Kristal E. Cain

Competitive females are successful females; phenotype, mechanism, and selection in a common songbird

In a variety of taxa, male reproductive success is positively related to the expression of costly traits such as large body size, ornaments, armaments, and aggression. These traits are thought to improve male competitive ability and, thus, access to limited reproductive resources. Females of many species also express competitive traits. However, we know very little about the consequences of individual variation in competitive traits and the mechanisms that regulate their expression in females. Consequently, it is currently unclear whether females express competitive traits owing to direct selection or as an indirect result of selection on males. Here, we examine females of a mildly dimorphic songbird (Junco hyemalis) to determine whether females show positive covariance in traits (morphology and behavior) that may be important in a competition. We also examine whether trait expression relates either to testosterone (T) in terms of mechanism or to reproductive success in terms of function. We found that larger females were more aggressive and that greater ability to produce T in response to a physiological challenge consisting of a standardized injection of gonadotropin-releasing hormone predicted some measures of female body size and aggression. Finally, we found that aggressive females had greater reproductive success. We conclude that T may influence female phenotype and that females may benefit from expressing a competitive phenotype. We also suggest that the mild dimorphism observed in many species may be due in part to direct selection on females rather than simply a correlated response to selection in males.

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Costs and Benefits of Competitive Traits in Females: Aggression, Maternal Care and Reproductive Success

Recent research has shown that female expression of competitive traits can be advantageous, providing greater access to limited reproductive resources. In males increased competitive trait expression often comes at a cost, e.g. trading off with parental effort. However, it is currently unclear whether, and to what extent, females also face such tradeoffs, whether the costs associated with that tradeoff overwhelm the potential benefits of resource acquisition, and how environmental factors might alter those relationships. To address this gap, we examine the relationships between aggression, maternal effort, offspring quality and reproductive success in a common songbird, the dark-eyed junco (Junco hyemalis), over two breeding seasons. We found that compared to less aggressive females, more aggressive females spent less time brooding nestlings, but fed nestlings more frequently. In the year with better breeding conditions, more aggressive females produced smaller eggs and lighter hatchlings, but in the year with poorer breeding conditions they produced larger eggs and achieved greater nest success. There was no relationship between aggression and nestling mass after hatch day in either year. These findings suggest that though females appear to tradeoff competitive ability with some forms of maternal care, the costs may be less than previously thought. Further, the observed year effects suggest that costs and benefits vary according to environmental variables, which may help to account for variation in the level of trait expression.

Female and male song rates across breeding stage: Testing for sexual and nonsexual functions of female song

As a textbook example of a sexually selected trait, song in male birds has been extensively examined in the context of female mate choice and male–male competition for access to mates. Female song is also phylogenetically widespread, and probably ancestral. However, we know relatively little about when and why females sing. Female song may be important for female–male communication, e.g. fertility advertisement, mate attraction or coordinating the care of young. Alternatively, female song may function in the context of female–female competition for reproductive resources, e.g. nest sites, year-round territories or parental assistance. We quantified spontaneous song, and song in response to playback of an unfamiliar female song, in female and male superb fairy-wrens, Malurus cyaneus, across breeding stages. We found that females and males sang with roughly equal frequency spontaneously; however, females sang much more frequently than males in response to playback of unfamiliar female song. We found no difference in song rates across breeding stage, and no effect of age or the presence of subordinates. In both sexes, song rates increased slightly across the breeding season. Female song rates were also repeatable across the season. Overall, the results suggest that although female song is likely to be a multipurpose trait, as in males, the primary function in superb fairy-wrens appears to be female–female competition.

Female song rates in response to simulated intruder are positively related to reproductive success

Bird song is well studied in males as a sexually selected behavior. However, although song is also common among females, it is infrequently examined and poorly understood. Research suggests that song is often used as a resource defense behavior and is important in female-female competition for limited resources, e.g. mates and territories. If so, song should be positively related to fitness and related to other resource defense behaviors, but this possibility has rarely been explored. Here we examine fitness estimates in relation to spontaneous song rates and song rates in response to a simulated intruder (playback), in the superb fairy-wren (Malurus cyaneus), a cooperatively breeding songbird. We also determine how song rates relate to other territorial defense behaviors. Song rate in response to playback, but not spontaneous song rate, was positively related to nest success and the number of fledglings produced by successful females. Further, response song rate was also correlated with other territorial defense behaviors (latency to respond and flights). This evidence supports the hypothesis that female song may be used in the context of female-female competition to improve access to limited reproductive resources, and suggests that song may provide direct fitness benefits.

Next steps for understanding the selective relevance of female-female competition

INTRODUCTION After decades of neglect, recent empirical research on exaggerated female traits (e.g., ornaments, armaments, aggression, acoustic signals, etc.) has revived interest in this widespread but poorly understood phenomenon, and shown that these traits often function in the context of femalefemale competition (West-Eberhard, 1983; Amundsen, 2000; Clutton-Brock, 2009; Rosvall, 2011a; Stockley and BroJorgensen, 2011; Rubenstein, 2012 [Theme issue]; Stockley and Campbell, 2013 [Theme issue]). However, recent reviews have emphasized the applicability of sexual vs. social selection, rather than rigorously examining the role of different ecological contexts in shaping the evolution of traits used in competitive contexts (hereafter, “competitive traits”) in females. Thus, we still lack a solid understanding of the ecological and evolutionary mechanisms driving the evolution of female trait expression, in particular whether, how, and why these mechanisms vary among species, and between the sexes. It is our opinion that two critical issues impede our understanding the evolution of competitive traits in females. (1) The field has yet to investigate the ecological and evolutionary mechanisms that underlie interspecific and intersexual variation in the expression of these traits. This is perhaps due to a perceived “apples and oranges” problem stemming from the observation that animals compete over a wide variety of resources that vary by species or sex. However, by focusing on the relationships between fitness currencies and the resources over which animals compete, we can empirically compare the strength and direction of selection across species and sexes. (2) To date, research has primarily focused on the fitness costs or benefits of female competitive traits. As with many questions in behavioral and evolutionary ecology, quantifying how costs and benefits interact is essential to furthering our understanding of the evolution of competitive traits. Here, our goal is to draw attention to these solutions in order to spur more efficient and transformative progress.

Individual variation in testosterone and parental care in a female songbird; The dark-eyed junco (Junco hyemalis)

When competition for sex-specific resources overlaps in time with offspring production and care, trade-offs can occur. Steroid hormones, particularly testosterone (T), play a crucial role in mediating such trade-offs in males, often increasing competitive behaviors while decreasing paternal behavior. Recent research has shown that females also face such trade-offs; however, we know little about the role of T in mediating female phenotypes in general, and the role of T in mediating trade-offs in females in particular. Here we examine the relationship between individual variation in maternal effort and endogenous T in the dark-eyed junco, a common songbird. Specifically, we measure circulating T before and after a physiological challenge (injection of gonadotropin releasing hormone, GnRH), and determine whether either measure is related to provisioning, brooding, or the amount of T sequestered in egg yolk. We found that females producing more T in response to a challenge spent less time brooding nestlings, but provisioned nestlings more frequently, and deposited more T in their eggs. These findings suggest that, while T is likely important in mediating maternal phenotypes and female life history tradeoffs, the direction of the relationships between T and phenotype may differ from what is generally observed in males, and that high levels of endogenous T are not necessarily as costly as previous work might suggest.

Female song and aggression show contrasting relationships to reproductive success when habitat quality differs

Though well studied in males, little is known about the factors influencing variation in expression of exaggerated traits such as intense aggression, elaborate ornaments, and lethal weaponry in females. Current research suggests that these traits are important when females compete for access to limited reproductive resources and that greater trait expression leads to higher reproductive success. However, contest theory predicts that differences in resource availability will alter the costs and benefits of competition and contest rules, potentially changing the strength or direction of selection. Female superb fairy-wrens, a common Australian passerine, compete for exclusive breeding territories using song and aggression. A previous study in a population residing in uniform, high-quality habitat found that strong responses to a simulated intruder were associated with improved reproductive success. Here, we determine whether differences in resource availability, i.e., habitat quality, are associated with changes to this relationship by replicating this study in a second population that resides in lower-quality, patchy habitat. We quantified female response (activity and song rates) to a simulated same-sex intruder and examine the relationships with territory quality and annual reproductive success. Contrary to previous research, we found that in low-quality, patchy habitat, stronger responders occupied poorer quality territories and had lower reproductive success. However, basal song rates and responses to an intruder were overall much stronger in low-quality habitat. These results suggest that female–female contest rules and the intensity of competition differ according to resource availability, which may alter how selection acts on female competitive traits.Significance statementFemales appear to use costly social traits, e.g., ornaments, armaments, complex song, and aggression, in the context of female–female competition for limited resources. However, very little is known about how changes in resource availability might alter female–female contest rules or the relationship between trait expression and fitness estimates. Previous research in a population of superb fairy-wren, a songbird, residing in high-quality habitat, found that female song and aggression were positively related to reproductive success. Here, we replicate that study in a population that resides in low-quality, patchy habitat. We found higher levels of aggression and song and that the relationship between behavior and fitness was in the opposite direction. This suggests that resource availability can affect female behavior, dramatically alter the strength and direction of selection, and may change the rules that females observe when engaging in contests.

Testosterone production in response to exogenous gonadotropin releasing hormone (GnRH challenge) depends on social environment and color polymorphism

Testosterone is an important mediator of behavior, morphology and physiology. A cascade of signals regulates the amount of testosterone (T) circulating in the plasma; in response to stimulus the hypothalamus releases gonadotropin-releasing hormone (GnRH), which triggers secretion of gonadotropins from the pituitary, stimulating the synthesis and release of T from the gonads. Previous work has shown that changes to the social environment can alter circulating T-levels, which may have important fitness consequences, but it is currently unclear whether these changes are due to alterations in the signal from the brain, or changes in the ability of the pituitary and gonads to respond to this signal. Further, the strength and direction of response to a changing environment may differ according to life-history strategy. Species with genetically determined alternative strategies offer a pathway for examining these differences. Here we use a finch with a genetically determined polymorphism, the Gouldian finch (Erythrura gouldiae), to determine whether T-levels change in response to social environment. We also use injections of GnRH to determine whether these changes are due to alterations in the ability of the pituitary and gonads to respond to this signal. We found that social environment (presence of females) had a rapid effect on male circulating T-levels, and that this difference was reflected in responsiveness to GnRH. We observed no overall morph differences in T-levels, but we did observe morph differences in the pattern of T secretion across environments, and morph differences in the repeatability of T-levels across time and environment.

Habitat structure is linked to the evolution of plumage colour in female, but not male, fairy-wrens

BackgroundBoth natural and sexual selection may drive the evolution of plumage colouration in birds. This can lead to great variation in plumage not only across species, but also between sexes within species. Australasian fairy-wrens are famous for their brightly coloured males, which exhibit colours ranging from bright blue to red and black. Female plumage in fairy wrens (and in general) has been rarely studied, but it can also be highly variable, including both bright and cryptic plumages. We use a comparative framework to explore the basis for this variation, and test the possibility that female fairy-wrens experience selection for cryptic plumage when they occupy more exposed habitats that offer little concealment from predators. We use spectral measurements of plumage for species and subspecies of Australasian fairy-wrens.ResultsWe show that female colouration (contrast against background) is strongly correlated with vegetation cover: females in open habitats show less contrast to background colours than females in closed habitats, while male colouration is not associated with habitat type.ConclusionsFemale plumage appears to be under stronger natural selection than male plumage in fairy-wrens, providing an example of how selection may act differently on males and females of the same species.