Phenotypic Divergence along Lines of Genetic Variance

Abstract

Natural populations inhabiting the same environment often independently evolve the same phenotype. Is this replicated evolution a result of genetic constraints imposed by patterns of genetic covariation? We looked for associations between directions of morphological divergence and the orientation of the genetic variance-covariance matrix (G) by using an experimental system of morphological evolution in two allopatric nonsister species of rainbow fish. Replicate populations of both Melanotaenia eachamensis and Melanotaenia duboulayi have independently adapted to lake versus stream hydrodynamic environments. The major axis of divergence (z) among all eight study populations was closely associated with the direction of greatest genetic variance (gmax), suggesting directional genetic constraint on evolution. However, the direction of hydrodynamic adaptation was strongly associated with vectors of G describing relatively small proportions of the total genetic variance, and was only weakly associated with gmax. In contrast, divergence between replicate populations within each habitat was approximately proportional to the level of genetic variance, a result consistent with theoretical predictions for neutral phenotypic divergence. Divergence between the two species was also primarily along major eigenvectors of G. Our results therefore suggest that hydrodynamic adaptation in rainbow fish was not directionally constrained by the dominant eigenvector of G. Without partitioning divergence as a consequence of the adaptation of interest (here, hydrodynamic adaptation) from divergence due to other processes, empirical studies are likely to overestimate the potential for the major eigenvectors of G to directionally constrain adaptive evolution.

Studying phenotypic evolution using multivariate quantitative genetics

“…Schluter (1996) explicitly looked for and found evidence that the direction of divergence becomes less similar to major eigenvectors of G as time since divergence increases. This result contrasts with that of McGuigan et al . (2005) who also compared G with directions of divergence over different timescales.…”

“…Development of methods for associating G with divergence, along with Schluter's (1996) results, encouraged a flurry of empirical tests of directional genetic constraint on evolution. These analyses both supported (Schluter 1996; Arnold & Phillips 1999; Badyaev & Foresman 2000; Begin & Roff 2003, 2004; Blows & Higgie 2003; McGuigan et al . 2005) and rejected (Merilä & Björklund 1999; Badyaev & Hill 2000; McGuigan et al .…”

“…These analyses both supported (Schluter 1996; Arnold & Phillips 1999; Badyaev & Foresman 2000; Begin & Roff 2003, 2004; Blows & Higgie 2003; McGuigan et al . 2005) and rejected (Merilä & Björklund 1999; Badyaev & Hill 2000; McGuigan et al . 2005) the hypothesis that G imposes a directional constraint on phenotypic evolution over typical micro‐evolutionary time frames.…”

“…(A) The diagonals of G indicate how much additive genetic variance underlies each trait, while the off‐diagonals summarize the additive genetic covariance between each pair of traits. (B) Quantitative genetics of morphology in a population of the Lake Eacham rainbow fish ( Melanotaenia eachamensis ) (see McGuigan et al . 2005).…”

“…Six traits were measured: (1) standard length (a–f); (2) predorsal length (a–c measured along midline); (3) head depth (vertical distance through b); (4) body depth (vertical distance through c); (5) caudal peduncle length (d–e); and (6) caudal peduncle depth (e–g). G was estimated by regression of laboratory‐reared offspring on wild‐caught parents for 44 families (McGuigan et al . 2005).…”