Contrasting parental roles shape sex differences in poison frog space use but not navigational performance

Abstract

Sex differences in vertebrate spatial abilities are typically interpreted under the adaptive specialization hypothesis, which posits that male reproductive success is linked to larger home ranges and better navigational skills. The androgen spillover hypothesis counters that enhanced male spatial performance may be a byproduct of higher androgen levels. Animal groups that include species where females are expected to outperform males based on life-history traits are key for disentangling these hypotheses. We investigated the association between sex differences in reproductive strategies, spatial behavior, and androgen levels in three species of poison frogs. We tracked individuals in natural environments to show that contrasting parental sex roles shape sex differences in space use, where the sex performing parental duties shows wider-ranging movements. We then translocated frogs from their home areas to test their navigational performance and found that the caring sex outperformed the non-caring sex only in one out of three species. In addition, males across species displayed more explorative behavior than females and androgen levels correlated with explorative behavior and homing accuracy. Overall, we reveal that poison frog reproductive strategies shape movement patterns but not necessarily navigational performance. Together this work suggests that prevailing adaptive hypotheses provide an incomplete explanation of sex differences in spatial abilities.

Intraspecific divergence of sexual size dimorphism and reproductive strategies in a polytypic poison frog

“…Moreover, by measuring estrogen levels in females from different populations, we could investigate the possibility that females can affect the sex ratios of their clutches via endogenous sex steroids (Nakamura, 2010). An environmental explanation for female-biased sex ratios is that males might generally face a higher predation pressure compared to females, because they move larger distances when transporting tadpoles (Pašukonis et al, 2019;Pašukonis et al, 2022), potentially making them more conspicuous to predators (Rojas & Endler, 2013). In line with having the largest SSD, frogs from Mataroni also had the most female-biased sex ratio, which might be related to their comparatively higher fecundity.…”

Still little evidence sex differences in spatial navigation are evolutionary adaptations

“…[ 1 ]. Species included the Asian small-clawed otter ( Aonyx cinereus ) [ 15 ], brilliant-thighed poison frog ( Allobates femoralis ) [ 48 ], California mouse ( Peromyscus californicus ) [ 43 , 49 ], chimpanzee ( Pan troglodytes ) [ 50 – 53 ], cuttlefish ( Sepia officinalis ) [ 54 ], deer mouse ( Peromyscus maniculatus ) [ 43 , 55 – 57 ], diablito poison frog ( Oophaga sylvatica ) [ 48 ], dyeing poison frog ( Dendrobates tinctorius ) [ 48 ], European rabbit ( Oryctolagus cuniculus ) [ 58 – 60 ], giant panda ( Ailuropoda melanoleuca ) [ 15 , 61 ], horse ( Equus caballus ) [ 62 – 64 ], human ( Homo sapiens ) [ 5 , 23 – 25 , 33 , 65 – 78 ], meadow vole ( Microtus pennsylvanicus ) [ 12 , 79 – 81 ], mouse ( Mus musculus ) [ 82 – 87 ], Natal mole-rat ( Cryptomys hottentotus ) [ 88 ], pine vole ( Microtus pinetorum ) [ 12 ], prairie vole ( Microtus ochrogaster ) [ 42 , 89 – 91 ], rat ( Rattus norvegicus ) [ 92 – 96 ], rhesus monkey ( Macaca mulatta ) [ 97 – 99 ], rusty crayfish ( Orconectes rusticus ) [ 100 , 101 ] and Talas tuco-tuco ( Ctenomys talarum ) [ 102 – 104 ].…”

“…We compiled home range size and spatial navigation data from 66 studies and 21 species (electronic supplementary material, table S1), nearly double the numbers in Clint et al [1]. Species included the Asian small-clawed otter (Aonyx cinereus) [15], brilliant-thighed poison frog (Allobates femoralis) [48], California mouse (Peromyscus californicus) [43,49], chimpanzee (Pan troglodytes) [50][51][52][53], cuttlefish (Sepia officinalis) [54], deer mouse (Peromyscus maniculatus) [43,[55][56][57], diablito poison frog (Oophaga sylvatica) [48], dyeing poison frog (Dendrobates tinctorius) [48], European rabbit (Oryctolagus cuniculus) [58][59][60],…”

Individual Behavioral Variability Across Time and Contexts inDendrobates tinctoriusPoison Frogs

“…These species’ vivid hues are an honest signal of their toxicity, and both traits have coevolved with bold behavior and a conspicuous, diurnal lifestyle as compared to most anurans (Summers 2003; Maan and Cummings 2012). Poison frogs exhibit a rich array of complex behaviors, encompassing anti- predator defenses (Breed 2008), aggressive territoriality (Crothers and Cummings 2015), parental care (Roland and O’Connell 2015; Fischer et al 2019), spatial learning and navigation (Liu et al 2016; Pašukonis et al 2022), and behavioral plasticity (Ringler et al 2017; Peignier et al 2023). Taken together, these characteristics have garnered poison frogs increasing attention in the realm of animal personality and behavioral syndromes.…”

“…Dyeing poison frogs, Dendrobates tinctorius , have long been popular in zoos, aquaria, and the pet trade, and have recently received increasing research attention in the wild (Rojas and Pašukonis 2019; Fouilloux et al 2021; Pašukonis et al 2022) and the lab (Sonnleitner et al 2022; Fischer et al 2019, Fischer and O’Connell 2020). D. tinctorius boast a variety of bright color morphs without sexual dimorphism in coloration.…”