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.early conditions ͉ fetal testosterone ͉ reproductive success ͉ sex allocation ͉ sex ratio C onditions experienced before birth can have profound effects on the subsequent growth, survival, and reproductive capacity of individuals from a wide range of taxa (1, 2). For example, in humans, the quality and quantity of nutrition received in utero and/or the seasonal timing of birth have been shown to predict postnatal growth rates (3), the onset of chronic diseases in adulthood (4), longevity (5, 6), and reproductive success or fitness (7,8). Another, but less often considered, aspect of the early environment that can have significant downstream consequences for offspring is the amount of sex hormones (testosterones and estrogens) to which developing young are exposed (9-11).Testosterone and estrogen are fat-soluble steroids and therefore can be transported both in the bloodstream as well as by diffusion. Consequently, it is now well established that, in viviparous animals, sex hormones diffuse through fetal membranes and amniotic fluid, leading to fetuses receiving significant concentrations of sex hormones from their developing neighbors (9, 12). Such acquisition has been shown to have substantial consequences for individual morphology, physiology, and behavior across a wide range of wild, domesticated, and laboratory mammals, as well as in ...

Twins Less Frequent Than Expected Among Male Births in Risk Averse Populations

“…This circumstance intimates that self-reported risk aversion may predict selection in utero against the male twin sets more than mixed-sex pairs. Females from mixed-sex twin gestations exhibit lower fitness than those from same sex sets (Lummaa et al, 2007) implying that selection against males in mixed sex gestations may also be adaptive in threatening environments.…”

“…The fitness deficit of these gestations arises principally, although not solely (Lummaa et al, 2007), from relatively high rates of infant and child mortality among male twins born into threatening environments.…”

Twinning in humans: maternal heterogeneity in reproduction and survival

“…The few studies that have investigated the reproductive and lifehistory effects of twinning in natural fertility populations have conducted analyses with very small sample sizes (largest 250) [10,12,21,38,41,42,45,46] often yielding equivocal results. Using the largest dataset of twin mothers yet published, at least 18 times larger than any previously analysed historical sample, we have shown that mothers of twins surpass their singleton-only bearing counterparts on several life-history and reproductive measures.…”

Heritability and cross-sex genetic correlations of early-life circulating testosterone levels in a wild mammal

“…a positive genetic correlation [17]) would constrain either sex from reaching their optimum. Testosterone levels may also be important to sex-specific trait development in early life (see [18] and references therein). For example, neonatal male rats with suppressed testosterone develop feminized adult behaviour, whereas neonatal females exposed to high levels of testosterone are less receptive to males as adults [19].…”