Phenotypic integration mediated by hormones: associations among digit ratios, body size and testosterone during tadpole development

Leandro Lofeu,Renata Brandt,Tiana Kohlsdorf

doi:10.1186/s12862-017-1021-0

Leandro Lofeu, Renata Brandt + Show 1 more

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https://doi.org/10.1186/s12862-017-1021-0

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Abstract

BackgroundDevelopmental associations often explain phenotypic integration. The intersected hormonal regulation of ontogenetic processes fosters predictions of steroid-mediated phenotypic integration among sexually dimorphic traits, a statement defied by associations between classical dimorphism predictors (e.g. body size) and traits that apparently lack sex-specific functions (e.g. ratios between the lengths of Digits II and IV - 2D:4D). Developmental bases of female-biased 2D:4D have been identified, but these remain unclear for taxa presenting male-biased 2D:4D (e.g. anura). Here we propose two alternative hypotheses to investigate evolution of male-biased 2D:4D associated with sexually dimorphic body size using Leptodactylus frogs: I)‘hypothesis of sex-specific digit responses’ - Digit IV would be reactive to testosterone but exhibit responses in the opposite direction of those observed in female-biased 2D:4D lineages, so that Digit IV turns shorter in males; II) ‘hypothesis of identity of the dimorphic digit’- Digit II would be the dimorphic digit.ResultsWe compiled the following databases using Leptodactylus frogs: 1) adults of two species from natural populations and 2) testosterone-treated L. fuscus at post-metamorphic stage. Studied traits seem monomorphic in L. fuscus; L. podicipinus exhibits male-biased 2D:4D. When present, 2D:4D dimorphism was male-biased and associated with dimorphic body size; sex differences resided on Digit II instead of IV, corroborating our ‘hypothesis of identity of the dimorphic digit’. Developmental steroid roles were validated: testosterone-treated L. fuscus frogs were smaller and exhibited masculinized 2D:4D, and Digit II was the digit that responded to testosterone.ConclusionWe propose a model where evolution of sexual dimorphism in 2D:4D first originates from the advent, in a given digit, of increased tissue sensitivity to steroids. Phenotypic integration with other sexually dimorphic traits would then occur through multi-trait hormonal effects during development. Such process of phenotypic integration seems fitness-independent in its origin and might explain several cases of steroid-mediated integration among sexually dimorphic traits.

Highlights

The difference between lineages that exhibit a malebiased 2D:4D values (2D):4D and those characterized by a femalebiased 2D:4D resides on the identity of the dimorphic digit responding to steroids during development
Dimorphism in digit ratios is developmentally correlated with variation in body size in anurans, an association identified in Leptodactylus natural populations and validated by experiments exposing developing tadpoles to increased testosterone concentrations
We provide evidence that testosterone plays a major role in the establishment of such phenotypic integration, and likely rules the evolution of female-biased body size dimorphism in Anura

Summary

Introduction

The intersected hormonal regulation of ontogenetic processes fosters predictions of steroid-mediated phenotypic integration among sexually dimorphic traits, a statement defied by associations between classical dimorphism predictors (e.g. body size) and traits that apparently lack sex-specific functions (e.g. ratios between the lengths of Digits II and IV - 2D:4D). Multiple-trait effects of hormonal variation are especially evident in sexually dimorphic phenotypes, given that sex steroids (androgens and estrogens) modulate several physiological, morphological and behavioral sex-specific features in vertebrate animals [5,6,7]. Such steroids may affect the development of traits that apparently lack sex-specific functions, such as digit proportions [8, 9]. Whereas in some species the 2D:4D ratio is larger in females than males (2D:4D female-biased, identified in salamanders, lizards, rodents and some primates, including the chacm baboons, gorillas and some populations of chimpanzees), in other lineages the males exhibit the largest 2D:4D values (2D:4D male-biased, observed in anurans, birds and some primates, including the guinea baboons and the rhesus macaque [10, 41, 43]), a variation that suggests some evolutionary lability at the level of digit tissue responses to sex steroids during development ([41, 43]; see Fig. 1)

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