Phenotypic evolution of dispersal-enhancing traits in insular voles

Abstract

Evolutionary theory predicts that in metapopulations subject to rapid extinction-recolonization dynamics, natural selection should favour evolution of traits that enhance dispersal and recolonization ability. Metapopulations of field voles (Microtus agrestis) on islands in the Stockholm archipelago, Sweden, are characterized by frequent local extinction and recolonization of subpopulations. Here, we show that voles on the islands were larger and had longer feet than expected for their body size, compared with voles from the mainland; that body size and size-specific foot length increased with increasing geographical isolation and distance from mainland; and that the differences in body size and size-specific foot length were genetically based. These findings provide rare evidence for relatively recent (less than 1000 years) and rapid (corresponding to 100-250 darwins) evolution of traits facilitating dispersal and recolonization in island metapopulations. 1. INTRODUCTION Studies of island populations have played an important role in generating and testing hypotheses central to the ecology and evolution of biological diversity, both historically [1,2] and currently [3-5]. Evolutionary theory predicts that in metapopulations subject to rapid extinction -recolonization dynamics, natural selection should favour evolution of traits enhancing dispersal and recoloni-zation ability [6-8]. However, empirical evidence is relatively scarce. Populations of field voles, Microtus agrestis, on groups of islands in the Stockholm archipelago provide a good model system to test this prediction. These islands emerged from the sea approximately 500-1000 years ago [9] as a result of land elevation following the termination of the latest glaciations, and were colonized by field voles from the mainland [10]. These insular populations are characterized by drastic fluctuations in numbers of individuals and high turnover rates; extinctions and recolonizations from neighbouring islands are frequent [11-13]. There is evidence to suggest increased rates of emigration/dispersal before subpopulation extinctions [11,13], as well as evidence for life-history adaptations in insular environments. Laboratory breeding over several generations show that insular voles produce larger (5.27 versus 4.13) and heavier (17.06 versus 11.02 g) litters; bear larger young, which grow faster; and make a larger reproductive effort compared with mainland voles [10]. However, there is as yet no evidence that selection has favoured the evolution of traits that enhance dispersal and recolonization ability in these insular vole populations. Morphological traits linked to locomotion and

An evolutionary process that assembles phenotypes through space rather than through time

“…For example, imagine a species that expands its range by dispersing from the mainland to numerous islands and exhibits strong phenotypic similarities between organisms on different islands even though they were founded by separate dispersal events from the mainland. The Darwinian view would attribute that similarity to convergent adaptation to island conditions, but spatial sorting could generate the same pattern (5,12,43,44). That is, individuals from island populations resemble each other not because they have experienced similar selective forces in their insular homes but because of similar winnowing for dispersal-enhancing phenotypes in the process of reaching those islands.…”

The straight and narrow path: the evolution of straight-line dispersal at a cane toad invasion front

“…For most biological invasions, the only evidence available to test predictions of increased dispersal involves an overall acceleration in rate of range expansion through time [13] or morphological traits at the invasion front that correlate with rapid dispersal, such as wings, or enlarged flight muscles or legs [14][15][16][17]. For a few systems, however, we also have more detailed information on individual behaviour.…”

Selecting for invasive tendencies: the evolution of morphological, physiological, and movement behaviour traits associated with dispersal

“…Relative locomotor apparatus size is also strongly associated with dispersal. For example, in comparison to residents, dispersive cane toads (Rhinella marina) had longer legs relative to their body size (Phillips et al 2006) and dispersive field voles (Microtus agrestis) had relatively longer feet (Forsman et al 2010) than their respective resident conspecifics.…”

“…Dispersal syndromes are frequently discussed in conjunction with large body size and large locomotor apparatus relative to body size (Phillips et al 2006;Forsman et al 2010;Laparie et al 2013). Assuming that the measures of movement ability and displacement could be reasonable proximate measures for dispersal (Hawkes 2009;Ducatez et al 2012), then these measures should correlate well with body size and relative locomotor apparatus size.…”

“…Evidence for the evolution of dispersal ability and dispersalassociated traits at range edges has been demonstrated across diverse taxa (Chuang & Peterson 2016). Broadly, traits that may characterise dispersive individuals are a larger body size (Hill et al 1999;Gutowsky & Fox 2012;Kelehear et al 2012;Brown et al 2013;Laparie et al 2013), larger locomotor appendages relative to body size (Phillips et al 2006;Forsman et al 2010;Therry et al 2014b), a better body condition (Carol et al 2009;Lopez et al 2012;Rebrina et al 2015), boldness, aggressiveness, or low sociality (Fraser et al 2001;Duckworth 2006;Myles-Gonzalez et al 2015) compared with residents. Individuals that disperse have also been found to grow or mature faster (Bøhn et al 2004;Carol et al 2009;Phillips 2009), and exhibit a generally higher metabolic rate (MR) at rest (MylesGonzalez et al 2015) and during locomotion (Haag et al 2005;Niitepõld et al 2009).…”