Abstract
Phenotypic plasticity can either hinder or promote adaptation to novel environments. Recent studies that have quantified alignments between plasticity, genetic variation, and divergence propose that such alignments may reflect constraints that bias future evolutionary trajectories. Here, we emphasize that such alignments may themselves be a result of natural selection and do not necessarily indicate constraints on adaptation. We estimated developmental plasticity and broad sense genetic covariance matrices (G) among damselfly populations situated along a latitudinal gradient in Europe. Damselflies were reared at photoperiod treatments that simulated the seasonal time constraints experienced at northern (strong constraints) and southern (relaxed constraints) latitudes. This allowed us to partition the effects of (1) latitude, (2) photoperiod, and (3) environmental novelty on G and its putative alignment with adaptive plasticity and divergence. Environmental novelty and latitude did not affect G, but photoperiod did. Photoperiod increased evolvability in the direction of observed adaptive divergence and developmental plasticity when G was assessed under strong seasonal time constraints at northern (relative to southern) photoperiod. Because selection and adaptation under time constraints is well understood in Lestes damselflies, our results suggest that natural selection can shape the alignment between divergence, plasticity, and evolvability.
Highlights
Because phenotypic plasticity can rapidly generate phenotypes that are better matched to novel environmental settings, plasticity can allow organisms to survive the initial stages of change, leaving an opportunity for subsequent genetic adaptation through natural selection (Waddington 1953; West-Eberhard 2003; Lande 2009; Levis and Pfennig 2016)
It is possible that an alignment between developmental plasticity, genetic variation, and divergence could be created over relatively short time scales by contemporary natural selection shaping all three levels of biological variation simultaneously (Cheverud 1984; Schluter 1996; Houle et al 2017; Noble et al 2019; Svensson and Berger 2019)
Determining the extent to which such alignments are a consequence of genetic/developmental constraints or the adaptive outcomes of contemporary natural selection is important for predicting evolutionary potential: the former alternative implies a limited capacity for adaptation to novel selection pressures, in contrast to the latter alternative that implies potential for rapid adaptive responses
Summary
Whether phenotypic plasticity hinders or facilitates adaptation in new environments has been debated, and recently interest in this issue has intensified due to the increasing need to understand species’ responses to global environmental change (Whitlock 1996; Price et al 2003; West-Eberhard 2003; Ghalambor et al 2007; Lande 2009; Chevin et al 2010; Walters et al 2012; Levis and Pfennig 2016; Uller et al 2018; Levis and Pfennig 2019; Noble et al 2019). A recent meta-analysis by Noble et al (2019) found that phenotypic plasticity was aligned with the amount of genetic (co)variance within and between traits, but whether genetic variation was quantified in the ancestral or a novel environment had no overall effect on the alignment or the total amount of expressed variation These results were discussed with regard to the “plasticity first hypothesis,” stating that plasticity takes the lead in adaptive evolution (Levis and Pfennig 2016; Radersma et al 2020). In addition to information on plasticity and genetic (co)variation in the studied traits, knowledge of trait divergence and multivariate phenotypic selection is necessary (Levis and Pfennig 2016; Noble et al 2019)
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