Experimental analysis of character coupling across a complex life cycle: Pigment pattern metamorphosis in the tiger salamander,Ambystoma tigrinum tigrinum

Abstract

Developmental relationships among characters are expected to bias patterns of morphological variation at the population level. Studies of character development thus can provide insights into processes of adaptation and the evolutionary diversification of morphologies. Here I use experimental manipulations to test whether larval and adult pigment patterns are coupled across metamorphosis in the tiger salamander, Ambystoma tigrinum tigrinum (Ambystomatidae). Previous investigations showed that the early larval pigment pattern depends on interactions between pigment cells and the lateral line sensory system. In contrast, the results of this study demonstrate that the major features of the adult pigment pattern develop largely independently of both the early larval pattern and the lateral lines. These results suggest that ontogenetic changes that occur across metamorphosis decouple larval and adult pigment patterns and could thereby facilitate independent evolutionary modifications to the patterns during different stages of the life cycle. J. Morphol. 237:53–67, 1998. © 1998 Wiley‐Liss, Inc.

The genetic covariance between life cycle stages separated by metamorphosis

“…Since the early development of the adaptive decoupling hypothesis, empirical studies have been designed to prove or disprove adaptive decoupling by examining genetic correlations for traits on the same side of metamorphosis and traits separated by metamorphosis [9,10,54], or by examining the stage, or stages in which genes with specific functions are expressed [11,12,55]. Although these studies show that adaptive decoupling and developmental constraints across the metamorphic boundary exist, the evolutionary consequences of genetic associations across metamorphosis still remain uncertain.…”

“…Accordingly, the adaptive decoupling hypothesis for the benefits of metamorphosis [4] predicts that traits separated by metamorphosis should be genetically uncorrelated, thereby allowing evolutionary change to occur within each stage, without corresponding effects on phenotypes expressed in other stages. Studies that have tested this prediction by examining genetic associations across metamorphosis have found contradictory results [9][10][11][12], and so the relevance of the & 2014 The Author(s) Published by the Royal Society. All rights reserved.…”

Evolution of danio pigment pattern development

“…Indeed, a metamorphosis of one sort or another is present in the majority of animal life cycles, yet the degree to which premetamorphic and postmetamorphic traits depend on common genetic and developmental mechanisms is an important but largely unexplored question: if traits share genes and cell populations across the metamorphic transition, phenotypes appearing at one stage may be biased by the phenotype expressed at another stage, and evolutionary changes in these phenotypes may be limited or enhanced by countervailing or concordant selection operating across stages (Haldane, 1932;Ebenman, 1992;Moran, 1994;Parichy, 1998).…”

A Comprehensive Expressed Sequence Tag Linkage Map for Tiger Salamander and Mexican Axolotl: Enabling Gene Mapping and Comparative Genomics in Ambystoma

“…The complex as a whole is an important, naturalistic model system because taxa are characterized by extensive interspecific and intraspecific variation for a number of ecologically important traits, including expression of metamorphic vs. nonmetamorphic (paedomorphic) life histories (Gould 1977;Shaffer and Voss 1996), timing of metamorphosis (Rose and Armentrout 1976;Voss and Smith 2005), cannibal vs. normal larval morphologies (Powers 1907;Hoffman and Pfennig 1999), infectious disease (Collins et al 2004), variation in adult coloration and pigment patterning (Reese 1969;Parichy 1996Parichy , 1998, and variation in general morphology (Shaffer 1984;Irschick and Shaffer 1997). In addition, these salamanders are important laboratory models for olfaction (Marchand et al 2004;Park et al 2004), vision (Thoreson et al 2004;Chichilnisky and Reike 2005), cardiogenesis (Denz et al 2004;Zhang et al 2004), embryogenesis (Bachvarova et al 2004;Ericsson et al 2004), and postembryonic development (Parichy 1998;Voss and Smith 2005), including organ and tissue regeneration (Christensen et al 2002;Schnapp and Tanaka 2005). Both natural and laboratory-based research areas are in need of a comprehensive genome map that can be used to identify the position and effect of loci that contribute to phenotypic variation and that can be used to compare features of the salamander genome to other vertebrates.…”