Guppies as a model system
Guppies have become a model system in ecology and evolutionary biology due to repeated, independent adaptation of natural populations to distinct predation environments (Endler, 1995; Haskins, Haskins, McLaughlin, & Hewitt, 1961; D. Reznick, Butler IV, & Rodd, 2001). In Trinidad, high- and low-predation population pairs from different river drainages represent independent evolutionary lineages (Barson, Cable, & Van Oosterhout, 2009; Fraser, Künstner, Reznick, Dreyer, & Weigel, 2015; Gilliam, Fraser, & Alkins-Koo, 1993; Willing et al., 2010) in which colonization of low-predation environments has led to parallel, adaptive changes in life history traits, morphology, and behavior (Endler, 1995; Magurran, 2005; D. A. Reznick, Bryga, & Endler, 1990; D. Reznick et al., 2001; D. N. Reznick, 1997). For example, low-predation guppies shoal less tightly (Huizinga, Ghalambor, & Reznick, 2009; Magurran & Seghers, 1990b, 1991), escape more slowly (Ghalambor, Reznick, & Walker, 2004), are slower to re-commence movement following a predator encounter (Elvidge, Ramnarine, & Brown, 2014; Harris, Ramnarine, Smith, & Pettersson, 2010), and perform fewer predator inspections (Magurran & Seghers, 1990a, 1994) than their high-predation counterparts.
Building on decades of work comparing high- and low-predation populations from the wild, more recent laboratory breeding designs have disentangled genetic and environmental influences of predation on phenotypic differences. These studies demonstrate that a combination of genetic and environmental influences shape guppy life history (Torres Dowdall et al., 2012), morphology (Fischer, Soares, Archer, Ghalambor, & Hoke, 2013; C. A. Handelsman, Ruell, Torres-Dowdall, & Ghalambor, 2014; Ruell et al., 2013; Torres-Dowdal, Handelsman, Reznick, & Ghalambor, 2012), physiology (Fischer, Harris, Hofmann, & Hoke, 2014; Corey A. Handelsman et al., 2013), and behavior (Fischer, Ghalambor, & Hoke, 2016b; Huizinga et al., 2009; Torres-Dowdal et al., 2012). Yet despite many years of work at the level of organism level phenotypes, the mechanisms underlying adaptive phenotypic differences in guppies remain largely unexplored. A single study characterized brain gene expression in multiple populations from the same lineage during the earliest stages of adaptation (~3 generations after colonization of low-predation environments) and found a negative relationship between phenotypic plasticity and adaptive divergence (Ghalambor et al., 2015).
In the current study, we compare the effects of genetic background (high- versus low-predation populations) and developmental environment (rearing with and without predator cues) on brain gene expression patterns in two parallel, independent evolutionary lineages of guppies. These lineages diverged at least 600,000 years ago, with subsequent, more recent colonization of low-predation environments by high-predation ancestors within each river drainage (Fajen & Breden, 1992; Willing et al., 2010). We here compare whole-brain gene expression patternswithin and between lineages based on evolutionary history with and rearing with predators. We focus on gene expression specifically in the brain because the previous gene expression study in guppies used brain tissue (Ghalambor et al., 2015) and because of previous evidence for behavioral plasticity in our focal populations (Fischer et al., 2016b).
To test our hypotheses we (1) quantify the extent of overlap in genes exhibiting significant expression plasticity as well as genetic expression divergence within each drainage, (2) examine associations in the direction of plastic and genetic expression differences, (3) ask whether expression plasticity itself evolves, and (4) assess whether parallel phenotypic adaptation across lineages relies on shared gene expression mechanisms. First, if developmental plasticity does indeed predict genetic divergence, we expect a within-lineage association in gene identity and/or expression direction among those genes showing plastic and genetic expression differences. Second, if gene expression plasticity itself evolves, we expect the extent and/or direction of plastic responses to differ between genetic backgrounds. Finally, if only a few gene expression configurations (i.e. mechanistic paths) can give rise to shared adaptive behavioral phenotypes, we expect parallel adaptation to low-predation habitats to be characterized by parallel evolution in a set of genes that are largely shared between lineages. In contrast, if transcriptional mechanisms are flexible, we expect gene expression divergence in largely non-overlapping gene sets. Taken together, our results allow us to assess the flexibility of transcriptional mechanisms of adaptation across timescales – from developmental plasticity, to genetic divergence, to parallel adaptation across lineages.