Biased birth sex ratios of mammals and birds in zoos

Abstract

Birth sex ratio biases can amplify extinction risks, especially in small, zoo-maintained populations which is of particular concern in species under threat of extinction. Thus, understanding the drivers of such biases is critical for conservation outcomes. We analysed birth records from 129 avian and 324 mammalian species in zoos worldwide between 1980 and 2021. Using Bayesian phylogenetic models, we found a phylogenetic signal in birth sex ratios (BSR), with substantial variation across clades. Penguins, falcons, and parrots showed slightly male-biased BSRs; ungulates showed female-biased BSR, and primates male-biased BSR. Across birds, variation in BSRs was predicted by sexual size dimorphism and clutch size, whereas in mammals, mating system was the main predictor of BSR. We identified 30 conservation flagship species with significantly biased BSRs, raising concern for the demographic sustainability of their captive populations. These results highlight the role of both evolutionary history and life-history traits in shaping sex ratio variation across taxa. Our findings underscore the importance of integrating phylogenetic and biological predictors into conservation planning and breeding program design. They also call for further research into the biological and management processes-that include sexual selection, parental investment, housing, and sexing practices-that may contribute to sex ratio variation in zoo populations.

Keywords: Biodiversity; Conservation; Evolutionary ecology; Mating systems; Sex allocation; Sexual dimorphism; Zoo management.

Fig. 1

(A) Forest plot displaying posterior means (deviation from equal sex ratio) and their corresponding 95% credible intervals (CI) for birth sex ratio (BSR) and temporal trend in birth sex ratio (tBSR) in birds, using the intercept as an explanatory variable. Sex ratios are expressed as proportion of males. Posterior means and standard deviations were obtained from MCMCglm models. (B) Phylogenetic distribution of BSR and tBSR in 129 bird species. The plot shows a consensus tree constructed from 100 equally probable phylogenetic trees based on the bird phylogeny by Jetz et al.using the least squares method. Branch color gradients represent BSR, with blue indicating male-biased and red indicating female-biased BSR. Tip point color gradients represent tBSR, with fluorescent blue indicating male-biased and purple indicating female-biased tBSR. Orders are numbered, indicating specific nodes from which they branch. The Gruiformes order is represented by nodes 4 and 7, as the houbara bustard (Chlamydotis undulata), a member of this order, branches before the most recent common ancestor (MRCA) of shorebirds, flamingos, and cranes. Two species are highlighted: the near threatened nēnē (Branta sandvicensis), endemic to the Hawaiian Islands, which showed a statistically significant male BSR (binomial test p = 0.049), and the vulnerable houbara bustard, known for its extravagant male courtship displays, which exhibited statistically significant tBSR (β = 0.021, p = 0.013).

Fig. 2

(A) Forest plot displaying posterior means (deviation from equal sex ratio) and their corresponding 95% credible intervals (CI) for birth sex ratio (BSR) and temporal trend in birth sex ratio (tBSR) in mammals, using the intercept as an explanatory variable. Sex ratios are expressed as proportion of males. Posterior means and standard deviations were obtained from MCMCglm models. (B) Phylogenetic distribution of BSR and tBSR in 324 mammal species. The plot shows a consensus tree constructed from 100 equally probable phylogenetic trees based on the mammal phylogeny by Upham et al. (2019), using the extend method. Branch color gradients represent BSR, with blue indicating male-biased and red indicating female-biased BSR. Tip point color gradients represent tBSR, with dark blue indicating male-biased and pink indicating female-biased tBSR. Orders are numbered, indicating specific nodes from which they branch. Two species are highlighted: the endangered African wild dog (Lycaon pictus), which showed a statistically significant male BSR (binomial test p = 0.022), and the endangered Asian elephant (Elephas maximus), which exhibited a statistically significant positive tBSR (β = 0.006, p = 0.009).

Fig. 3

A forest plot of standardized posterior means and associated 95% credible intervals (CI) for the predictor variables used in models of (A) birth sex ratio (BSR) and in the (B) temporal trend in birth sex ratio (tBSR) in both birds and mammals (84 and 306 species, respectively). Posterior means and SDs were obtained from the MCMCglm models. Sample size were 129 bird species, and 322 mammal species for the model that include IUCN status as predictor.