Selection on personality in a songbird affects maternal hormone levels tuned to its effect on timing of reproduction

Groothuis, Ton G. G.; Carere, Claudio; Lipar, Joe; Drent, Piet J.; Schwabl, Hubert

doi:10.1098/rsbl.2008.0258

Cited by 53 publications

(40 citation statements)

References 22 publications

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“…Importantly, a high consistency of yolk T deposition within females and between mothers and daughters does not preclude a plastic and adaptive female response to environmental variation, but in addition, it opens up the opportunity for hormone-mediated maternal effects to respond to selection and thus to evolve. Such indirect genetic effects can modify or accelerate phenotypic change in natural populations and might thereby play an important role in evolutionary processes such as parentoffspring coevolution (Kölliker et al 2000(Kölliker et al , 2005Müller et al 2007;Tschirren and Richner 2008), the evolution of behavioral syndromes (Dingemanse et al 2003;van Oers et al 2004;Groothuis and Carere 2005;Gil and Faure 2007;Tobler and Sandell 2007;Groothuis et al 2008), or dispersal behavior and the colonization of new environments (Hahn et al 2005;Duckworth and Badyaev 2007;Tschirren et al 2007) in a range of taxa. We hope that by elucidating the heritable basis of yolk hormone deposition, this study will bring us closer to an understanding of the evolution of hormone-mediated maternal effects, the patterns that shape their current expression both within and among species, and their consequences for the direction and speed of phenotypic change in natural populations.…”

Section: Discussionmentioning

confidence: 99%

Heritable Variation in Maternal Yolk Hormone Transfer in a Wild Bird Population

Tschirren¹,

Sendecka²,

Groothuis³

et al. 2009

The American Naturalist

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Differential reproductive investment by the mother can critically influence offspring development and phenotype, and strong selection is therefore expected to act on such maternal effects. Although a genetic basis is a prerequisite for phenotypic traits to respond to selection and thus to evolve, we still know very little about the extent of heritable variation in maternal effects in natural populations. Here, we present the first estimates of intrafemale repeatability across breeding seasons and estimates of heritability of hormonemediated maternal effects in a wild population of collared flycatchers (Ficedula albicollis). We found that maternal yolk testosterone (T) concentrations, yolk mass, and egg mass were moderately to highly repeatable within females across years, whereas intrafemale consistency of maternal yolk androstenedione (A4) deposition was low yet statistically significant. Furthermore, maternal yolk T transfer, yolk mass, and egg mass were significantly heritable, whereas yolk A4 transfer was not. These results strongly suggest that two major maternal yolk androgens are differentially regulated by genes and the environment. Selection on heritable variation in maternal yolk T deposition has the potential to shape the rate and direction of phenotypic change in offspring traits and can thereby accelerate or impede the response to selection in natural populations.

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Section: Discussionmentioning

confidence: 99%

Heritable Variation in Maternal Yolk Hormone Transfer in a Wild Bird Population

Tschirren¹,

Sendecka²,

Groothuis³

et al. 2009

The American Naturalist

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“…Studies measuring the development of personality tend to focus on unitary organisms and the role of early experience (DiRienzo et al, 2012), maternal effects (Groothuis et al, 2008) and persistence across life stages (Bell and Stamps, 2004). It has been shown that the consistency of personality can vary through ontogeny and upon maturation.…”

Section: Defining and Evaluating Collective Personalitiesmentioning

confidence: 99%

The development of collective personality: the ontogenetic drivers of behavioral variation across groups

2014

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For the past decade, the study of personality has become a topic on the frontier of behavioral ecology. However, most studies have focused on exploring inter-individual behavioral variation in solitary animals, and few account for the role that social interactions may have on the development of an individual's personality. Moreover, a social group may exhibit collective personality: an emergent behavioral phenotype displayed at the group-level, which is not necessarily the sum or average of individual personalities within that group. The social environment, in many cases, can determine group success, which then influences the relative success of all the individuals in that group. In addition, group-level personality may itself evolve, subject to the same selection pressures as individual-level behavioral variation, when the group is a unit under selection. Therefore, we reason that understanding how collective personalities emerge and change over time will be imperative to understanding individual-and group-level behavioral evolution. Personality is considered to be fixed over an individual's lifetime. However, behavior may shift throughout development, particularly during adolescence. Therefore, juvenile behavior should not be compared with adult behavior when assessing personality. Similarly, as conditions within a group and/or the local environment can shift, group behavior may similarly fluctuate as it matures. We discuss potential within-group factors, such as group initiation, group maturation, genetic make-up of the group, and the internal social environment, and external factors, such as how local environment may play a role in generating group-level personalities. There are a variety of studies that explore group development or quantify group personality, but few that integrate both processes. Therefore, we conclude our review by discussing potential ways to evaluate development of collective personality, and propose several focal areas for future research.

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“…allocation of higher levels of T in first-laid eggs, could exacerbate disadvantages for later hatchlings, facilitating brood reduction under bad food conditions [63]. In this latter case, the higher levels of maternally-derived T in the first-laid eggs would boost the competitive ability of the first-hatched chicks and precipitate brood reduction via the death of the less competitive chick(s) hatched from the last-laid egg(s) [9], [56].…”

Section: Introductionmentioning

confidence: 99%

Brood Reduction via Intra-clutch Variation in Testosterone - An Experimental Test in the Great Tit

2013

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In birds, yolk androgen concentrations in eggs can increase or decrease over the laying sequence and common hypotheses hold that this serves to favour the competitive ability of either first- or last-hatched chicks depending on the prevailing conditions, and thus promote brood reduction or maintenance of original brood size respectively. Intra-clutch variation of testosterone can shift relative competitive ability of siblings and hence competitive dynamics. In a natural population of great tits, we experimentally investigated the effects and function of maternal testosterone on offspring phenotype in relation to the laying position of the egg in a context of hatching asynchrony. To this end, we created three types of clutches where either the first three or the last three eggs of a clutch were injected with testosterone (T) dissolved in sesame oil, and the remaining eggs with sesame oil only, or where all eggs of a clutch were injected with sesame oil. Increased levels of yolk T in the last-laid eggs resulted in the last-hatched chicks being significantly lighter and smaller than their siblings, while increased levels of T in the first-laid eggs had no direct effect on the first-hatched chicks, but an indirect negative effect on their siblings. Our results suggest that females can potentially adjust offspring phenotype by modulating, over the laying sequence, the amounts of T deposited in the eggs. These results are in contradiction, however, with current hypotheses and previous findings, which suggest that under good conditions higher levels of maternally derived T in the last-laid eggs should mitigate the negative effects of hatching asynchrony.

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Selection on personality in a songbird affects maternal hormone levels tuned to its effect on timing of reproduction

Cited by 53 publications

References 22 publications

Heritable Variation in Maternal Yolk Hormone Transfer in a Wild Bird Population

Heritable Variation in Maternal Yolk Hormone Transfer in a Wild Bird Population

The development of collective personality: the ontogenetic drivers of behavioral variation across groups

Brood Reduction via Intra-clutch Variation in Testosterone - An Experimental Test in the Great Tit

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