Complex and Dynamic Gene-by-Age and Gene-by-Environment Interactions Underlie Functional Morphological Variation in Adaptive Divergence in Arctic Charr (Salvelinus alpinus)

Abstract

The evolution of adaptive phenotypic divergence requires heritable genetic variation. However, it is underappreciated that trait heritability is molded by developmental processes interacting with the environment. We hypothesized that the genetic architecture of divergent functional traits was dependent on age and foraging environment. Thus, we induced plasticity in full-sib families of Arctic charr (Salvelinus alpinus) morphs from two Icelandic lakes by mimicking prey variation in the wild. We characterized variation in body shape and size at two ages and investigated their genetic architecture with quantitative trait locus (QTL) analysis. Age had a greater effect on body shape than diet in most families, suggesting that development strongly influences phenotypic variation available for selection. Consistent with our hypothesis, multiple QTL were detected for all traits and their location depended on age and diet. Many of the genome-wide QTL were located within a subset of duplicated chromosomal regions suggesting that ancestral whole genome duplication events have played a role in the genetic control of functional morphological variation in the species. Moreover, the detection of two body shape QTL after controlling for the effects of age provides additional evidence for genetic variation in the plastic response of morphological traits to environmental variation. Thus, functional morphological traits involved in phenotypic divergence are molded by complex genetic interactions with development and environment.

Keywords: development; genetic architecture; phenotypic divergence; phenotypic plasticity; salmonid fishes.

Figure 1

A schematic depicting the linear measurement traits (A) generated between pairs of 18 homologous landmarks (B) used to investigate morphological variation in Arctic charr (Salvelinus alpinus). The linear measurement traits are shown with color‐coded lines (head measurements [purple] – jawL: 1–18, jaw length; headL: 1–17, head length; headD: 5–15, head depth; eyeD: 2–3, eye diameter; body measurements [blue] – bodyD1: 6–14, body depth 1; bodyD2: 7–14, body depth 2; caudal peduncle measurements [green] – caudP1: 8–9, caudal peduncle 1; caudP2: 9–11, caudal peduncle 2; caudP3: 11–12, caudal peduncle 3; caudP4: 8–12, caudal peduncle 4; fin measurements [orange] – dorsW: 6–7, width at base of dorsal fin; pecW: 15–16, width at base of pectoral fin; body size [gray] – forkL: 1–10, fork length).

Figure 2

Family specific scatter plots of the first two principal component (PC) axes based on principal components analysis of all landmark positions from all fish combined (eight families, two diets, two juvenile ages), showing diet‐induced body shape variation over ontogeny in Arctic charr morphs from Þingvallavatn (T‐LB – large benthivore, T‐PL – planktivore). Wireframe graphs illustrate the extremes of body shape change (red lines, black dots) from the mean shape (gray lines, gray dots) along each PC axis, at a magnification of 2.5×. Benthic A1: benthic diet, juvenile age 1 (90 days); Benthic A2: benthic diet, juvenile age 2 (160 days); Limnetic A1: limnetic diet, juvenile age 1 (90 days); Limnetic A2: limnetic diet, juvenile age 2 (160 days).

Figure 3

Family specific scatter plots of the first two principal component (PC) axes based on principal components analysis of all landmark positions from all fish combined (eight families, two diets, two juvenile ages), showing diet‐induced body shape variation over ontogeny in Arctic charr morphs from Vatnshlíðarvatn (V‐B – brown, V‐S – silver). Wireframe graphs illustrate the extremes of body shape change (red lines, black dots) from the mean shape (gray lines, gray dots) along each PC axis, at a magnification of 2.5×. Benthic A1: benthic diet, juvenile age 1 (90 days); Benthic A2: benthic diet, juvenile age 2 (160 days); Limnetic A1: limnetic diet, juvenile age 1 (90 days); Limnetic A2: limnetic diet, juvenile age 2 (160 days).

Figure 4

Arctic charr linkage groups with significant QTL at the chromosome‐wide level for 13 linear measurement traits and the first 2 principal components (PC) in 8 full‐sib families from 4 morphs (Þingvallavatn: T‐LB – large benthivore, T‐PL – planktivore; Vatnshlíðarvatn: V‐B – brown, V‐S – silver). The progeny were reared on alternate diet treatments (benthic and limnetic) and sampled at two juvenile ages, 90 days (A1) and 160 days (A2).