Adult sex ratios: causes of variation and implications for animal and human societies

Abstract

Converging lines of inquiry from across the social and biological sciences target the adult sex ratio (ASR; the proportion of males in the adult population) as a fundamental population-level determinant of behavior. The ASR, which indicates the relative number of potential mates to competitors in a population, frames the selective arena for competition, mate choice, and social interactions. Here we review a growing literature, focusing on methodological developments that sharpen knowledge of the demographic variables underlying ASR variation, experiments that enhance understanding of the consequences of ASR imbalance across societies, and phylogenetic analyses that provide novel insights into social evolution. We additionally highlight areas where research advances are expected to make accelerating contributions across the social sciences, evolutionary biology, and biodiversity conservation.

Fig. 1. Sex ratios at various life stages and their consequences.

Males (M) and females (F) flow through stages from birth (b) through development into juveniles (or subadults) for up to j time steps, maturation (m), and adulthood. Adults include newly mature individuals and individuals who reached sexual maturity at an earlier time. Adults are classified as breeders (br), nonbreeders (nbr) that are capable of breeding but at present are not reproductively active, and post-reproductive individuals (pr) that are senescent. Transitions between stages are shown with white arrows and within stages with black arrows. The number of females and males, respectively, are depicted at birth (F_b and M_b), one (F_b+1 and M_b+1) and j time steps later (F_b+j and M_b+j), at maturation (F_m and M_m), breeding (F_br and M_br), non-breeding (F_nbr and M_nbr) and post-reproduction (F_pr and M_pr). Different sex ratios emerge from various combination of the sexes at different stages: (1) Birth sex ratio = M_b / (F_b + M_b); (2) Juvenile sex ratio = (M_b+1 + M_b+j) / (F_b+1 + F_b+j + M_b+1 + M_b+j); (3) Maturation sex ratio (MSR) = M_m / (F_m + M_m); and (4) Adult sex ratio (ASR) = (M_m + M_nb + M_br + M_pr) / (F_m + F_nb + F_br + F_pr + M_m + M_nb + M_br + M_pr). Consequences of sex ratios discussed in the paper are shown.

Fig. 2. Causes of ASR variation in grayling, shorebirds, and humans.

a Adult sex ratios link to climate change in grayling of Lake Thun, Switzerland: male-biased adult sex ratios during spawning period and average yearly water temperatures at the spawning site. The transition from the red to the green background indicates the average yearly adult sex ratio from 1948 to 1992. These adults were on average five years old, and the gray shading highlights the 5-year period after the global temperature regime shift in 1987/88. b ASR and demographic parameters in three plover species (Charadrius spp): hatchling and adult sex ratios (round symbols; means and 95% CI) and sex-specific juvenile and adult survival (medians, quartiles, and ranges). c Sex ratios and proportions of death by sex across human age groups presented for homicides, infections/parasitic deaths, and all causes (US Census data 2009–2011). Drawings by Lara Wedekind using data from refs. ^,.

Fig. 3. Condition-dependent sex determination and sex change.

a Density-dependent sex determination potentially affecting ASR in (1) the nematode Romanomermis culicivorax, (2) temperate eels, (3) the pejerrey, (4) the brook lamprey, (5) the European sea bass and (6) the zebrafish Danio rerio. In all the above-mentioned species, more males are produced at high density. b Socially induced sex change occurs in various species such as (7) protandrous clownfishes, protogynous (8) wrasses (e.g., Thalassoma bifasciatum) and (9) Potter’s angelfish as-well as bi-directional sex change as exemplified in (10) the blue-banded goby. Other examples of socially controlled sex change were observed in both crustaceans and amphibians: (11) Northern shrimp exhibit protandrous sex change that occurs at small size when the density of females in the population is high. Protogynous sex change was also observed in (12) captive reed frogs and its occurrence is linked to local male density. Hence, for most sex changing species, those individuals that do not change sex are more numerous. Note that the direction of the arrow in the right panel (b) indicates the direction of sex change: orange from male to female (protandrous) and maroon from female to male (protogynous). Drawing by Pierre Lopez (MARBEC) based on data from refs. ^–,.

Fig. 4. Adult sex ratio variation and its implications for mating systems.

a Small populations, such as human hunter-gatherers, are particularly susceptible to variation in partner availability which can result in flexible, yet fragile, pair-bonds (e.g., Savanna Pumé, credit: R.D. Greaves); b polygyny and male size dimorphism are common among species with female excess (e.g., mountain gorilla, credit: A. H. Harcourt); c monogamy and biparental care are characteristic of even sex ratios and slight male excess across many species (e.g., Laysan albatross, credit: A. Badyaev); d as male-bias in the adult sex ratio becomes even more dramatic, polyandry, female-biased sexual dimorphism and sex-role reversal are common (e.g., African jacana, credit: T. Székely).

Fig. 5. Spatial and temporal variation in ASR.

Every social group may have different number of adult females (red circles) and males (blue circles). A group’s ASR will change as a result of deaths, maturations, emigrations and immigrations over time, and neighboring groups of a population often have different ASRs. Adults may move between groups, and local ASR may trigger these movements^,. The average ASR may vary across populations of the same species. This variation also raises the questions whether the current local or the average long-term population- or species-specific ASR underly variation in social behavior and how animals perceive the relevant sex ratio.