Bailey et al. (2017) bring us improved understanding of the relevance of indirect genetic effects (IGEs) for behavioral ecology. In addition to reviewing the evidence for IGEs and outlining the theoretical framework underlying the action of IGEs on behavioral phenotypes, they propose a methodological approach that will purportedly inform on whether behavior has a unique role in evolution. Before addressing this notable aspect of Bailey et al.’s (2017) contribution, I will comment on issues dealing with semantics and bias. IS IT ALL SOCIAL? Bailey et al. slightly overuse the term social in its many forms (the word social is used over 80 times, and social environment over 25 times). Of course, their terminology is meant to simplify concepts, and indeed they acknowledge (though only in the last page of their review) that the term social should be broadened to include any interaction. Yet the abuse of the “social perspective” in IGEs research (which is prevalent for obvious reasons) will likely contribute to research bias. Some IGEs may actually have little to do with social connotations. IGEs emerging through maternal oviposition choices, for example, do not involve the generation of any social environment per se. Semantics matter because they may inadvertently lead to future research neglecting a series of interesting and far-reaching IGEs. For instance, ejaculates do not directly contribute to the generation of a social environment for the offspring-to-be either; yet ejaculate-driven IGEs are emerging as important players in a range of evolutionary questions (Garcia-Gonzalez and Simmons 2007; Lane et al. 2014; Zajitschek et al. 2014; Garcia-Gonzalez and Dowling 2015). Genetically based variation in the characteristics of the seminal fluid can be both a source of paternal IGEs, but also, remarkably, of interacting phenotypes IGEs when ejaculates from different males overlap (Garcia-Gonzalez and Simmons 2007). These recent findings have brought to an end the traditional notion that in species without paternal care fathers can contribute little beyond genes to offspring phenotype. Viewing IGEs as the exclusive result of social environments would contribute to aggravate the general dismissal of paternal IGEs when there is no paternal care, and might potentially hamper the discovery of other interesting, thus far unknown, IGEs. SPECIAL ROLE OF BEHAVIOR IN EVOLUTION The variance decomposition approach suggested by Bailey et al. (see also Bijma 2014) will indubitably be of great utility to compare the relative importance of IGEs vs direct genetic effects at different levels. By using mean-standardized variances, the approach will also shed light on the relationship between IGEs and evolvabilities (Garcia-Gonzalez et al. 2012). Based on these premises, undertaking Bailey et al.’s IGE approach will return exceptional benefits. A different question, however, is whether, by weighting the relative importance of IGEs upon behavioral and nonbehavioral traits, we can draw well-founded conclusions about whether behavior has a special role in evolution. I contend here that everything is important and everything is special. Bailey et al.’s proposition for testing the special role of behavior in evolution may suffer from some limitations. They argue that IGEs will be more frequently involved (and so detected) for behavioral traits than for nonbehavioral traits. One problem, however, is that drawing the line for behavioral or nonbehavioral involvement is not always easy. For instance, in Garcia-Gonzalez and Simmons’s (2007) study, embryo viability was shown to be determined by sire and nonsire ejaculate-driven IGEs. In that case, neither the focal trait (offspring viability) nor the vehicle that mediates IGEs (ejaculates) are behavioral traits. Nevertheless, the opportunity for the interacting phenotype IGE is possible thanks to a behavior (multiple mating) by a third actor, the multiple mating female. This example illustrates that extreme caution must be taken when separating traits into different categories. Bailey et al. argue that the more frequent detection of IGEs for behavioral traits will support the unique role of behavior, provided that traits are surveyed in an unbiased manner. However, testing for IGEs is not trivial, and while ideally traits should be screened randomly, general limitations exist in regards to the known, possible and feasible technologies, methodologies and resources that can be used to assay phenotypes randomly. Bailey et al. claim that the unique role of behavior in evolution will be supported if IGEs are more common and of greater magnitude for behavioral traits compared with other types of traits. Such more is better principle is debatable. Will differences in the phenotypic variance explained by IGEs affecting behavioral versus nonbehavioral traits, or on the evolvabilities of these IGEs, or on the frequency that behavioral traits are affected by IGEs compared to other traits, really imply that some traits have a “more” special role in evolution than others? This is arguably a difficult question to answer. In the meantime, Bailey et al.’s variance partitioning approach and their call for an increased focus on IGEs will undoubtedly spur much-needed research on the topic and will greatly advance our understanding of evolution and behavioral ecology, even if everything is unique and special, as it is usually the case in evolution. FUNDING F. G.-G. was supported by grant CGL2016-76173-P from the Spanish Ministry of Economy (co-funded by the European Regional Development Fund). REFERENCES Bailey NW LJ. Marie-Orleach Allen Moore. Indirect genetic effects in behavioral ecology: does behavior play a special role in evolution? Behav. Ecol. doi:10.1093/beheco/arx127 Bijma P. 2014. The quantitative genetics of indirect genetic effects: a selective review of modelling issues. Heredity (Edinb) . 112: 61– 69. Google Scholar CrossRef Search ADS PubMed Garcia-Gonzalez F Dowling DK. 2015. Transgenerational effects of sexual interactions and sexual conflict: non-sires boost the fecundity of females in the following generation. Biol. Lett . 11: 20150067. Google Scholar CrossRef Search ADS PubMed García-González F Simmons LW. 2007. Paternal indirect genetic effects on offspring viability and the benefits of polyandry. Curr Biol . 17: 32– 36. Google Scholar CrossRef Search ADS PubMed Garcia-Gonzalez F Simmons LW Tomkins JL Kotiaho JS Evans JP. 2012. Comparing evolvabilities: common errors surrounding the calculation and use of coefficients of additive genetic variation. Evolution . 66: 2341– 2349. Google Scholar CrossRef Search ADS PubMed Lane M Robker RL Robertson SA. 2014. Parenting from before conception. Science . 345: 756– 760. Google Scholar CrossRef Search ADS PubMed Zajitschek S Hotzy C Zajitschek F Immler S. 2014. Short-term variation in sperm competition causes sperm-mediated epigenetic effects on early offspring performance in the zebrafish. Proc Biol Sci . 281: 20140422. Google Scholar CrossRef Search ADS PubMed © The Author(s) 2017. Published by Oxford University Press on behalf of the International Society for Behavioral Ecology. All rights reserved. For permissions, please e-mail: email@example.com
Behavioral Ecology – Oxford University Press
Published: Jan 1, 2018
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