Life History Trade-Offs and Behavioral Sensitivity to Testosterone: An Experimental Test When Female Aggression and Maternal Care Co-Occur

Abstract

Research on male animals suggests that the hormone testosterone plays a central role in mediating the trade-off between mating effort and parental effort. However, the direct links between testosterone, intrasexual aggression and parental care are remarkably mixed across species. Previous attempts to reconcile these patterns suggest that selection favors behavioral insensitivity to testosterone when paternal care is essential to reproductive success and when breeding seasons are especially short. Females also secrete testosterone, though the degree to which similar testosterone-mediated trade-offs occur in females is much less clear. Here, I ask whether testosterone mediates trade-offs between aggression and incubation in females, and whether patterns of female sensitivity to testosterone relate to female life history, as is often the case in males. I experimentally elevated testosterone in free-living, incubating female tree swallows (Tachycineta bicolor), a songbird with a short breeding season during which female incubation and intrasexual aggression are both essential to female reproductive success. Testosterone-treated females showed significantly elevated aggression, reduced incubation temperatures, and reduced hatching success, relative to controls. Thus, prolonged testosterone elevation during incubation was detrimental to reproductive success, but females nonetheless showed behavioral sensitivity to testosterone. These findings suggest that the relative importance of both mating effort and parental effort may be central to understanding patterns of behavioral sensitivity in both sexes.

Estrogen receptor α polymorphism in a species with alternative behavioral phenotypes

“…This life-history tradeoff is believed to be mediated in part by T, which increases singing and mate-finding and decreases parental behavior in many seasonally breeding sparrows (27)(28)(29)(30). In free-living populations of white-throated sparrows, plasma T levels are higher in WS birds (7,8), which have the ZAL2 m rearrangement, than in TS birds, which do not (2,31).…”

Determinants of making success in female Tree Swallows (Tachycineta Bicolor)

“…These results are similar to a previous study in tree swallows that experimentally elevated T levels of females during incubation and reported cooler nest temperatures and complete hatching failure (Rosvall, 2013). Female great tits implanted with T during nest building also had lower incubation temperatures and hatching success (de Jong et al, 2016), but such negative effects of T on incubation behaviour were not observed in female dark-eyed juncos implanted prior to breeding (Clotfelter et al, 2004).…”

“…T has been shown to have masculinizing effects on female traits in a variety of taxa, although whether such changes reduce their attractiveness to potential mates is unclear (Ketterson et al, 2005;Lahaye et al, 2013). Given that exogenous T increases aggressive behaviour in female tree swallows (Rosvall, 2013), in my study T-treated female tree swallows likely spent more time involved in aggressive interactions and territory defence, as previously suggested for spotless starlings (García-Vigón et al, 2008), rather than seeking extra-pair copulations.…”

“…In addition, sexual behaviour of females may enhance the opportunity for engaging in extra-pair copulations; for example, during the fertile period, female humans (Homo sapiens) have greater desire or interest in extra-pair mates (e.g., Gangestad et al, 2002;Gangestad et al, 2005). Experimentally elevating T concentrations increases aggressive behaviour in female birds (Zysling et al, 2006;Sandell, 2007;Rosvall, 2013) and sexual interest, libido and behaviour in humans (reviewed in Bolour and Braunstein, 2005); however, studies investigating whether elevated T mediates extra-pair copulation behaviour in female birds have produced mixed results. T-treated female dark-eyed juncos (Junco hyemalis) did not differ from control females in the proportion of extra-pair offspring in their nests (Gerlach and Ketterson, 2013), whereas extra-pair paternity was lower for T-treated female spotless starlings (Sturnus unicolor) and blue tits (Cyanistes caeruleus) when compared to control females (García-Vigón et al, 2008;de Jong, 2013, respectively).…”

“…As far as I am aware, the combined use of ATD+F has not been employed previously to examine how T-mediated behaviour influences extra-pair paternity in female birds. If extrapair copulation behaviour of female tree swallows is correlated with the expression of aggressive or sexual behaviour and is mediated by T and its estrogenic metabolites, then I predicted that T-treated females would have a greater proportion of extra-pair offspring in their broods than females in the ATD+F and control treatments as a result of being more aggressive (Rosvall 2013) or having greater sexual interest in extra-pair mates. In contrast, I…”