Evolutionary interactions between thermal ecology and sexual selection

Abstract

Thermal ecology and mate competition are both pervasive features of ecological adaptation. A surge of recent work has uncovered the diversity of ways in which temperature affects mating interactions and sexual selection. However, the potential for thermal biology and reproductive ecology to evolve together as organisms adapt to their thermal environment has been underappreciated. Here, we develop a series of hypotheses regarding (1) not only how thermal ecology affects mating system dynamics, but also how mating dynamics can generate selection on thermal traits; and (2) how the thermal consequences of mate competition favour the reciprocal co-adaptation of thermal biology and sexual traits. We discuss our hypotheses in the context of both pre-copulatory and post-copulatory processes. We also call for future work integrating experimental and phylogenetic comparative approaches to understand evolutionary feedbacks between thermal ecology and sexual selection.Overall, studying reciprocal feedbacks between thermal ecology and sexual selection may be necessary to understand how organisms have adapted to the environments of the past and could persist in the environments of the future. K E Y W O R D Sclimate change, co-adaptation, mate choice, mate competition, mating systems, reciprocal causation, I N T RODUC T IONOrganisms must balance many demands as they adapt to their environments (Noordwijk & de Jong, 1986;Reznick et al., 2000;Ricklefs & Wikelski, 2002). Competing for mates, for example, often requires that animals use habitats or express traits that hinder survival (Andersson, 1994;Wiens & Tuschhoff, 2020;Zuk & Kolluru, 1998). Biologists have long understood that these survival costs can offset the benefits of mating success and limit the exaggeration of reproductive characters (

Reproducing in hot water: Experimental heatwaves deteriorate multiple reproductive traits in a freshwater ectotherm

“…Similarly, our finding that after a heatwave males rely more on sneaky matings compared to control males, a tactic that undermines female choice, indicates that there are more opportunities for sexual conflict under heat stress. Altogether, by affecting survival and traits underlying pre‐ and postcopulatory selection, heatwaves are likely to play an important role in the evolutionary feedbacks between thermal ecology and sexual selection (Leith et al, 2022).…”

Multiple mating rescues offspring sex ratio but not productivity in a haplodiploid exposed to developmental heat stress

“…Often, responses to sublethal high temperatures are sex specific (Iossa, 2019), with important and sometimes drastic evolutionary consequences (García‐Roa et al, 2020; Leith et al, 2022). For instance, in the butterfly Bicyclus anynana , high developmental temperature affect the costs and benefits of mating in opposite ways in males and females, such that changes in sexual roles and ornamentation are observed (Prudic et al, 2011).…”

“…Often, responses to sublethal high temperatures are sex specific (Iossa, 2019), with important and sometimes drastic evolutionary consequences (García-Roa et al, 2020;Leith et al, 2022).…”

The potential for the evolution of thermally sensitive courtship behaviours in the treehopper, Enchenopa binotata

“…However, adaptation to novel climatic regimes ultimately requires adjustments in traits related to reproduction in addition to those related to survival (García-Roa et al, 2020; Moore et al, 2021;Leith et al, 2020;Leith et al, 2022). Little attention has been directed to understanding genetic variation in mating-related traits despite their prevalent sensitivity to temperature (reviewed in Leith et al, 2021).…”

“…A growing body of research has found significant genetic variation—a prerequisite to adaptive genetic responses—in the thermal sensitivity of a range of ecologically relevant traits, including those that affect life history (Garant et al, 2008; Møller, 2001; Pulido et al, 2001; Van Der Jeugd & McCleery, 2002), physiology (Diamond et al, 2017; Doyle et al, 2011; Kelly et al, 2012; Ketola et al, 2012; Leal & Gunderson, 2012; Mattila & Hanski, 2014; Meffe et al, 1995; Munday et al, 2017; Muñoz et al, 2015), and performance (Gilchrist, 1996; Latimer et al, 2011; Logan et al, 2020). However, adaptation to novel climatic regimes ultimately requires adjustments in traits related to reproduction in addition to those related to survival (García‐Roa et al, 2020; Moore et al, 2021; Leith et al, 2020; Leith et al, 2022). Little attention has been directed to understanding genetic variation in mating‐related traits despite their prevalent sensitivity to temperature (reviewed in Leith et al, 2021).…”