Non‐human primates avoid the detrimental effects of prenatal androgen exposure in mixed‐sex litters: combined demographic, behavioral, and genetic analyses

Abstract

Producing single versus multiple births has important life history trade-offs, including the potential benefits and risks of sharing a common in utero environment. Sex hormones can diffuse through amniotic fluid and fetal membranes, and females with male littermates risk exposure to high levels of fetal testosterone, which are shown to have masculinizing effects and negative fitness consequences in many mammals. Whereas most primates give birth to single offspring, several New World monkey and strepsirrhine species regularly give birth to small litters. We examined whether neonatal testosterone exposure might be detrimental to females in mixed-sex litters by compiling data from long-term breeding records for seven primate species (Saguinus oedipus; Varecia variegata, Varecia rubra, Microcebus murinis, Mirza coquereli, Cheirogaleus medius, Galago moholi). Litter sex ratios did not differ from the expected 1:2:1 (MM:MF:FF for twins) and 1:2:2:1 (MMM:MMF:MFF:FFF for triplets). Measures of reproductive success, including female survivorship, offspring-survivorship, and inter-birth interval, did not differ between females born in mixed-sex versus all-female litters, indicating that litter-producing non-human primates, unlike humans and rodents, show no signs of detrimental effects from androgen exposure in mixed sex litters. Although we found no evidence for CYP19A1 gene duplications-a hypothesized mechanism for coping with androgen exposure-aromatase protein evolution shows patterns of convergence among litter-producing taxa. That some primates have effectively found a way to circumvent a major cost of multiple births has implications for understanding variation in litter size and life history strategies across mammals.

A comparative study of litter size and sex composition in a large dataset of callitrichine monkeys

“…We did not detect survival or reproductive costs of being born into a mixed‐sex litter for either males or females (Figure S1). This finding recapitulates a growing literature which espouses that callitrichines, unlike other litter‐bearing mammals (Hackländer & Arnold, ; Korsten, Clutton‐Brock, Pilkington, Pemberton, & Kruuk, ; Monclús & Blumstein, ; Ryan & Vandenbergh, ), have evolved mechanisms which shield females from brother‐derived masculinization (Bradley et al, ; French et al, ). This is true even in wild golden lion tamarins ( L. rosalia ): individuals from mixed‐sex litters were indistinguishable from those from isosexual litters in several morphological (growth to maturity and adult body size), survival (lifetime survivorship), and reproductive metrics (age at first reproduction, reproductive rates, and reproductive tenures; Frye, B.M., Hankerson, Sears, Tardif, & Dietz, n.d.).…”

“…However, in some species (i.e., Callithrix jacchus ), captive mothers routinely produce larger litters because of excess energy stores, which impacts ovulation dynamics (Tardif, Layne, & Smucny, ). The sex composition of litters also may mediate individuals' developmental outcomes—for example, via exposure to sex hormones produced by males—but the overall evidence of such sex‐related effects on development remains mixed (Bradley et al, ; De Moura, ; French et al, ; Frye, Rapaport, Melber, Sears, & Tardif, ; Rutherford, DeMartelly, Layne Colon, Ross, & Tardif, ).…”

Sibling sex, but not androgens, shapes phenotypes in perinatal common marmosets (Callithrix jacchus)

“…The few investigations that have assessed the developmental sequelae of prenatal androgen exposure in litter-bearing primates have yielded mixed results. Litter effects were largely negligible in eight callitrichine and strepsirrhine species (i.e., Leontopithecus rosalia , Saguinus oedipus , Varecia variegata , Varecia rubra , Microcebus murinis , Mirza coquereli , Cheirogaleus medius , and Galago moholi 30,31 ). Others (i.e., Callithrix jacchus and Leontopithecus rosalia ), though, exhibited some evidence of sex-dependent fetal interactions 31,32 .…”

Cortisol advantage of neighbouring the opposite sex in utero

“…Other advantages to opposite-sex twins in humans are heavier birth weight [ 12 , 59 ], at least for males [ 60 ], and longer gestation [ 61 ], perhaps owing to the tendency of female fetuses to have longer gestations [ 61 ]. In cotton-top tamarins ( Saguinus oedipus ), male twins had significantly lower survival rates than those born in male–female litters [ 62 ]. However, in other systems, opposite-sex co-twins can have adverse effects.…”