Sex ratio bias, male aggression, and population collapse in lizards

Abstract

The adult sex ratio (ASR) is a key parameter of the demography of human and other animal populations, yet the causes of variation in ASR, how individuals respond to this variation, and how their response feeds back into population dynamics remain poorly understood. A prevalent hypothesis is that ASR is regulated by intrasexual competition, which would cause more mortality or emigration in the sex of increasing frequency. Our experimental manipulation of populations of the common lizard (Lacerta vivipara) shows the opposite effect. Male mortality and emigration are not higher under male-biased ASR. Rather, an excess of adult males begets aggression toward adult females, whose survival and fecundity drop, along with their emigration rate. The ensuing prediction that adult male skew should be amplified and total population size should decline is supported by long-term data. Numerical projections show that this amplifying effect causes a major risk of population extinction. In general, such an "evolutionary trap" toward extinction threatens populations in which there is a substantial mating cost for females, and environmental changes or management practices skew the ASR toward males.

Fig. 1.

Demographic consequences of the adult sex ratio manipulation. MB, male-biased populations; FB, female-biased populations. Numbers above the error bars indicate sample size. (A) Emigration probability in adults before hibernation (mean ± SE) per sex in each treatment. For details on statistics, see text. (B) Annual survival probability (mean ± SE) per age class (circle, juveniles; triangles, yearlings; squares, adults) and sex in each treatment. For details on statistics, see Table 1. (C) Frequency distribution of the fecundity (number of offspring that successfully hatched) in each treatment. The difference between treatments is significant (Poisson regression, treatment: F_1,10 = 10.24, P = 0.009; effect of age: F_2,110 = 16.40, P < 0.0001; age × treatment: F_2,108 = 0.08, P = 0.92). Arrows indicate least-square mean per treatment after controlling for differences among age classes and populations.

Fig. 2.

Mean snout-vent length (±SE) of females in relation to treatment, age class (circle, juveniles; triangles, yearlings; squares, adults), and period. Filled symbols, male-biased populations; open symbols, female-biased populations. The trajectory of female body size was modeled with a repeated-measures model, with the measures taken at release, in August 2002, and in June 2003 as repeats. Body size was not affected by the treatment (F_1,10 = 1.73, P = 0.22), and the two-way interactions of treatment with time (F_1,457 = 0.06, P = 0.81), and age class (F_2,458 = 1.38, P = 0.25), as well as the three-way interaction (F_2,455 = 0.85, P = 0.43) were not significant. Growth rates differed among age classes (F_2,460 = 718.60, P < 0.0001)

Fig. 3.

Adult sex ratio, male aggression, and population extinction risk. See supporting information for model construction and analysis and all parameter values. (A) Cumulated extinction probability over time of an isolated population, as predicted by a one-sex model, a two sex-model without male aggression, and a two-sex model with male aggression. Filled symbols, initially male-biased populations; open symbols, initially female-biased populations. (B) Demographic dynamics during extinction in the two-sex model with male aggression, as predicted for an isolated, initially female-biased population. Data shown are population size (scaled to its initial value), yearling and adult sex ratio, yearling and adult female survival, and recruitment (number of female offspring per female) conditional on nonextinction (2). (C) Cumulated extinction probability over time as predicted by a two-sex metapopulation model in the absence of male aggression, with male aggression and random emigration, or with male aggression and female emigration in response to higher local density of females. All results are based on Monte Carlo simulations of 2,000 trajectories. Filled symbols, initially male-biased populations; open symbols, initially female-biased populations. (D) Evolutionary trap: nonmonotonic response of median persistence time (Monte Carlo simulations of 2,000 extinct trajectories) to increasing adult male survival as predicted by a two-sex metapopulation model with male aggression and female emigration in response to higher local density of females. Population viability is maximized for adult male survival probabilities similar to the ones observed in wild populations from which the lizards originated (15). Population viability is also higher when the initial ASR is female-biased.