Selection and the direction of phenotypic evolution

Abstract

Predicting phenotypic evolution on the short-term of tens to hundreds of generations, partic-ularly in changing environments and under finite population sizes, is an important theoretical goal. Because organisms are not simply collections of independent traits, making headway into this goal requires understanding if the phenotypic plasticity of ancestral populations aligns with the phenotypic dimensions that contain more genetic variation for selection to be effective and eventually feedback on the maintenance of genetic variation and promote adaptation or rescue from extinction. By performing 50 generations of experimental evolution in a changing envi-ronment we show that ancestral phenotypic plasticity for locomotion behavior in the partially-outcrossing nematode Caenorhabditis elegans is nonadaptive because it does not align with the phenotypic dimension encompassing most genetic variance in the ancestral population and is of no consequence to future phenotypic divergence. Despite evolution of the genetic structure of locomotion behavior we are able to predict the direction of phenotypic divergence, but not the magnitude, based on the genetic covariances between the component traits of locomotion behavior and fitness of the ancestral population. We further demonstrate that indirect selection on the component traits of locomotion behavior with unobserved trait(s) is responsible for the observed phenotypic divergence on them. Our findings indicate that selection theory can predict the direction of short-term adaptive phenotypic evolution.

Phenotypic stasis with genetic divergence

“…This dimension may represent a continuum between activity and direction of movement in foraging and dwelling, expressed by the positive association between transition rates from the still state (Flavell et al, 2020;Gray et al, 2005). Stabilizing selection favors a negative association between transition rates from the still state, which, elsewhere, we have shown is under directional selection in a new stressful environment (Mallard et al, 2023a). As was the case here, however, transition rates from the still state in the new stressful environment did not evolve under directional selection because of a lack of relevant genetic variation in the appropriate direction.…”

“…All three replicate populations showed similar posterior distributions, however, and no estimate overlaps zero. Another explanation is that we might have overestimated the strength selection or have biased estimates about the form of selection because environmental covariances with unmeasured traits could have caused correlated selection with transition rates (Blows and Brooks, 2003; Hunt et al, 2007; Mallard et al, 2022a). This seems an unlikely explanation.…”

“…A more serious concern is the role of unmeasured traits under potential selection that might be genetically correlated with the observed transition rates (Barton and Turelli, 1987; Lande, 1979; Mallard et al, 2022a; Shaw et al, 1995). Modelling additive genetic similarity among the inbred lines used in the regression (Noble et al, 2017, 2019) does not qualitatively change the inference about selection on transition rates (not shown), though we did not model the genetic architecture of locomotion behavior with multiple traits as the dependent variables.…”

“…Responses to selection in turn will depend on the size and shape of the G-matrix, the additive genetic variance-covariance matrix of multiple traits (Lande, 1979). For example, phenotypic dimensions with more genetic variation are expected to facilitate adaptation, as selection will be more efficient (Lande, 1976(Lande, , 1979Schluter, 1996), even if indirect selection can confound predictions about phenotypic evolution (Mallard et al, 2023a;Morrissey and Bonnet, 2019;Stinchcombe et al, 2014).…”

“…When considering mutation-selection balance on the long-term (as scaled by the effective population sizes), theory has been successfully applied to explain, for example, fly wing evolution over a period of 40 million years (Houle et al, 2017), or nematode embryogenesis over 100 million years (Farhadifar et al, 2015). On the short-term of a few tens to hundreds of generations, however, many natural populations depend on standing genetic variation for adaptation or rescue from extinction, when mutation should be of little influence and founder effects, demographic stochasticity and genetic drift are important (Chelo et al, 2013; Hill, 1982; Mallard et al, 2023a; Matuszewski et al, 2015).…”