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, 17 (1), 175

Phenotypic Integration Mediated by Hormones: Associations Among Digit Ratios, Body Size and Testosterone During Tadpole Development

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Phenotypic Integration Mediated by Hormones: Associations Among Digit Ratios, Body Size and Testosterone During Tadpole Development

Leandro Lofeu et al. BMC Evol Biol.

Abstract

Background: Developmental 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.

Results: We 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.

Conclusion: We 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.

Keywords: Leptodactylus; Male-biased 2D:4D; Sexual dimorphism; Steroids.

Conflict of interest statement

Ethics approval and consent to participate

Animals were collected under ICMBio permit 32,862–1, following protocols from IUCN [56], and the experimental procedures were implemented according to the Animal Research Committee of University of São Paulo (CEUA/USP).

Competing interests

The authors declare that they have no competing interests.

Publisher’s Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Figures

Fig. 1
Fig. 1
Proposed hypotheses for sexual dimorphism in 2D:4D ratios. a 2D:4D female-biased sexual dimorphism, which consists of larger digit ratios in females (F) than males (M), a pattern explained by Digit IV responding to sex-steroids (‘SS’, androgens and estrogens); (b and c) two hypotheses proposed here for the establishment of male-biased 2D:4D digit ratios. b Hypothesis I (HI): male-biased patterns are explained by inverted between-sex responses of Digit IV to sex-steroids; thus, Digit IV becomes shorter in males in response to testosterone. c Hypothesis II (HII): male-biased patterns reflect a change in the identity of the digit responding to sex-steroids, not the direction of the response (elongation or shortening); thus, Digit II is the one dimorphic and is longer in males and shorter in females
Fig. 2
Fig. 2
Comparisons between sexes and among treatments in Leptodactylus frogs. a Residuals against body size of digit ratios 2D:4D (2D:4D) and lengths of Digit II and Digit IV for males (black) and females (white) of Leptodactylus podicipinus and L. fuscus. b Residuals of phalangeal lengths (proximal and distal phalanges) of Digit II in males (black) and females (white) of Leptodactylus podicipinus.c X-ray images indicating bone segments measured in adult specimens (scale bar of 10 mm provided): DII = Digit II, D IV = Digit IV, dp = distal phalanx, pp. = proximal phalanx, m = metacarpal. d Results from experimental testosterone exposure of Leptodactylus fuscus tadpoles during development, indicating differences in 2D:4D and digit lengths between the testosterone-exposed group (black) and the two controls (white: Control A = vehicle solution only and grey: Control B = only water). e Osteological differences regarding the length of Digit II proximal phalanx between the group treated with testosterone (black) and the two controls (white: Control A = vehicle solution only and grey: Control B = only water). In all graphs, the columns correspond to mean values, and the vertical bars indicate standard errors; all measurements were taken in millimeters. Statistically significant differences (p < 0.05) are indicated by asterisks
Fig. 3
Fig. 3
Phenotypic integration of body size and digit ratios in Leptodactylus. a Correlation between sexual dimorphism indexes (SDI) for the digit ratio 2D:4D and body size (SVL) for the six L. podicipinus populations. The localities are Humaitá, AM (H), Corumbá, MT (C), São José do Rio Preto, SP (RP), Uberlândia, MG (Ub), Rio Claro, SP (RC) and Porto Velho, RO (PV). b Correlation between body size (SVL) and 2D:4D digit ratios of L. fuscus tadpoles in three conditions: treated with testosterone (black), Control A (white) and Control B (grey); all measurements were taken in millimeters
Fig. 4
Fig. 4
Hypothetic model of the evolution of digit ratio dimorphism modulated by multi-trait hormonal effects on developmental pathways. Acquisition of higher sensitivity to sex steroids in specific digits (indicated by stars, Digit II or IV) is initially independent of hormonal concentrations per se (see blue arrows), and the identity of dimorphic digits seems labile among tetrapod lineages (small black arrows among digits). The advent of sexual dimorphism in digit ratios evolves independently of variation in the hormonal milieu (blue arrows), and such trajectory results on a diversity of patterns of digit ratio dimorphism in Tetrapoda. Once the sensibility of a dimorphic digit to steroids is present in the lineage, the length of the digit (and consequently the digit ratio) changes in response to variations in hormonal concentrations and together with others traits that are also hormonally-regulated (doted black arrows).Multi-trait effects of circulating steroids during development (orange lines and arrows) establish correlated variation between digit ratios and other dimorphic traits

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References

    1. Melo D, Porto A, Cheverud JM, Marroig G. Modularity: genes, development, and evolution. Annu Rev Ecol Evol Syst. 2016; doi:10.1146/annurev-ecolsys-121415-032409. - PMC - PubMed
    1. Klingenberg CP. Studying morphological integration and modularity at multiple levels: concepts and analysis. Phil Trans R Soc B. 2014; doi:10.1098/rstb.2013.0249. - PMC - PubMed
    1. Cox RM, McGlothlin JW, Bonier F. Hormones as mediators of phenotypic and genetic integration: an evolutionary genetics approach. Integr Comp Biol. 2016; doi:10.1093/icb/icw033. - PubMed
    1. McGlothlin JW, Ketterson ED. Hormonal Pleiotropy and the evolution of correlated Traits1. In: Ketterson ED, Atwell JW, editors. Integrative biology and evolutionary diversity in the junco. Snowbird: University of Chicago Press; 2016. pp. 100–119.
    1. Ketterson E, JrV N. Adaptation, Exaptation, and constraint: a hormonal perspective. Am Nat. 1999; doi:10.1086/303280. - PubMed
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