Developmental plasticity mirrors differences among taxa in spadefoot toads linking plasticity and diversity

*Department of Biology, Boston University, 5 Cummington Street, Boston, MA 02215; and
^‡Department of Biological Sciences, University of Cincinnati, Cincinnati, OH 45221

Edited by David B. Wake, University of California, Berkeley, CA, and approved October 25, 2006 (received for review May 1, 2006)

Abstract

Developmental plasticity is found in most organisms, but its role in evolution remains controversial. Environmentally induced phenotypic differences may be translated into adaptive divergence among lineages experiencing different environmental conditions through genetic accommodation. To examine this evolutionary mechanism, we studied the relationship between plasticity in larval development, postmetamorphic morphology, and morphological diversity in spadefoot toads, a group of closely related species that are highly divergent in the larval period and body shape and are distributed throughout temperate areas of both the New and the Old World. Previous studies showed that accelerated metamorphosis is adaptive for desert-dwelling spadefoot toads. We show that even under common garden conditions, spadefoot toad species show divergent reaction norms for the larval period. In addition, experimentally induced changes in the larval period caused correlated morphological changes in postmetamorphic individuals such that long larval periods resulted in relatively longer hindlimbs and snouts. A comparative analysis of morphological variation across spadefoot toad species also revealed a positive correlation between the larval period and limb and snout lengths, mirroring the effects of within-species plasticity at a higher taxonomic level. Indeed, after ≈110 Ma of independent evolution, differences in the larval period explain 57% of the variance in relative limb length and 33% of snout length across species. Thus, morphological diversity across these species appears to have evolved as a correlated response to selection for a reduced larval period in desert-dwelling species, possibly diverging from ancestral plasticity through genetic accommodation.

Footnotes

^†To whom correspondence should be addressed. E-mail: igmestre{at}bu.edu
Author contributions: I.G.-M. and D.R.B. designed research, performed research, analyzed data, and wrote the paper.
The authors declare no conflict of interest.
This article is a PNAS direct submission.
This article contains supporting information online at www.pnas.org/cgi/content/full/0603562103/DC1.
Abbreviations:

PGLS,

phylogenetic generalized least-squares;

TH,

thyroid hormone