Ancestral plasticity and allometry in threespine stickleback reveal phenotypes associated with derived, freshwater ecotypes

Abstract

For over a century, evolutionary biologists have debated whether and how phenotypic plasticity impacts the processes of adaptation and diversification. The empirical tests required to resolve these issues have proven elusive, mainly because it requires documentation of ancestral reaction norms, a difficult prospect where many ancestors are either extinct or have evolved. The threespine stickleback radiation is not limited in this regard, making it an ideal system in which to address general questions regarding the role of plasticity in adaptive evolution. As retreating ice sheets have exposed new habitats, oceanic stickleback founded innumerable freshwater populations, many of which have evolved parallel adaptations to their new environments. Because the founding oceanic population is extant, we can directly evaluate whether specific patterns of ancestral phenotypic expression in the context of novel environments (plasticity), or over ontogeny, predisposed the repeated evolution of “benthic” and “limnetic” ecotypes in shallow and deep lakes, respectively. Consistent with this hypothesis, we found that oceanic stickleback raised in a complex habitat and fed a macroinvertebrate diet expressed traits resembling derived, benthic fish. Alternatively, when reared in a simple environment on a diet of zooplankton, oceanic stickleback developed phenotypes resembling derived, limnetic fish. As fish in both treatments grew, their body depths increased allometrically, as did the size of their mouths, while their eyes became relatively smaller. Allometric trajectories were subtly but significantly impacted by rearing environment. Thus, both environmental and allometric influences on development, along with their interactive effects, produced variation in phenotypes consistent with derived benthic and limnetic fish, which may have predisposed the repeated genetic accommodation of this specific suite of traits. We also found significant shape differences between marine and anadromous stickleback, which has implications for evaluating the ancestral state of stickleback traits.

Effects of Allometry, Sex, and River Location on Morphological Variation of Freshwater Drum Aplodinotus grunniens in the Wabash River, USA

“…Rather, it is multifaceted and results from a combination of allometry, sex, and river location (i.e., local habitat). These conclusions are similar to those of Hood and Heins (2000) and Wund et al (2012), where ontogenic Fig. 3.…”

A heuristic model on the role of plasticity in adaptive evolution: plasticity increases adaptation, population viability and genetic variation

“…Congruently, there are many cases of rapidly diversifying groups of species where genetic accommodation of plasticity is likely to have been the main driver for divergence [53], as in sticklebacks [54,55], anole lizards [56] or arctic charrs [57]. Rapid adaptive transitions between environments are more easily achieved by plastic than nonplastic genotypes ( figures 3 and 4), and we show that genetic assimilation of induced phenotypes and the associated loss of plasticity will occur if costs of plasticity are high and the environment stabilizes (figure 4).…”

Life-history plasticity in female threespine stickleback

“…The threespine stickleback adaptive radiation has proven a model for understanding evolutionary processes in general (Bell and Foster, 1994), and for investigating behavioral (Foster and Wund, 2011;Foster et al, 2015) and morphological (Wund et al, 2008(Wund et al, , 2012 plasticity specifically. In contrast, there has been much less discussion of life-history plasticity in this model species.…”