; drift load; eco-evolutionary feedback; extinction vortex; inbreeding depression; migration load; small populations. Received 3 May 2016; accepted 11 May 2016. Corresponding Editor: D. P. C. Peters. Copyright: © 2016 Luque et al. This is an open access article under the terms of the Creative Commons Attribution License, which permits use, distribution and reproduction in any medium, provided the original work is properly cited. † E-mail: [email protected] INTRODUCTION et al. 2004, Taylor and Hastings 2005, Johnson et al. 2006). This concept, first introduced by the The Allee effect can be defined as a decrease in American ecologist Warder Clyde Allee in the fitness caused by a decrease in population size 1930s, has been the focus of growing interest from (Stephens et al. 1999). The Allee effect jeopardizes population ecologists over the last two decades. the persistence of small populations, whether In 1999, Stephens et al. formalized the defini- declining or bottlenecked (threatened species; tion of Allee effects, making a crucial distinction Angulo et al. 2007, Bonsall et al. 2014, Kuparinen between component and demographic Allee et al. 2014; introduced/invasive species; Davis effects. A component Allee effect is a decrease v www.esajournals.org 1 July 2016 v Volume 7(7) v Article e01413 SynTHESIS & InTEGration LuquE et al. in the value of any component of individual fit- modeling inbreeding depression; e.g., Glémin ness caused by a decrease in population size. 2003) and dynamicists usually view genetic pro- A demographic Allee effect is the consequent cesses as affecting populations only in the long decrease in the per capita growth rate of the pop- term. This would make them likely to think that ulation caused by a decrease in population size small populations do not generally stay small for and resulting from one or several component long enough (because they grow or disappear Allee effects. Allee effects have been discovered due to demographic processes) to suffer from in a wide range of taxa, with various mechanisms genetic Allee effects. There may have been too underpinned by a shortage of cooperative inter- little dialog between the two disciplines as yet actions at low density (Courchamp et al. 1999, (Kokko and Lopez- Sepulcre 2007, Metcalf and 2008). Pavard 2007, Pelletier et al. 2009) for the genetic Population dynamicists working on the Allee Allee effect to have emerged as a robust unifying effect may have overlooked the fact that genetic paradigm. processes can also impact populations at an The aim of this work was to propose the genetic ecological time scale of only a few generations Allee effect as a heuristic framework for studying (Glémin 2003, Spielman et al. 2004). This is par- the interplay between genetics and demography ticularly relevant when genetic processes are in small populations. We first propose a formal combined with demographic processes, such definition for the genetic Allee effect and describe as demographic and environmental stochas- the processes potentially underlying this effect. ticity (Tanaka 2000, Hanski and Saccheri 2006). We review the evidence for genetic Allee effects, Some of these genetic mechanisms can gener- including population genetic studies, which, ate component Allee effects (Courchamp et al. although not referring to the Allee effect, pro- 1999) because they yield a positive relationship vide numerous examples of genetic Allee effects. between population size and fitness (Fischer Based on these examples, we then propose meth- et al. 2000, Willi et al. 2005, Berec et al. 2007). ods for detecting genetic Allee effects and distin- These mechanisms are inbreeding depression guishing them from ecological Allee effects. In (Frankham 1995, Spielman et al. 2004), loss of the last section of the study, we discuss the spec- genetic variation (Gomulkiewicz and Holt 1995, ificity, limits, and demographic consequences of Amos and Balmford 2001), and the accumula- genetic Allee effects. tion of deleterious mutations (Lande 1994, Lynch et al. 1995b). DEFINITION Contrasting with the pervasive evidence that genetic mechanisms affect the dynamics of small one fundamental principle of evolutionary populations, even in the short term, fewer than biology is that a population is a collection of dif- ten publications have made specific reference to ferent genotypes vehicled by a number of differ- a genetic Allee effect. There are two possible rea- ent individuals. Changes in genotype frequencies sons for the lack of studies considering genetic correspond to changes in the number, frequency, Allee effects. First, although mentioned in a hand- and association of different alleles within and ful of studies, the genetic Allee effect has never between loci. These genotype frequencies are been formally defined, so the concept may still referred to hereafter as the (within- population) be too vague to stimulate new studies. Second, genetic structure. Changes in genetic structure the genetic mechanisms occurring in small pop- yield changes in the fitness components that ulations are the classic territory of population these genotypes influence (Soulé 1980). This rela- genetics, whereas the Allee effect is a concept tionship underlies the genetic Allee effect because derived principally from population dynamics. population size is one of the determinants of These two communities view populations differ- genetic structure (nielsen and Slatkin 2013). ently and usually work on different entities (e.g., Here (following the evolutionary paradigm individual numbers vs. genotype frequencies), described by Waples and Gaggiotti 2006), the concepts and time scales. Most studies in popu- term “population” refers to a “a group of indi- lation genetics assume populations of constant viduals of the same species living in close enough size, unaffected by individual fitness (even when proximity
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