title: 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.
authors.affiliation: Department of Anthropology, The George Washington University, Washington, District of Columbia. bradleyjbrenda@gwu.edu.|Department of Anthropology, Yale University, New Haven, Connecticut. bradleyjbrenda@gwu.edu.
authors.forename: Brenda J
authors.initials: BJ
authors.lastname: Bradley
authors.affiliation: Department of Psychology, University of Wisconsin, Madison, Wisconsin.
authors.forename: Charles T
authors.initials: CT
authors.lastname: Snowdon
authors.affiliation: Department of Archaeology & Anthropology, University of Cambridge, Cambridge, United Kingdom.
authors.forename: William C
authors.initials: WC
authors.lastname: McGrew
authors.affiliation: Department of Sociology and Anthropology, James Madison University, Harrisonburg, Virginia.
authors.forename: Richard R
authors.initials: RR
authors.lastname: Lawler
authors.affiliation: Department of Anthropology, Yale University, New Haven, Connecticut.
authors.forename: Elaine E
authors.initials: EE
authors.lastname: Guevara
authors.affiliation: Department of Anthropology, Yale University, New Haven, Connecticut.
authors.forename: Annick
authors.initials: A
authors.lastname: McIntosh
authors.affiliation: Institute for Genome Sciences and Program in Personalized and Genomic Medicine, University of Maryland School of Medicine, Baltimore, Maryland.|University of Maryland at College Park, College Park, Maryland.
authors.forename: Timothy
authors.initials: T
authors.lastname: O'Connor
mesh_terms: D000728:Androgens / Q000502:physiology*; D000818:Animals; D005260:Female; D008098:Litter Size; D008297:Male; D008322:Mammals; D011247:Pregnancy; D011297:Prenatal Exposure Delayed Effects; D011323:Primates / Q000502:physiology*; D012098:Reproduction; D012744:Sex Ratio
chemical_list: D000728:Androgens
keywords: CYP19A1; aromatase; callitrichid; strepsirrhine; testosterone; twins