Does plasticity enhance or dampen phenotypic parallelism? A test with three lake–stream stickleback pairs

Abstract

Parallel (and convergent) phenotypic variation is most often studied in the wild, where it is difficult to disentangle genetic vs. environmentally induced effects. As a result, the potential contributions of phenotypic plasticity to parallelism (and nonparallelism) are rarely evaluated in a formal sense. Phenotypic parallelism could be enhanced by plasticity that causes stronger parallelism across populations in the wild than would be expected from genetic differences alone. Phenotypic parallelism could be dampened if site-specific plasticity induced differences between otherwise genetically parallel populations. We used a common-garden study of three independent lake-stream stickleback population pairs to evaluate the extent to which adaptive divergence has a genetic or plastic basis, and to investigate the enhancing vs. dampening effects of plasticity on phenotypic parallelism. We found that lake-stream differences in most traits had a genetic basis, but that several traits also showed contributions from plasticity. Moreover, plasticity was much more prevalent in one watershed than in the other two. In most cases, plasticity enhanced phenotypic parallelism, whereas in a few cases, plasticity had a dampening effect. Genetic and plastic contributions to divergence seem to play a complimentary, likely adaptive, role in phenotypic parallelism of lake-stream stickleback. These findings highlight the value of formally comparing wild-caught and laboratory-reared individuals in the study of phenotypic parallelism.

Adaptive phenotypic plasticity contributes to divergence between lake and river populations of an East African cichlid fish

“…In stickleback, transcriptomic plasticity may play a substantial role in migrants’ adaptation to novel environments (Lohman et al., 2017). In this system genetic divergence and plasticity appear to work together in shaping between‐ecotype differences in gene expression (Lohman et al., 2017) and parallel adaptive phenotypic divergence between lake and stream populations (Oke et al., 2016). Our results provide support for the same forces working together in a cichlid lake‐stream system.…”

Allometric trajectories of body and head morphology in three sympatric Arctic charr (Salvelinus alpinus (L.)) morphs

“…This is often seen for primates (Mitteroecker, Gunz, Bernhard, Schaefer, & Bookstein, 2004; Richtsmeier, Corner, Grausz, Cheverud, & Danahey, 1993; Schultz, 1924) and for fish such as Eurasian perch ( Perca fluviatilis ; Svanbäck & Eklöv, 2002). However, species or morphs may show a converging morphology if they experience more similar environments at later life stages, for instance seen for three‐spined sticklebacks and European cave salamanders (Family: Plethodontidae; Adams & Nistri, 2010; Oke et al., 2016). …”

Heritable gene expression differences between lake and stream stickleback include both parallel and antiparallel components

“…This result intuitively suggests that some aspect of lake–stream divergence—that what is influenced by these antiparallel genes—must also be antiparallel. Indeed, antiparallel phenotypic divergence for some morphological traits is evident for lake–stream stickleback in the Robert’s versus Misty watersheds (Oke et al , 2016), for lake–stream stickeback in other watersheds (Hendry and Taylor, 2004; Kaeuffer et al , 2012) and for many other fishes (Oke et al , 2017). Recent work has attributed some of this lake–stream phenotypic antiparallelism to antiparallel divergence in lake–stream habitat features (Stuart et al , 2017) and therefore, presumably, antiparallel divergence in lake–stream natural selection.…”

“…In particular, these studies have usually examined gene expression in wild-caught individuals (see, for example, Galindo et al , 2010; Manousaki et al , 2013; Westram et al , 2014) that will include an unknown combination of plastic and gene sequence effects on gene expression. Plasticity in such situations can either promote or constrain adaptive divergence (Pfennig et al , 2010; Moczek et al , 2011; Fitzpatrick, 2012; Ghalambor et al , 2015; Oke et al , 2016); but, importantly, plastic expression changes are not encoded by sequence changes, and therefore cannot be used to predict evolutionary trajectories. Yet, other studies have shown that gene expression variation often can be heritable and has contributed to adaptive divergence in several species (Pritchard et al , 2017).…”

“…One type of ecotype pair that has proven particularly useful in this regard is that formed by parapatric lake–stream populations (see, for example, Moodie, 1972; Reimchen et al , 1985; Lavin and McPhail, 1993; Deagle et al , 1996; Reusch et al , 2001; Hendry et al , 2002; Aguirre, 2009; Berner et al , 2010; Eizaguirre et al , 2011; Kaeuffer et al , 2012; Roesti et al , 2012; Lucek et al , 2013; Ravinet et al , 2013; Oke et al , 2016; Stuart et al , 2017). Throughout its range, the lake ecotype has generally evolved a shallower body and more numerous gill rakers; adaptations for sustained swimming in open water while feeding on limnetic prey (Caldecutt and Adams, 1998; Berner et al , 2008; Kaeuffer et al , 2012).…”