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Population Genetics and Demography Unite Ecology and Evolution

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Population Genetics and Demography Unite Ecology and Evolution Review Population Genetics and Demography Unite Ecology and Evolution 1, 2 1 Winsor H. Lowe, * Ryan P. Kovach, and Fred W. Allendorf The interplay of ecology and evolution has been a rich area of research for Trends decades. A surge of interest in this area was catalyzed by the observation that Eco–evo interactions are mediated by evolution by natural selection can operate at the same contemporary timescales population genetics and demography, but current research often fails to con- as ecological dynamics. Specifically, recent eco-evolutionary research focuses sider this population context. on how rapid adaptation influences ecology, and vice versa. Evolution by non- adaptive forces also occurs quickly, with ecological consequences, but under- Population genetics theory provides a framework for understanding the full standing the full scope of ecology–evolution (eco–evo) interactions requires scope of eco–evo interactions, includ- explicitly addressing population-level processes – genetic and demographic. ing the effects of adaptive and non- We show the strong ecological effects of non-adaptive evolutionary forces and, adaptive forces. more broadly, the value of population-level research for gaining a mechanistic Our review shows the ecological understanding of eco–evo interactions. The breadth of eco-evolutionary effects of non-adaptive evolution and research should expand to incorporate the breadth of evolution itself. the mechanistic insight gained in popu- lation-level research on eco–evo interactions. The Scope of Ecological-Evolutionary Interactions fl Ecological and evolutionary processes in uence all levels of biological organization, but ecology Population-based approaches integrat- ing genetic and demographic informa- and evolution are inseparable at the population level. Survival, recruitment, abundance, density, tion will advance general understanding and exchange of individuals among populations are all determined by the interaction of of the scope, strength, and scale of ecological and evolutionary processes [1,2]. In turn, these demographic parameters determine eco–evo interactions. whether and how variation in individual fitness is converted into higher-order ecological and evolutionary effects, setting the rate and scale of future eco–evo interactions [3–5]. Population genetics theory provides a framework for understanding the interdependence of ecological and evolutionary processes by accounting for effects of demography on phenotype and gene frequencies (Figure 1). Natural selection acts at the level of the individual, but both adaptive and non-adaptive evolutionary forces acting at the population level determine whether, how, and at what spatial scale phenotypic change and resulting ecological consequences occur [6,7]. Likewise, ecological dynamics acting at higher levels of organization (e.g., species inter- actions in communities) must affect population processes to drive adaptive and non-adaptive evolution [8,9] through changes in selection, genetic drift (see Glossary), or gene flow. 1 Division of Biological Sciences, In the past decade, ecologists have embraced the concept of eco-evolutionary dynamics, University of Montana, Missoula, MT which emphasizes the power of ecological selection to cause rapid adaptation and, likewise, for 59812, USA 2 US Geological Survey, Northern adaptive evolution to influence ecological processes in real time [10,11]. The perceived novelty Rocky Mountain Science Center, of this concept appears to stem from the fast rate of interaction between ecological conditions Glacier National Park, West Glacier, and phenotypic adaptation, which contrasts with traditional, gradualistic models of adaptation. MT 59936, USA Aspects of the eco-evolutionary dynamics concept are challenging, including the difficulty of characterizing the rate of eco–evo interaction in a way that is not biased by human perception, *Correspondence: and the fact that all adaptive (or non-adaptive) evolution can be linked to ecological causes and [email protected] – consequences. However, there is also no doubt that exciting examples of observable eco evo (W.H. Lowe). Trends in Ecology & Evolution, February 2017, Vol. 32, No. 2 http://dx.doi.org/10.1016/j.tree.2016.12.002 141 © 2016 Elsevier Ltd. All rights reserved. interactions have come to light recently [12–14], adding to a foundation of classic examples Glossary [15–18]. Compensatory mortality: when one source of mortality largely replaces another source of mortality, resulting We are mainly concerned that a narrow focus on adaptation in eco-evolutionary studies in little or no change in population obscures equally strong and rapid ecological effects of non-adaptive evolutionary forces dynamics. (Figure 1). To understand the ecological causes and consequences of the full scope of Density dependence: when fi evolutionary forces, eco-evolutionary research could benefit from explicit integration of popula- population growth or speci c demographic rates (e.g., mortality, tion processes – genetic and demographic. Greater integration of population-level processes will fecundity) are regulated by the not only elucidate the ecological effects of non-adaptive evolution but also provide novel insight density of the population. on how these non-adaptive forces promote (or prevent) rapid phenotypic adaptation. Dispersal: permanent movement away from an origin and long-term settlement at a new location. Our goal is to show the importance of considering the full scope of evolutionary processes – Disruptive selection: natural adaptive and non-adaptive – to advance mechanistic understanding of eco–evo interactions. selection that favors extreme values fi We rst review the treatment of population genetic principles in evolutionary biology and ecology, of a trait over intermediate values, also known as diversifying selection. and the history of the view that population-level processes conflict with adaptive evolution – a Eco-evolutionary dynamics: misperception that still influences eco-evolutionary research both implicitly and explicitly. To interplay between ecological and move beyond this view, we then review studies showing how demographic parameters mediate evolutionary dynamics in real time (i. eco–evo interactions via adaptive and non-adaptive mechanisms. Finally, we identify emerging e., relatively instantaneously). Effective population size (Ne): the opportunities for population-level research on the interplay of ecology and evolution. size of an ideal population that would experience the same amount of Wrestling with the Population Context of Ecological-Evolutionary Interactions genetic drift as the observed Population genetics theory provides a mechanistic framework for integrating ecological and population. Fixation index (FST): a measure of evolutionary processes by explicitly incorporating population parameters that are, themselves, population subdivision that indicates shaped by ecological interactions (Box 1). More generally, population genetics theory illuminates the proportion of heterozygosity the full suite of forces that promote or prevent evolutionary change, and the genetic and found between populations relative to demographic mechanisms that govern these forces. By contrast, the recent surge of eco- the amount within populations. Gene flow: movement of genes from evolutionary research hinges on the rate of adaptive phenotypic change, thus emphasizing one population to another. In directional selection at the cost of other evolutionary processes and their demographic bases. population genetics theory, gene flow ‘ ’ While often described as contemporary evolution , this area of research might be better is represented by migration rate (m) – described as ‘contemporary adaptation’ [19]. the proportion of individuals in a focal population that are immigrants. Genetic drift: change in gene The rift between longstanding population genetics theory and current eco-evolutionary research frequencies over time owing to underscores the challenge of fully addressing the forces that drive evolution at the population random differences in the survival and fecundity of individuals, as well level. This challenge is not new ([20], p. 64), and is embodied in a historical debate over the power as to binomial sampling of alleles of selection to drive evolutionary change in the face of other, non-adaptive forces – a debate that during meiosis. is largely settled in the field of evolutionary biology, but the root of a narrow view of evolution in Genetic rescue: increase in many current eco-evolutionary studies. population growth of small populations following immigration, resulting from the reduction of By treating genes as independent units, population genetics was criticized by some evolutionary genetic load caused by inbreeding biologists as overly simplistic and devoid of the functional interrelationships among genes that depression. are crucial to selection (reviewed in [21]). Mayr [22] questioned whether this ‘mathematical’ Hard selection: natural selection that removes from the population school contributed anything to evolutionary theory, characterizing gene pool models as ‘bean- individuals whose phenotype does bag genetics’ because they merely track the frequency and distribution of individual genes, not attain a particular threshold, fl ignoring the functional integration of these genes. This criticism re ects a broader debate on the independently of population density relative power of selection to drive evolutionary change. or genotype/phenotype frequency. Hard
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