Beyond Genes and Environments: Indirect Genetic Effects and the Evolution of Behaviour

Hunt, John; Rapkin, James; House, Clarissa M.; Wilson, Alastair J.

doi:10.1002/9781119313663.ch4

Cited by 3 publications

(5 citation statements)

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“…Indeed, Liedvogel et al 2012) report estimates from their main model (i.e., including fixed effects) for both female and male additive genetic variance that are considerably lower than those we report here, consistent with such an explanation for the discrepancies between analyses with broadly overlapping sample populations. Clearly, incorporating the impact of the social environment into empirical description of evolutionary dynamics under natural settings is a considerable challenge, and it is perhaps unsurprising that published estimates of direct-indirect genetic correlations for free-living populations are exceedingly few (Fisher and Pruitt 2019;Hunt et al 2019), despite the increasing application of quantitative genetic analyses to long-term study populations more generally (Postma 2014). Nonetheless, while the extent to which indirect genetic determination applies to behavioral traits remains unclear, recent results from laboratory studies suggest it is potentially widespread (Carter et al 2019;Dewan et al 2019).…”

Section: Discussionmentioning

confidence: 99%

“…Clearly, incorporating the impact of the social environment into empirical description of evolutionary dynamics under natural settings is a considerable challenge, and it is perhaps unsurprising that published estimates of direct‐indirect genetic correlations for free‐living populations are exceedingly few (Fisher and Pruitt 2019; Hunt et al. 2019), despite the increasing application of quantitative genetic analyses to long‐term study populations more generally (Postma 2014). Nonetheless, while the extent to which indirect genetic determination applies to behavioral traits remains unclear, recent results from laboratory studies suggest it is potentially widespread (Carter et al.…”

Section: Discussionmentioning

confidence: 99%

“…The study of IGEs in wild populations has been dominated by a focus on maternal genetic effects (McAdam et al 2014). However, social interactions between non-relatives can also give rise to IGEs (Wade et al 2010;Costa e Silva et al 2013), although published estimates for populations in natural settings are scant (Hunt et al 2019). In this context, sexual partnerships have clear potential to facilitate indirect genetic effects, particularly in species where pairs form an association that persists beyond fertilization (Carter et al 2019;Chakrabarty et al 2019).…”

mentioning

confidence: 99%

“…2013), although published estimates for populations in natural settings are scant (Hunt et al. 2019). In this context, sexual partnerships have clear potential to facilitate indirect genetic effects, particularly in species where pairs form an association that persists beyond fertilization (Carter et al.…”

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confidence: 99%

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It takes two: Heritable male effects on reproductive timing but not clutch size in a wild bird population*

2020

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Within-population variation in the traits underpinning reproductive output has long been of central interest to biologists. Since they are strongly linked to lifetime reproductive success, these traits are expected to be subject to strong selection and, if heritable, to evolve. Despite the formation of durable pair bonds in many animal taxa, reproductive traits are often regarded as femalespecific, and estimates of quantitative genetic variation seldom consider a potential role for heritable male effects. Yet reliable estimates of such social genetic effects are important since they influence the amount of heritable variation available to selection. Based on a 52-year study of a nestbox-breeding great tit (Parus major) population, we apply "extended" bivariate animal models in which the heritable effects of both sexes are modeled to assess the extent to which males contribute to heritable variation in seasonal reproductive timing (egg laying date) and clutch size, while accommodating the covariance between the two traits. Our analyses show that reproductive timing is a jointly expressed trait in this species, with (positively covarying) heritable variation for laydate being expressed in both members of a breeding pair, such that the total heritable variance is 50% larger than estimated by traditional models. This result was robust to explicit consideration of a potential male-biased environmental confound arising through sexually dimorphic dispersal. In contrast to laydate, males' contribution to heritable variation in clutch size was limited. Our study thus highlights the contrasting extent of social determination for two major components of annual reproductive success, and emphasizes the need to consider the social context of what are often considered individual-level traits.

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Section: Discussionmentioning

confidence: 99%

Section: Discussionmentioning

confidence: 99%

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confidence: 99%

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confidence: 99%

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It takes two: Heritable male effects on reproductive timing but not clutch size in a wild bird population*

2020

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“…For example, behavioural traits are a key element of any social interaction and are typically considered to be highly plastic. Behavioural traits may therefore show large IGE variance (Bailey et al, 2018; see Hunt et al, 2019 for a review of IGEs on behaviours). However, behavioural traits may also vary more in response to the non-social environment, in which case the proportion of variance in phenotypes due to IGEs may not be so high.…”

Section: Introductionmentioning

confidence: 99%

Indirect genetic effects increase the heritable variation available to selection and are largest for behaviours: a meta-analysis

Santostefano,

Moiron,

Sánchez-Tójar

et al. 2024

Preprint

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The rate of trait evolution is governed by the amount of heritable variation available to selection. While this is typically quantified based on genetic variation in a focal individual for its own traits (direct genetic effects, DGEs), when social interactions occur, genetic variation in interacting partners can influence a focal individual's traits (indirect genetic effects, IGEs). Theory and studies on domesticated species have suggested IGEs can greatly impact evolutionary trajectories, but whether this is true more broadly remains unclear. Here we perform a systematic review and meta-analysis to quantify the amount of trait variance explained by IGEs and the contribution of IGEs to predictions of evolutionary change. We identified 180 effect sizes from 47 studies across 21 species and found that, on average, IGEs account for a small but statistically significant amount of phenotypic variation (3%). As IGEs affect the trait values of each interacting group member and due to a typically positive – although statistically nonsignificant – correlation with DGEs (rDGE–IGE = 0.25), IGEs ultimately increase trait heritability substantially from 26% (narrow-sense heritability) to 40% (total heritable variance). This 54% average increase in heritability suggests IGEs have a great potential to enhance the rate of evolution. Furthermore, IGEs were most prominent for behavioural traits, and to a lesser extent for reproduction and survival, in contrast to morphological, metabolic, physiological, and development traits. Our meta-analysis therefore shows that IGEs tend to enhance the rate of evolution, especially for traits tightly related to interactions with other individuals such as behaviour and reproduction.

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Indirect genetic effects increase the heritable variation available to selection and are largest for behaviors: a meta-analysis

Santostefano,

Moiron,

Sánchez-Tójar

et al. 2024

Evolution Letters

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The evolutionary potential of traits is governed by the amount of heritable variation available to selection. While this is typically quantified based on genetic variation in a focal individual for its own traits (direct genetic effects, DGEs), when social interactions occur, genetic variation in interacting partners can influence a focal individual’s traits (indirect genetic effects, IGEs). Theory and studies on domesticated species have suggested IGEs can greatly impact evolutionary trajectories, but whether this is true more broadly remains unclear. Here, we perform a systematic review and meta-analysis to quantify the amount of trait variance explained by IGEs and the contribution of IGEs to predictions of adaptive potential. We identified 180 effect sizes from 47 studies across 21 species and found that, on average, IGEs of a single social partner account for a small but statistically significant amount of phenotypic variation (0.03). As IGEs affect the trait values of each interacting group member and due to a typically positive—although statistically nonsignificant—correlation with DGEs (rDGE-IGE = 0.26), IGEs ultimately increase trait heritability substantially from 0.27 (narrow-sense heritability) to 0.45 (total heritable variance). This 66% average increase in heritability suggests IGEs can increase the amount of genetic variation available to selection. Furthermore, whilst showing considerable variation across studies, IGEs were most prominent for behaviors and, to a lesser extent, for reproduction and survival, in contrast to morphological, metabolic, physiological, and development traits. Our meta-analysis, therefore, shows that IGEs tend to enhance the evolutionary potential of traits, especially for those tightly related to interactions with other individuals, such as behavior and reproduction.

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Beyond Genes and Environments: Indirect Genetic Effects and the Evolution of Behaviour

Cited by 3 publications

References 77 publications

It takes two: Heritable male effects on reproductive timing but not clutch size in a wild bird population*

It takes two: Heritable male effects on reproductive timing but not clutch size in a wild bird population*

Indirect genetic effects increase the heritable variation available to selection and are largest for behaviours: a meta-analysis

Indirect genetic effects increase the heritable variation available to selection and are largest for behaviors: a meta-analysis

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