Repeated evolution and the impact of evolutionary history on adaptation

Abstract

BackgroundWhether natural selection can erase the imprint of past evolutionary history from phenotypes has been a topic of much debate. A key source of evidence that present-day selection can override historically contingent effects comes from the repeated evolution of similar adaptations in different taxa. Yet classic examples of repeated evolution are often among closely related taxa, suggesting the likelihood that similar adaptations evolve is contingent on the length of time separating taxa. To resolve this, we performed a meta-analysis of published reports of repeated evolution.ResultsOverall, repeated evolution was far more likely to be documented among closely related than distantly related taxa. However, not all forms of adaptation seemed to exhibit the same pattern. The evolution of similar behavior and physiology seemed frequent in distantly related and closely related taxa, while the repeated evolution of morphology was heavily skewed towards closely related taxa. Functionally redundant characteristics—alternative phenotypes that achieve the same functional outcome—also appeared less contingent.ConclusionsIf the literature provides a reasonable reflection of the incidence of repeated evolution in nature, our findings suggest that natural selection can overcome contingent effects to an extent, but it depends heavily on the aspect of the phenotype targeted by selection.Electronic supplementary materialThe online version of this article (doi:10.1186/s12862-015-0424-z) contains supplementary material, which is available to authorized users.

The Repeated Evolution of Behavior

“…Furthermore, more than 80% (40/49) of cases occur at sub-family taxonomic units (species/genus/subfamily/family). Previous observations of repeated evolutionary events across other traits including morphology, physiology, and life history shows a similar trend, indicating that behaviors are not subject to evolutionary processes distinct from these other phenotypes (Vermeij, 2006;Ord and Summers, 2015). In addition we find a significant positive correlation between clade size and conversion number (r 2 = 0.46; p = 0.001) but not between evolutionary divergence time and conversion (r 2 = 0.11; p = 0.46).…”

“…This owes largely to the fact that the original definitions predated the advent of modern molecular methods (Losos, 2011;summarized in Table 1). Recently authors have suggested replacing the terms with others, including repeated evolution (Gompel and Prud'homme, 2009;Ord and Summers, 2015), homoplasy (Wake et al, 2011), and phylogenetic replication (Kopp, 2009). Arendt and Reznick (2008), on the other hand, collapse the distinctions altogether under one banner-convergent evolution-arguing that the convergent vs. parallel split represents a false dichotomy.…”

Evolutionary assembly patterns of prokaryotic genomes

“…Importantly, our model that gene acquisition is affected by recipient genome content is consistent with the observed enrichment of HGT among close relatives, which presumably have similar genome content (Gogarten et al 2002;Andam and Gogarten 2011;). This taxonomic clustering of innovation by HGT is also in agreement with previous studies that demonstrated that phenotypic and genetic parallel evolution is more common than convergent evolution, potentially due to the effects of historical contingency (Gould and Lewontin 1979;Conte et al 2012;Christin et al 2015;Ord and Summers 2015). However, in contrast to other studies, we present direct evidence that the mechanism by which contingency controls evolution is epistasis.…”

“…This predictability is consistent with the hypothesis that genegene dependencies constrain the evolution of genomes by HGT. More broadly, this analysis and our finding that PGCEs can predictably determine future evolutionary gains provide substantial evidence that the preponderance of parallel evolution over convergent evolution (Conte et al 2012;Ord and Summers 2015) may be the result of specific, identifiable genetic dependencies entraining the evolutionary trajectory taken by similar genomes. 8.04…”

“…Studies of specific proteins, for example, indicate that epistasis between sequence residues limits accessible evolutionary trajectories and thereby renders certain adaptive paths more likely than others (Weinreich et al 2006;Gong et al 2013;de Visser and Krug 2014;Harms and Thornton 2014). Similarly, both phenotypic characters (Ord and Summers 2015) and specific genetic adaptations (Conte et al 2012;Christin et al 2015) show strong evidence of parallel evolution rather than convergent evolution. That is, a given adaptation is more likely to repeat in closely related organisms than in distantly related ones.…”