A Reassessment of Genetic Limits to Evolutionary Change

Abstract

An absence of genetic variance in traits under selection is perhaps the oldest explanation for a limit to evolutionary change, but has also been the most easily dismissed. We review a range of theoretical and empirical results covering single traits to more complex multivariate systems, and show that an absence of genetic variance may be more common than is currently appreciated. From a single-trait perspective, we highlight that it is becoming clear that some trait types do not display significant levels of genetic variation, and we raise the possibility that species with restricted ranges may differ qualitatively from more widespread species in levels of genetic variance in ecologically important traits. A common misconception in many life-history studies is that a lack of genetic variance in single traits, and genetic constraints as a consequence of bivariate genetic correlations, are different causes of selection limits. We detail how interpretations of bivariate patterns are unlikely to demonstrate genetic limits to selection in many cases. We advocate a multivariate definition of genetic constraints that emphasizes the presence (or otherwise) of genetic variance in the multivariate direction of selection. For multitrait systems, recent results using longer term studies of organisms, in which more is understood concerning what traits may be under selection, have indicated that selection may exhaust genetic variance, resulting in a limit to the selection response.

Limited potential for adaptation to climate change in a broadly distributed marine crustacean

“…A geographical range limit is an evolutionary limit in the sense that it represents a failure to adapt to the conditions beyond the range boundary. Hypotheses for why a species should fail to adapt to conditions beyond its range boundary fall into two classes: (i) antagonistic gene flow from more central populations [44] and (ii) limited variation at the edge, either owing to genetic drift or fundamental limits in the traits themselves [31,45,46]. If adaptation in edge populations is limited by antagonistic gene flow, then populations at the edge of a species range should contain variation for environmental tolerance (and hence the capacity to evolve increased tolerance during periods of environmental change).…”

Comparing G: multivariate analysis of genetic variation in multiple populations

“…Although individual traits feature as the rows and columns of G, it is important to realise that these individual measured traits do not necessarily have a greater role in the response to selection than any combination of the traits. Recognising G as simply characterising the level of genetic variance in all possible trait combinations (Blows and Hoffmann, 2005) provides a point of departure for the framework we outline in this paper for establishing how G differs among populations, and the evolutionary consequences of those differences.…”

An assessment of the reliability of quantitative genetics estimates in study systems with high rate of extra-pair reproduction and low recruitment

“…However, as most traits are likely under the control of numerous genes with small effects (Lande, 1981;Falconer and Mackay, 1996;Husby et al, 2015), potentially interacting with the genetic components of other traits (Lande and Arnold, 1983;Blows and Hoffmann, 2005) and/or with the environment in which they are expressed (Via and Lande, 1985;Hoffmann and Merilä, 1999), this task remains challenging despite rapid advances in whole-genome analysis methods (Vinkhuyzen et al, 2013). For these reasons, quantitative genetic approaches-statistical methods using known relationships between individuals to assess the genetic and environmental components of a population phenotypic variance-remain efficient ways to infer the underlying genetic variation of focal traits (Falconer and Mackay, 1996;Kruuk et al, 2008).…”