Evolution of sex-specific pace-of-life syndromes: genetic architecture and physiological mechanisms

Abstract

Sex differences in life history, physiology, and behavior are nearly ubiquitous across taxa, owing to sex-specific selection that arises from different reproductive strategies of the sexes. The pace-of-life syndrome (POLS) hypothesis predicts that most variation in such traits among individuals, populations, and species falls along a slow-fast pace-of-life continuum. As a result of their different reproductive roles and environment, the sexes also commonly differ in pace-of-life, with important consequences for the evolution of POLS. Here, we outline mechanisms for how males and females can evolve differences in POLS traits and in how such traits can covary differently despite constraints resulting from a shared genome. We review the current knowledge of the genetic basis of POLS traits and suggest candidate genes and pathways for future studies. Pleiotropic effects may govern many of the genetic correlations, but little is still known about the mechanisms involved in trade-offs between current and future reproduction and their integration with behavioral variation. We highlight the importance of metabolic and hormonal pathways in mediating sex differences in POLS traits; however, there is still a shortage of studies that test for sex specificity in molecular effects and their evolutionary causes. Considering whether and how sexual dimorphism evolves in POLS traits provides a more holistic framework to understand how behavioral variation is integrated with life histories and physiology, and we call for studies that focus on examining the sex-specific genetic architecture of this integration.

Pace-of-life syndromes: a framework for the adaptive integration of behaviour, physiology and life history

“…gradients of risks and resources) in their models and tests of POLS (Montiglio et al 2018, topical collection on Pace-of-life syndromes; Salzman et al 2018, topical collection on Pace-of-life syndromes; Tieleman 2018, topical collection on Pace-of-life syndromes); (3) given the fundamental differences in life history between males and females, aspects of POLS should be sex-specific , topical collection on Pace-of-life syndromes; Immonen et al 2018, topical collection on Pace-of-life syndromes; Lehmann et al 2018, topical collection on Pace-of-life syndromes; Tarka et al 2018, topical collection on Pace-of-life syndromes); (4) POLS can be studied at different levels of variation, but "raw" phenotypic correlations between POLS traits (the prevailing level at which data are currently analysed: Royauté et al 2018, topical collection on Pace-of-life syndromes) alone seem relatively uninformative; (5) empirical studies should test the fundamental assumptions first (i.e. the trade-offs between life-history traits indicative of current versus future reproduction), use relevant traits (e.g.…”

“…The topical collection of articles we present here includes (1) reviews (Mathot and Frankenhuis 2018, topical collection on Pace-of-life syndromes; Montiglio et al 2018, topical collection on Pace-of-life syndromes; Tieleman 2018, topical collection on Pace-of-life syndromes) and meta-analyses of empirical literature (Royauté et al 2018, topical collection on Paceof-life syndromes; Tarka et al 2018, topical collection on Paceof-life syndromes) that draw a portrait of the current state of knowledge on the topic and propose conceptual advancements predicting the ecological conditions favouring POLSs, as well as sex-specific POLSs , topical collection on Pace-of-life syndromes; Immonen et al 2018, topical collection on Pace-of-life syndromes; Tarka et al 2018, topical collection on Pace-of-life syndromes), (2) a novel simulation model predicting relationships between traits involved in POLSs under different environmental conditions (Salzman et al 2018, topical collection on Pace-of-life syndromes), (3) novel statistical methodologies (Araya-Ajoy et al 2018, topical collection on Pace-of-life syndromes), and (4) empirical quantifications of POLSs at multiple levels of biological organisation (Bengston in review; Delahaie et al 2018, topical collection on Pace-of-life syndromes; Jablonszky et al 2018, topical collection on Pace-of-life syndromes; Lehmann et al 2018, topical collection on Pace-of-life syndromes; Sol et al 2018, topical collection on Pace-of-life syndromes). Here, we briefly summarise the main conclusions that can be drawn from these contributions.…”

“…Drawing from sexual selection theory, Hämäläinen et al (2018), topical collection on Pace-of-life syndromes developed a framework on what aspects of POLS might be sexspecific, based on which they suggest various ultimate mechanisms driving sex differences in mean trait expression and POLS-trait covariation and propose predictions on why and when we should expect to find sex-specific POLS. Immonen et al (2018), topical collection on Pace-of-life syndromes outline potential mechanisms for the evolution of sex differences in POLS. Assessing and evaluating the current knowledge on the genetic basis of POLS-traits and their covariation, they discuss how a sex-specific genetic architecture might evolve and how hormonal and metabolic mechanisms might mediate sex differences proximately.…”

Sex differences in life history, behavior, and physiology along a slow-fast continuum: a meta-analysis

“…Nonetheless, these predictions have not been supported across studies (Závorka et al 2015; Kim and Velando 2016). One explanation for this discrepancy might be that important systematic sources of variation, such as environment (Salzman et al 2018, topical collection on Pace-of-life syndromes), ecology (Montiglio et al 2018, topical collection on pace-of-life syndromes), or age- and sex-specific variation (Hämäläinen et al 2018, Immonen et al 2018; both in topical collection on Pace-of-life syndromes) have not often been considered.…”

“…Assuming that physiological and behavioral traits are aligned with life-history traits on a general POL-continuum, we might predict sex-specific differences in the POL (i.e., sex-specific differences in trait means across all trait categories). Sex differences in POL may be an important driver generating individual-level variation in POLS (i.e., sex-specific trait correlations within populations; e.g., Hämäläinen et al 2018, Immonen et al 2018; both in topical collection on pace-of-life syndromes). Indeed, males and females of many species differ in their physiology (e.g., immunology, (Lee 2006; Restif and Amos 2010), metabolism (Nagy 1987; Blaxter 1989; Rønning et al 2016), hormone profiles (Nelson 2011), and behavior (Smith and Blumstein 2008; Schuett et al 2010), but the directionality of these differences within and across trait categories has not been formally tested.…”