An evolutionary process that assembles phenotypes through space rather than time

School of Biological Sciences A08, University of Sydney, Sydney, NSW 2006, Australia.
Proceedings of the National Academy of Sciences (Impact Factor: 9.67). 03/2011; 108(14):5708-11. DOI: 10.1073/pnas.1018989108
Source: PubMed


In classical evolutionary theory, traits evolve because they facilitate organismal survival and/or reproduction. We discuss a different type of evolutionary mechanism that relies upon differential dispersal. Traits that enhance rates of dispersal inevitably accumulate at expanding range edges, and assortative mating between fast-dispersing individuals at the invasion front results in an evolutionary increase in dispersal rates in successive generations. This cumulative process (which we dub "spatial sorting") generates novel phenotypes that are adept at rapid dispersal, irrespective of how the underlying genes affect an organism's survival or its reproductive success. Although the concept is not original with us, its revolutionary implications for evolutionary theory have been overlooked. A range of biological phenomena (e.g., acceleration of invasion fronts, insular flightlessness, preadaptation) may have evolved via spatial sorting as well as (or rather than) by natural selection, and this evolutionary mechanism warrants further study.

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    • "Countergradient variation, whereby genetic influences buffer environmental influences (Conover et al. 2009), may thereby generate similar trait changes as the expansion process. For example, flight ability may both increase in response to selection driven by the process of range expansion (Travis & Dytham 2002; Shine et al. 2011) as well as by antagonistic selection to counter potential reduction in flight ability at the suboptimal thermal regimes at higher latitudes (Therry et al. 2014c). "
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    ABSTRACT: Many species are expanding their range polewards and this has been associated with rapid phenotypic change. Yet, it is unclear to what extent this reflects rapid genetic adaptation or neutral processes associated with range expansion, or selection linked to the new thermal conditions encountered. To disentangle these alternatives, we studied the genomic signature of range expansion in the damselfly Coenagrion scitulum using 4950 newly developed genomic SNPs and linked this to the rapidly evolved phenotypic differences between core and (newly established) edge populations. Most edge populations were genetically clearly differentiated from the core populations and all were differentiated from each other indicating independent range expansion events. In addition, evidence for genetic drift in the edge populations, and strong evidence for adaptive genetic variation in association with the range expansion was detected. We identified one SNP under consistent selection in four of the five edge populations and showed that the allele increasing in frequency is associated with increased flight performance. This indicates collateral, non-neutral evolutionary changes in independent edge populations driven by the range expansion process. We also detected a genomic signature of adaptation to the newly encountered thermal regimes, reflecting a pattern of countergradient variation. The latter signature was identified at a single SNP as well as in a set of covarying SNPs using a polygenic multilocus approach to detect selection. Overall, this study highlights how a strategic geographic sampling design and the integration of genomic, phenotypic and environmental data can identify and disentangle the neutral and adaptive processes that are simultaneously operating during range expansions. This article is protected by copyright. All rights reserved.
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    • "dispersal, resulting in a population composed of a subsample of the phenotypes in the source habitats (Duckworth and Badyaev 2007; Clobert et al. 2009; Fogarty et al. 2011; Shine et al. 2011). For instance, newly established isolated populations of the Glanville fritillary butterfly (Melitaea cinxia) showed higher frequency of an allele related to a high flight metabolic rate (Haag et al. 2005). "
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    ABSTRACT: Spatial heterogeneity in the distribution of phenotypes among populations is of major importance for species evolution and ecosystem functioning. Dispersal has long been assumed to homogenise populations in structured landscapes by generating mal-adapted gene flows, making spatial heterogeneity of phenotypes traditionally considered resulting from local adaptation or plasticity. However, there is accumulating evidence that individuals, instead of dispersing randomly in the landscapes, adjust their dispersal decisions according to their phenotype and the environmental conditions. Specifically, individuals might move in the landscape to find and settle in the environmental conditions that best match their phenotype, therefore maximizing their fitness, a hypothesis named habitat matching. Although habitat matching and associated non-random gene flows can produce spatial phenotypic heterogeneity, their potential consequences for metapopulation and metacommunity functioning are still poorly understood. Here, we discuss evidence for intra and interspecific drivers of habitat matching, and highlight the potential consequences of this process for metapopulation and metacommunity functioning. We conclude that habitat matching might deeply affect the eco-evolutionary dynamics of meta-systems, pointing out the need for further empirical and theoretical research on its incidence and implications for species and communities evolution under environmental changes.
    Full-text · Article · Nov 2015 · Evolutionary Ecology
    • "Since competitive ability may increase the probability of resource acquisition (Harper 1982; Just and Morris 2003; Gherardi and Cioni 2004) and enhance success in coping with novel predators and competitors (Duckworth 2008; Pintor et al. 2008; Hudina and Hock 2012), it is intuitive to consider that elevated aggression will benefit the individuals entering the novel environment (Duckworth and Badyaev 2007; Duckworth 2008; Cote et al. 2010). Several studies suggested that aggression in combination with traits, such as boldness or activity may be conducive to better dispersal ability, priming individuals exhibiting such traits to drive the range expansion and, consequently , increasing their presence at the invasion front (Clobert et al. 2009; Cote et al. 2010; Shine et al. 2011). Aggression is also closely related to other ecological contexts such as population density and resource availability, both of which affect the intensity of resource competition with conspecifics (Grafen 1987; Enquist and Leimar 1987; Dugatkin and Ohlsen 1990; Morrell et al. 2005). "

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