Adaptive radiation along a deeply conserved genetic line of least resistance inAnolislizards

Abstract

On microevolutionary timescales, adaptive evolution depends upon both natural selection and the underlying genetic architecture of traits under selection, which may constrain evolutionary outcomes. Whether such genetic constraints shape phenotypic diversity over macroevolutionary timescales is more controversial, however. One key prediction is that genetic constraints should bias the early stages of species divergence along “genetic lines of least resistance” defined by the genetic (co)variance matrix, G. This bias is expected to erode over time as species means and G matrices diverge, allowing phenotypes to evolve away from the major axis of variation. We tested for evidence of this signal in West Indian Anolis lizards, an iconic example of adaptive radiation. We found that the major axis of morphological evolution was well aligned with a major axis of genetic variance shared by all species despite separation times of 20–40 million years, suggesting that divergence occurred along a conserved genetic line of least resistance. Further, this signal persisted even as G itself evolved, apparently because the largest evolutionary changes in G were themselves aligned with the line of genetic least resistance. Our results demonstrate that the signature of genetic constraint may persist over much longer timescales than previously appreciated, even in the presence of evolving genetic architecture. This pattern may have arisen either because pervasive constraints have biased the course of adaptive evolution or because the G matrix itself has been shaped by selection to conform to the adaptive landscape.

Characterizing morphological (co)variation using structural equation models: Body size, allometric relationships and evolvability in a house sparrow metapopulation

“…; McGlothlin et al. ). Although G matrices are highly conserved among some populations, they have also been demonstrated to diverge in response to both selection and/or experimental treatments (Hine et al.…”

“…The stability and evolution of the additive genetic variancecovariance matrix (the G matrix) has received considerable attention because of its implications for the evolutionary trajectory of traits (Arnold et al 2008;Björklund and Gustafsson 2015;Houle et al 2017;McGlothlin et al 2018). Although G matrices are highly conserved among some populations, they have also been demonstrated to diverge in response to both selection and/or experimental treatments (Hine et al 2009;Björklund et al 2012).…”

Does phenotypic plasticity initiate developmental bias?

“…Indeed, previous research on arctic charr (Salvelinus alpinus) ecomorphs shows that while they all display the typical shape responses to benthic and limnetic diets, the variance in shape corresponds to their degree of ecological specialization (Parsons, Skulason, & Ferguson, 2010). Nonetheless, the concept of genetic lines of least resistance remains appealing to many researchers as cases of adaptive divergence often exhibit stereotypical patterns whereby parallelism or convergence in phenotypes predominate across populations or species (Dick, Hinh, Hayashi, & Reznick, 2018;McGlothlin et al, 2018). This is likely reflective of a developmental system that has not been exposed to such conditions for several thousand years.…”

Adaptive phenotypic divergence in an annual grass differs across biotic contexts*

“…; McGlothlin et al. ). However, changing environmental conditions may simultaneously shift both selection on traits (Etterson and Shaw ) and trait variance–covariance relationships (Wood and Brodie III ).…”

“…The course of adaptation to divergent environments can be strongly affected by trait variance and covariance (Schluter 1996;Etterson and Shaw 2001;Chenoweth et al 2010;Yang et al 2019). For example, differences between the direction of selection and the major axis of trait variation may cause trait divergence among populations to reflect the major axis of the G matrix in individual populations (Schluter 1996;Chenoweth et al 2010;McGlothlin et al 2018). However, changing environmental conditions may simultaneously shift both selection on traits (Etterson and Shaw 2001) and trait variance-covariance relationships (Wood and Brodie III 2015).…”