Direct and indirect genetic effects of sex-specific mitonuclear epistasis on reproductive ageing

Immonen, Elina; Collet, Marie; Goenaga, Julieta; Arnqvist, Göran

doi:10.1038/hdy.2015.112

Cited by 42 publications

(54 citation statements)

References 52 publications

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“…Another D. melanogaster study recovered a significant effect of male partner identity on female fecundity, consistent with a male IGE affecting female fitness components (Tennant et al 2014). Male IGEs affecting female fecundity appear to be exerted through male mitonuclear epistasis in seed beetles (Callosobruchus maculatus), suggesting a complex interplay between organelle-specific IGEs and sexual conflict (Immonen et al 2016).…”

Section: Empirical Evidence For Iges In Behavioral Ecology Researchmentioning

confidence: 93%

Indirect genetic effects in behavioral ecology: does behavior play a special role in evolution?

2017

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Behavior is rapidly flexible and highly context-dependent, which poses obvious challenges to researchers attempting to dissect its causes. However, over a century of unresolved debate has also focused on whether the very flexibility and context-dependence of behavior lends it a unique role in the evolutionary origins and patterns of diversity in the Animal Kingdom. Here, we propose that both challenges can benefit from studying how indirect genetic effects (IGEs: the effects of genes expressed in one individual on traits in another individual) shape behavioral phenotypes. We provide a sketch of the theoretical framework that grounds IGEs in behavioral ecology research and focus on recent advances made from studies of IGEs in areas of behavioral ecology such as sexual selection, sexual conflict, social dominance, and parent-offspring interactions. There is mounting evidence that IGEs have important influences on behavioral phenotypes associated with these processes, such as sexual signals and preferences and behaviors which function to manipulate interacting partners. IGEs can also influence both responses to selection and selection itself, and considering IGEs refines evolutionary predictions and provides new perspectives on the origins of seemingly perplexing behavioral traits. A key unresolved question, but one that has dominated the behavioral sciences for over a century, is whether behavior is more likely than other types of traits to contribute to evolutionary change and diversification. We advocate taking advantage of an IGE approach to outline falsifiable hypotheses and a general methodology to rigorously test this frequently proposed, yet still contentious, special role of behavior in evolution.

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Section: Empirical Evidence For Iges In Behavioral Ecology Researchmentioning

confidence: 93%

Indirect genetic effects in behavioral ecology: does behavior play a special role in evolution?

2017

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“…Same-aged mated and virgin beetles were kept individually for 24 h with beans, after which they were snap-frozen with liquid nitrogen and stored in −80°C. This time point was chosen as it corresponds to the time when females lay most of their eggs (Fox 1993; Immonen et al. 2016a) and males still undergo increased postmating metabolism, presumably due to ejaculate renewal (Immonen et al.…”

Section: Methodsmentioning

confidence: 99%

Mating Changes Sexually Dimorphic Gene Expression in the Seed Beetle Callosobruchus maculatus

Immonen

Sayadi

Bayram

et al. 2017

Genome Biology and Evolution

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Sexually dimorphic phenotypes arise largely from sex-specific gene expression, which has mainly been characterized in sexually naïve adults. However, we expect sexual dimorphism in transcription to be dynamic and dependent on factors such as reproductive status. Mating induces many behavioral and physiological changes distinct to each sex and is therefore expected to activate regulatory changes in many sex-biased genes. Here, we first characterized sexual dimorphism in gene expression in Callosobruchus maculatus seed beetles. We then examined how females and males respond to mating and how it affects sex-biased expression, both in sex-limited (abdomen) and sex-shared (head and thorax) tissues. Mating responses were largely sex-specific and, as expected, females showed more genes responding compared with males (∼2,000 vs. ∼300 genes in the abdomen, ∼500 vs. ∼400 in the head and thorax, respectively). Of the sex-biased genes present in virgins, 16% (1,041 genes) in the abdomen and 17% (243 genes) in the head and thorax altered their relative expression between the sexes as a result of mating. Sex-bias status changed in 2% of the genes in the abdomen and 4% in the head and thorax following mating. Mating responses involved de-feminization of females and, to a lesser extent, de-masculinization of males relative to their virgin state: mating decreased rather than increased dimorphic expression of sex-biased genes. The fact that regulatory changes of both types of sex-biased genes occurred in both sexes suggests that male- and female-specific selection is not restricted to male- and female-biased genes, respectively, as is sometimes assumed.

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“…neutral and nonfunctional. This view contrasts with an increasing number of recent studies that have shown that naturally occurring mitochondrial DNA (mtDNA) haplotypes affect ageing and lifehistory phenotypes (e.g., James and Ballard 2003;Ellison and Burton 2006;Maklakov et al 2006;Rand et al 2006;Ballard et al 2007a;Clancy, 2008;Dowling et al 2009;Arnqvist et al 2010;Immonen et al 2016).…”

mentioning

confidence: 87%

Sex-specific mitonuclear epistasis and the evolution of mitochondrial bioenergetics, ageing, and life history in seed beetles

et al. 2016

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The role of mitochondrial DNA for the evolution of life-history traits remains debated. We examined mitonuclear effects on the activity of the multisubunit complex of the electron transport chain (ETC) involved in oxidative phosphorylation (OXPHOS) across lines of the seed beetle Acanthoscelides obtectus selected for a short (E) or a long (L) life for more than >160 generations. We constructed and phenotyped mitonuclear introgression lines, which allowed us to assess the independent effects of the evolutionary history of the nuclear and the mitochondrial genome. The nuclear genome was responsible for the largest share of divergence seen in ageing. However, the mitochondrial genome also had sizeable effects, which were sex-specific and expressed primarily as epistatic interactions with the nuclear genome. The effects of mitonuclear disruption were largely consistent with mitonuclear coadaptation. Variation in ETC activity explained a large proportion of variance in ageing and life-history traits and this multivariate relationship differed somewhat between the sexes. In conclusion, mitonuclear epistasis has played an important role in the laboratory evolution of ETC complex activity, ageing, and life histories and these are closely associated. The mitonuclear architecture of evolved differences in life-history traits and mitochondrial bioenergetics was sex-specific.

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Direct and indirect genetic effects of sex-specific mitonuclear epistasis on reproductive ageing

Cited by 42 publications

References 52 publications

Indirect genetic effects in behavioral ecology: does behavior play a special role in evolution?

Indirect genetic effects in behavioral ecology: does behavior play a special role in evolution?

Mating Changes Sexually Dimorphic Gene Expression in the Seed Beetle Callosobruchus maculatus

Sex-specific mitonuclear epistasis and the evolution of mitochondrial bioenergetics, ageing, and life history in seed beetles

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