Structure and evolution of the sexually dimorphic integumentary swelling on the hands of dendrobatid poison frogs and their relatives (Amphibia: Anura: Dendrobatoidea)

Abstract

The hands of adult males of many dendrobatid poison frogs and their relatives possess swelling formed by glandular tissue hypothesized to secrete courtship pheromones delivered to the female during cephalic amplexus. Variation in the occurrence and external morphology of the swelling of finger IV has provided important evidence for dendrobatoid systematics for decades, but its underlying structure has not been investigated. We undertook a detailed comparative analysis of the integument of the hand, including both external morphology and histology, of 36 species representing the diversity of dendrobatoid frogs and several close relatives. The swelling is caused by four densely packed, hypertrophic, morpho‐histochemical types of specialized mucous glands (SMGs). We observed type I SMGs on fingers II–V and the wrist, including areas that are not swollen, types II and IV exclusively on finger IV, and type III on finger IV and the wrist. Type I SMGs occur either in isolation or together with types II, III, or IV; types II, III, and IV never occur together or without type I. We delimited 15 characters to account for the variation in external morphology and the occurrence of SMGs. Our data suggest that type I SMGs are a new synapomorphy for Dendrobatoidea and that type II SMGs originated in either the most recent common ancestor (MRCA) of Dendrobatidae or independently in the MRCAs of Aromobatidae and Colostethinae, respectively, while types III and IV are restricted to Anomaloglossus. The discovery of these SMGs adds a new dimension to studies of poison frog reproductive biology, which have investigated acoustic, visual, and tactile cues in courtship, mating, and parental care across the diversity of Dendrobatoidea for decades but have almost entirely overlooked the possible role of chemical cues.

Sexy fingers: Pheromones in the glands of male dendrobatid frogs

“…Further analyses are necessary to identify and compare the expression pattern of SPFs from the different SMGs and swelling types between species. Likewise, given the SPF expression pattern in both species, we expect that similar results will be found across dendrobatid frogs with type I and II SMGs, for example, in Silverstoneia flotator, species of the genus Ameerega, Colostethus, Epipedobates, Leucostethus and in species of the subfamily Hyloxalinae except H. pulchellus, for which the absence of SMGs was confirmed (Cavalcanti et al, 2022).…”

“…In dendrobatids, during cephalic amplexus, the male's fingers, hands, and arms are in contact with the female's snout, loreal region, lips and throat, leading to the suggestion of a transcutaneous pheromone delivery (Cavalcanti et al, 2022) Based on our results, we hypothesise that L. brachistriatus also has cephalic amplexus, although direct observations are still needed to confirm this.…”

“…In other amphibians, SPFs are highly expressed in male salamander and frog macroglands and are most likely produced and stored in SMGs (Bossuyt et al, 2019;Janssenswillen, Willaert, et al, 2015b;Schulte et al, 2021Schulte et al, , 2022. In dendrobatid frogs, SMGs are responsible for the male swelling (macroglands) in the fingers and wrist (Cavalcanti et al, 2022). While type I SMGs are widely distributed in dendrobatid fingers and extend to the wrist, type II SMGs are restricted to finger IV and are primarily present in species with visible swelling (Cavalcanti et al, 2022).…”

“…Adult males of many species have been reported to have swelling in the wrists and fingers (Grant et al, 2006(Grant et al, , 2017Grant & Rodríguez, 2001). This swelling is most notable in finger IV (finger numeration following Fabrezi & Alberch, 1996) and is caused by different types of SMGs known only in Dendrobatoidea (Cavalcanti et al, 2022). Type I SMGs are present in swollen areas (finger and wrist) and in fingers lacking visible swelling.…”

“…Type II is only present in swollen regions of finger IV, exclusively in the family Dendrobatidae. Types III and IV are also present in the swollen areas but only in the genus Anomaloglossus (Cavalcanti et al., 2022). Histochemical analysis suggests that these SMGs have the potential to produce protein secretions (Cavalcanti et al., 2022), such as courtship pheromones like SPFs, that could be transferred to the female during amplexus, as suggested for other frogs with nuptial pads (Bossuyt et al., 2019; Thomas et al., 1993; Willaert et al., 2013).…”