Male twins reduce fitness of female co-twins in humans

Abstract

In mammals, including humans, female fetuses that are exposed to testosterone from adjacent male fetuses in utero can have masculinized anatomy and behavior. However, the reproductive consequences of such prebirth sex-ratio effects for offspring and their implications for maternal fitness remain unexplored. Here we investigate the effects of being gestated with a male co-twin for daughter lifetime reproductive success, and the fitness consequences for mothers of producing mixed-sex twins in preindustrial (1734-1888) Finns. We show that daughters born with a male co-twin have reduced lifetime reproductive success compared to those born with a female co-twin. This reduction arises because such daughters have decreased probabilities of marrying as well as reduced fecundity. Mothers who produce opposite-sex twins consequently have fewer grandchildren (and hence lower fitness) than mothers who produce same-sex twins. Our results are unlikely to be a consequence of females born with male co-twins receiving less nutrition because such females do not have reduced survival and increases in food availability fail to improve their reproductive success. Nor are our results explained by after-birth social factors (females growing up with similarly aged brothers) because females born with a male co-twin have reduced success even when their co-twin dies shortly after birth and are raised as singletons after birth. Our findings suggest that hormonal interactions between opposite-sex fetuses known to influence female morphology and behavior can also have negative effects on daughter fecundity and, hence, maternal fitness, and bear significant implications for adaptive sex allocation in mammals.

Fig. 1.

Effect of having a same-sex versus opposite-sex co-twin for female (white bars) and male (gray bars) fitness in premodern Finland. (A) Probability of reproducing in one's lifetime. (B) Lifetime reproductive success measured as the total number of offspring raised to adulthood (age 15 years). FF, females from female–female twin births; FM, females from female–male twin births; MM, males from male–male twin births; MF, males from male–female twin births. Bars indicate predicted means (±1 SE); numbers above the bars indicate sample sizes. Note that the true difference in final fitness between FM and FF females will be even larger than shown in B, given that unmarried women (who were more likely to be FM) with zero numbers of children were not included in the analyses of the effects of having a same- versus opposite-sex co-twin on the numbers of children born and raised.

Fig. 2.

Effects of having a same- versus opposite-sex co-twin for female (white bars) and male (gray bars) underlying life-history traits responsible for differences in fitness in Fig. 1. (A) Probability of ever marrying in a lifetime. (B) Lifetime fecundity measured as the total number of offspring delivered. Analyses for the effects on marriage probability only include individuals who survived to the age in which 90% of individuals in a population were married, if they were ever to marry in their lifetime (30 years). FF, females from female–female twin births; FM, females from female–male twin births; MM, males from male–male twin births; MF, males from male–female twin births. Bars indicate predicted means (±1 SE); numbers above the bars indicate sample sizes.

Fig. 3.

Effect of the death of a co-twin within 3 months after birth on the fitness of the survivor. (A) Lifetime fecundity. (B) Lifetime reproductive success of twin females raised as singletons since birth, but born with a same-sex (FF) or opposite-sex (FM) co-twin. Bars indicate predicted means (±1 SE); numbers above bars indicate sample sizes.

Fig. 4.

Effect of producing same- versus mixed-sex twins on the mother's fitness, measured as the number of grandchildren produced by her offspring (controlling for differing numbers of offspring raised to adulthood). Bars indicate predicted means (±1 SE); numbers above bars indicate sample sizes.