Maternal glucocorticoid levels affect sex allocation in black howler monkeys

Abstract

When sons and daughters impart different fitness benefits, mothers should bias investment according to offspring sex, in some cases modifying offspring sex ratios. Sex allocation in monotocous organisms is expected to be costlier than for polytocous species, as it imposes a greater loss of reproductive effort in terms of mating and fertilization. Here, we show that variation in glucocorticoid concentrations around the time of conception predicts infant sex in a monotocous anthropoid, the black howler monkey (Alouatta pigra), suggesting that sex allocation is linked to a hormonal mechanism that affects early embryonic development. Glucocorticoids signal environmental conditions, and in our study, their variation was positively related to factors affecting infant survival. These results offer insight into sex allocation strategies in monotocous organisms.

Factors influencing infant sex ratio in howler monkeys (Alouatta spp.): A literature review and analysis

“…Although there is growing evidence that fathers can affect infant sex ratios (e.g., Edwards & Cameron, ; Lavoie, Tedeschi, García‐González, & Firman, ; Tanaka, Fukano, & Nakamura, ; reviewed in Douhard, ), variation in mammalian infant sex ratios has been found to be mostly linked to maternal physical condition, proxied by age (e.g., Martin & Festa‐Bianchet, ; Packer, Collins, & Eberly, ; Saltz, ), body mass (e.g., Borowik & Jędrzejewska, ), access to food resources (e.g., Schwanz & Robert, ), dominance rank (e.g., Schino, ; van Schaik & Hrdy, ), occurrence of lactation at the time of conception (e.g., Dias, Coyohua‐Fuentes, Canales‐Espinosa, & Rangel‐Negrín, ; Rutberg, ), rainfall (e.g., Kruuk, Clutton‐Brock, Albon, Pemberton, & Guinness, ; Law, Fike, & Lent, ), or sex of preceding offspring (e.g., Hogg, Hass, & Jenni, ). It is assumed that these factors affect maternal reproductive physiology, and thus, sex allocation, an assumption now supported by the observation of covariation between maternal glucose or hormonal concentrations and offspring sex (Cameron, Lemons, Bateman, & Bennett, ; Gutiérrez‐Adán, Granados, Pintado, & De la Fuente, ; Rangel‐Negrín, Coyohua‐Fuentes, Canales‐Espinosa, Chavira‐Ramírez, & Dias, ; Ryan et al, ). Ultimately, variation in infant sex ratios is expected when fitness returns vary between sexes and parents are able to couple offspring sex with investment potential and local conditions (Altmann & Altmann, ; Clark, ; Trivers & Willard, ; but see Booksmythe, Mautz, Davis, Nakagawa, & Jennions, ; Cockburn, Legge, & Double, ).…”

“…Longitudinal surveys of ursine ( Alouatta arctoidea ; 8 years) and brown ( Alouatta guariba ; 4 years) howler monkey populations indicate that infant sex ratio tends to unity (0.9 sons per daughter: Crockett & Rudran, ; Strier, Mendes, & Santos, ), whereas in black howler monkeys ( Alouatta pigra ; 7 years) it is skewed in favor of sons (1.7: Dias et al, ). In black howler monkeys, sons are born more often to mothers with higher glucocorticoid hormone metabolite concentrations around the time of conception (Rangel‐Negrín, Coyohua‐Fuentes, Canales‐Espinosa, et al, ). This association appears to be mediated by environmental conditions, such that fewer daughters are born to mothers living in anthropogenically disturbed habitats.…”

“…This association appears to be mediated by environmental conditions, such that fewer daughters are born to mothers living in anthropogenically disturbed habitats. In disturbed habitats, sons are produced more than daughters (Rangel‐Negrín, Coyohua‐Fuentes, Canales‐Espinosa, et al, ). A bias toward the production of sons in disturbed habitats supports the Local Resource Competition hypothesis for sex allocation (Clark, ) as sons are more likely to disperse than daughters (Rangel‐Negrín, Coyohua‐Fuentes, Canales‐Espinosa, et al, ) and disturbed habitats may have lower food availability and thus increased food competition.…”

“…In disturbed habitats, sons are produced more than daughters (Rangel‐Negrín, Coyohua‐Fuentes, Canales‐Espinosa, et al, ). A bias toward the production of sons in disturbed habitats supports the Local Resource Competition hypothesis for sex allocation (Clark, ) as sons are more likely to disperse than daughters (Rangel‐Negrín, Coyohua‐Fuentes, Canales‐Espinosa, et al, ) and disturbed habitats may have lower food availability and thus increased food competition. In ursine howler monkeys, daughters are produced more than sons at low population densities (Crockett, ; Crockett & Pope, ; Rudran & Fernández‐Duque, ), supporting the Local Resource Enhancement hypothesis, as lower population densities are expected to reduce food competition.…”

“…Given that sex allocation is proximately affected by maternal physical condition (Cameron et al, ; Gutiérrez‐Adán et al, ; Rangel‐Negrín, Coyohua‐Fuentes, Canales‐Espinosa, et al, ; Ryan et al, ), we reviewed the literature to assess variation in infant sex ratio relative to maternal condition in howler monkeys. As there are very few data on the physical condition of female howler monkeys (Cano‐Huertes et al, ; Dias et al, ; Rangel‐Negrín, Coyohua‐Fuentes, Chavira‐Ramírez, Canales‐Espinosa, & Dias, ), we indexed maternal condition by annual rainfall and the potential for resource competition.…”