Social Selection and the Evolution of Maladaptation

Abstract

Evolution by natural selection is often viewed as a process that inevitably leads to adaptation, or an increase in population fitness over time. However, maladaptation, an evolved decrease in fitness, may also occur in response to natural selection under some conditions. Social effects on fitness (or social selection) have been identified as a potential cause of maladaptation, but we lack a general rule identifying when social selection should lead to a decrease in population mean fitness. Here we use a quantitative genetic model to develop such a rule. We show that maladaptation is most likely to occur when social selection is strong relative to the nonsocial component of selection and acts in an opposing direction. In this scenario, evolutionary increases in traits that impose fitness costs on others may outweigh evolved gains in fitness for the individual, leading to a net decrease in population mean fitness. Further, we find maladaptation may also sometimes occur when phenotypes of interacting individuals negatively covary. We outline the biological situations where maladaptation in response to social selection can be expected, provide both quantitative genetic and phenotypic versions of our derived result, and suggest what empirical work would be needed to test it. We also consider the effect of social selection on inclusive fitness and support previous work showing that inclusive fitness cannot suffer an evolutionary decrease. Taken together, our results show that social selection may decrease population mean fitness when it opposes individual-level selection, even as inclusive fitness increases.

The Indirect Genetic Effect Interaction Coefficientψ: Theoretically Essential and Empirically Neglected

“…In the time since Moore et al (1997) first described the interaction coefficient in IGE models, ψ has been persistently emphasized in IGE theory as a fundamental, measurable parameter that describes evolutionary effects of IGEs. Such traitbased models range from the original theoretical work describing evolutionary effects of IGEs (Moore et al 1997;Wolf et al 1998;Wolf et al 1999), to metapopulation models (Agrawal et al 2001), sexual conflict models (Moore and Pizzari 2005), sexual selection models (Bailey and Moore 2012), social selection models (Wolf et al 1999;McGlothlin et al 2010;Bailey and Kölliker 2019;Bailey et al 2021), game theory models , models of maladaptation (McGlothlin and Fisher 2021), and models examining the evolution of ψ itself (Kazancıoğlu et al 2012). In each case, evolutionary predictions about the effects of IGEs are either explicitly articulated using the interaction coefficient ψ (or matrix Ψ), or implicitly dependent on ψ.…”

Social selection is density dependent but makes little contribution to total selection in New Zealand giraffe weevils

“…Social selection may not align with direct selection (Table 3 of [9]), which can alter the direction and tempo of trait evolution [8], possibly leading to maladaptation [10]. For instance, 'selfish' traits may increase the fitness of an individual that bears them but may be costly when displayed by those they interact with.…”