Consequences of elevating plasma testosterone in females of a socially monogamous songbird: evidence of constraints on male evolution?

Clotfelter, Ethan D.; O'Neal, Dawn M.; Gaudioso, Jacqueline M; Casto, Joseph M.; Parker-Renga, Ian M; Snajdr, Eric; Duffy, Deborah L.; Nolan, Val; Ketterson, Ellen D.

doi:10.1016/j.yhbeh.2004.03.003

Cited by 145 publications

(133 citation statements)

References 36 publications

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“…They have been explored mainly in the field of sexual selection (e.g. Clotfelter et al 2004;McGlothlin et al 2004), but they are probably important in other contexts of functional differentiation of males and females (e.g. Temeles et al 2000).…”

Section: Discussionmentioning

confidence: 99%

Male behavioural maturation rate responds to selection on pollen hoarding in honeybees

2006

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Division of labour in social insect colonies relies on behavioural functional differentiation (specialization) of individuals with similar genomes. However, individual behavioural traits do not evolve independently of each other (behavioural syndromes). A prime example is the suite of behavioural differences in honeybee workers that has evolved in response to bidirectional selection on pollen hoarding of honeybee colonies (pollen-hoarding syndrome). More generally, these differences reflect functional differentiation between nectar and pollen foragers. We demonstrate here that this pollen-hoarding syndrome extends to drones. Similar to what has been shown in workers, drones from the high-pollen-hoarding strain had a higher locomotion activity after emergence, and they initiated flight earlier than did males derived from the low-pollen-hoarding strain, with hybrids intermediate. However, these two behavioural traits were unlinked at the individual level. We also found that social environment (the colony) affects the age at which drones initiate flight. The indirect selection responses of male behaviour suggest that male and worker evolution are not independent and may constrain each other's evolution. Furthermore, we identified three distinct peaks in the probability of flight initiation over the course of the experiment and a decreased phenotypic variability in the 'hybrid' males, contrary to quantitative genetic expectations.Social insects owe much of their evolutionary success to the coordinated action of behaviourally specialized members of their colonies (Oster & Wilson 1978; Winston 1987;Hölldobler & Wilson 1990). Division of labour is a hallmark of social evolution (Beshers & Fewell 2001), and among honeybee workers, it is mainly determined by age and genetic effects (Winston 1987). To promote individual specialization, the response thresholds to different task stimuli should vary independently among individuals (Beshers & Fewell 2001). This seems not to be the case: honeybees show well-established behavioural differences among races that extend to multiple behavioural phenotypes, as well as to morphology and life history (Winston 1987). Similar multiple behavioural phenotypes in honeybees are also correlated at the individual level (Page & Erber 2002;Pankiw 2003;Scheiner et al. 2004), indicating their evolution as behavioural syndromes (array of correlated behavioural characteristics: Sih et al. 2004). Linked sets of behavioural traits may have arisen through adaptation in certain contexts (Amdam et al. 2004), but the correlation among behavioural traits may constrain the division of labour in social insects, and behavioural optimization in general (Price & Langen 1992;Sih et al. 2004 One of the best-studied examples of behavioural syndromes in insects is the behavioural differentiation among workers of two strains of honeybees that have been bidirectionally selected over multiple generations for different amounts of pollen stored in their nests . Many different aspects of foraging behaviour Wadd...

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Section: Discussionmentioning

confidence: 99%

Male behavioural maturation rate responds to selection on pollen hoarding in honeybees

2006

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“…Measures of F 2 EPO and F 2 WPO production were calculated both for all returning females (so as to measure the contribution of each type of F 2 offspring to total reproductive success) and for females that produced at least one genotyped offspring (so as to compare the effect of F 1 paternity on F 2 paternity distribution). [26,30,31]. Because testosterone significantly increases reproductive success in males [26] and decreases reproductive success in females [30], we included the number of years an individual received a testosterone implant (as the percentage of total breeding tenure; '%T years') as a covariate in all analyses of reproductive performance based on paternity.…”

Section: (A) Field Methodsmentioning

confidence: 99%

Promiscuous mating produces offspring with higher lifetime fitness

et al. 2011

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In many species, each female pairs with a single male for the purpose of rearing offspring, but may also engage in extra-pair copulations. Despite the prevalence of such promiscuity, whether and how multiple mating benefits females remains an open question. Multiple mating is typically thought to be favoured primarily through indirect benefits (i.e. heritable effects on the fitness of offspring). This prediction has been repeatedly tested in a variety of species, but the evidence has been equivocal, perhaps because such studies have focused on pre-reproductive survival rather than lifetime fitness of offspring. Here, we show that in a songbird, the dark-eyed junco ( Junco hyemalis), both male and female offspring produced by extra-pair fertilizations have higher lifetime reproductive success than do offspring sired within the social pair. Furthermore, adult male offspring sired via extra-pair matings are more likely to sire extrapair offspring (EPO) themselves, suggesting that fitness benefits to males accrue primarily through enhanced mating success. By contrast, female EPO benefited primarily through enhanced fecundity. Our results provide strong support for the hypothesis that the evolution of extra-pair mating by females is favoured by indirect benefits and shows that such benefits accrue much later in the offspring's life than previously documented.

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“…We measured plasma testosterone concentrations using an enzyme immunoassay (EIA) kit (901-065; Assay Designs, Ann Arbor, MI, USA) as described in Clotfelter et al [17]. Briefly, steroids were extracted thrice with diethyl ether.…”

Section: (B) Physiological Measurementsmentioning

confidence: 99%

Female plumage colour influences seasonal oxidative damage and testosterone profiles in a songbird

2013

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Across diverse taxa, morphological traits mediate social interactions and mate selection. Physiological constraints on signal elaboration have been widely documented, but the potential for trait display to influence physiological state remains poorly understood. We tested for the presence of causal links between ventral plumage colour-a trait known to covary with reproductive performance-and physiological measures in female North American barn swallows, Hirundo rustica erythrogaster. Naturally darker swallows have lower levels of plasma oxidative damage. Females manipulated to display darker ventral plumage during reproduction rapidly decreased oxidative damage, adopting the physiological state of naturally darker individuals. These results support the presence of a social mechanism that links static plumage traits with the physiological state of their bearer during trait advertisement, long after the completion of signal development.

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Consequences of elevating plasma testosterone in females of a socially monogamous songbird: evidence of constraints on male evolution?

Cited by 145 publications

References 36 publications

Male behavioural maturation rate responds to selection on pollen hoarding in honeybees

Male behavioural maturation rate responds to selection on pollen hoarding in honeybees

Promiscuous mating produces offspring with higher lifetime fitness

Female plumage colour influences seasonal oxidative damage and testosterone profiles in a songbird

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