Metabolism as a screenwriter in the female–male coevolutionary play

Systematic differences between the sexes, what we call sexual dimorphism, abound in nature. In sexually reproducing species, which account for the great majority of known multicellular organisms (1), evolution has repeatedly driven the sexes to diverge in their behavior (e.g., mating strategies or parental care), morphology (e.g., size and ornamentation), physiology (e.g., stress response or disease susceptibility), and life history (e.g., reproductive schedules or life span). Some species take this to the extreme, such as Ceratioid anglerfish and Baetid mayflies. In the former, females are up to 60 times larger than the parasitic males that attach to their ventral side and frequently remain there, as parasitic dwarfs, for the rest of their life (2). In the latter, males not only usually live considerably shorter life spans than females but also showcase an extra pair of eyes (i.e., turbinate eyes) that are larger than normal compound eyes, harbor novel types of opsin photoreceptors, and are thought to develop through distinct developmental pathways (3). The sheer diversity in the degree and nature of sexual dimorphism across the tree of life is quite simply baffling. While in most birds males exhibit highly ornamented plumages and sophisticated displays that contrast sharply with their relatively drab female counterparts, such as in peacocks and birds of paradise, in a few species with sex role reversal it is the female plumage that catches the eye (4). While extreme sexual dimorphism led males and females of some species to be initially classified as belonging to different taxa (e.g., Ceratioids), in others the sexes are almost completely monomorphic. Understanding how and why sexual dimorphism evolves is thus one of evolutionary biology’s central questions, dating back to the work of Charles Darwin (5). Among the chief challenges in this prolific field is to disentangle what factors explain why sexual dimorphism takes on such diverse evolutionary routes across taxa. In PNAS, Arnqvist et al. (6) report on a series of exciting findings from an ambitious common garden comparative study that bring us closer to this old ambition.

Sexual dimorphism results from sex-specific selective pressures that can arise via natural or sexual selection. Intraspecific resource competition between the sexes can drive the evolution of sexual dimorphism via ecological character displacement (ECD) by decreasing the degree to which the ecological niche of females and males overlaps. Despite a recent surge in attention, however, there has been a dearth of studies reporting convincing evidence of sexual ECD (7, 8). In contrast, there is compelling evidence that sexual dimorphism can evolve readily via sexual selection, as a consequence of anisogamy and the distinct sexual roles that result from it (9–11). This so-called Darwin–Bateman paradigm has been very successful in explaining patterns in the evolution of sexual dimorphism, such as why certain differences between the sexes appear more frequently than others (11): for example, the finding that males tend to compete more strongly for access to mating partners and ensuing fertilizations, and tend to experience stronger sexual selection (12, 13). However, female–male coevolution can proceed via different evolutionary routes and give rise to strikingly different levels of sexual dimorphism even among closely related taxa, and sexual selection by itself cannot account for this diversity of outcomes.

Current theory aims to explain the diversity in the outcomes of sexual selection via an interaction between ecology, life history, and the economics of reproduction. The classic paper of Emlen and Oring (14) established how, by modulating the costs and benefits of mate monopolization, ecology is expected to drive the evolution of mating systems and with it, sexual selection and ensuing sexual dimorphism. In the last few decades, we have come to understand that this picture is further complicated by the dynamic interplay between ecology and life history on the one hand and life history and mating systems on the other (15) (Fig. 1A). Thus, it is clear that ecology directly or indirectly modulates life histories and sexual selection, which in turn drive sexual dimorphism. What is far from clear is the causal link between ecology, life history, and sexual selection. A promising avenue to disentangle this relationship is metabolism.

Fig. 1.

Evolutionary interplay between ecology, life history, and sexual selection. (A) Ecology has well-established effects on the evolution of life history and mating systems (and thus, sexual selection) via its modulation of the economics of mating. Sexual selection and life histories are also intimately linked. (B) Metabolism might be a critical nexus in the interplay between this trinity, helping us to disentangle the correlated responses of life history and sexual selection to ecology and the resulting female–male coevolutionary dynamics. Arnqvist et al. (6) show that in seed beetles, ecology (i.e., whether a species feeds on seeds of annual herbs vs. perennial trees) dictates resource availability, and this, in turn, selects for high or low metabolic rates (i.e., resting metabolic rates; RMR) that ultimately modulate POLS and the economics of mating to drive female–male coevolution.

Metabolism is a unifying feature of life because all organismal functions (i.e., growth survival and reproduction) are fueled by metabolic routes. Biophysical constraints condition the uptake, transformation, and expenditure of energy and materials from the environment (e.g., arising from organismal size or temperature effects), and recent studies have pointed out that understanding the physiological machinery that converts energy to fitness may help unravel the relationship between ecological processes, life history, and the economics of reproduction (16–19). As a matter of fact, life history variation is mostly constrained across a slow–fast axis called the pace of life syndrome (POLS) (20). Organisms at one end of this spectrum are characterized by a low reproductive rate, slow development, and long life span, while organisms at the other end are characterized by the opposite traits. Importantly, metabolism is thought to underly the POLS due to the correlated evolution of physiological traits and metabolic rate (18–20). Thus, fast organisms necessarily rely on high metabolic rates and vice versa, and because ecology fundamentally affects how organisms harvest energy from their ecosystems, metabolic rate seems to be an obvious nexus between life history variation, reproduction, and ecology. A specific prediction is that environments characterized by low resource availability and/or high resource competition effectively limit metabolic rate and should select for slow POLS and life history traits, while environments rich in resources should favor high metabolic rates and fast POLS. Furthermore and as a consequence of sexual selection, males and females are often subject to diverging POLS (21) and potentially, sex-specific metabolic rates (22). Thus, the scene is set to suggest that female–male coevolution and sexual dimorphism could result from ecology, life history, and the economics of reproduction interacting via the evolution of sex-specific metabolic rates (Fig. 1B). Conveniently and as seen above, this framework derives specific predictions as to how resource availability should mediate metabolic rate, POLS, and female–male coevolution.

To test this overarching idea, Arnqvist et al. (6) conducted a long-term comparative common garden study where they measured metabolic rate, 11 life history traits, and 17 reproductive traits across males and females of 12 species of seed beetles (Bruchinae). Seed beetles exhibit high variation in their mating systems (from conventional sex roles to sex role reversal), and different species feed on legumes of either annual herbs or perennial trees, which has profound repercussions for their ecology. While annual herbs provide ephemeral bursts of resources sustaining low-density populations (i.e., low resource competition and high resource availability), perennial trees provide continuous resources and sustain large high-density populations (i.e., high resource competition and low resource availability). Furthermore, seed beetles have an evolutionary history of strong sexually antagonistic coevolution between the sexes that has given rise to marked variation in the economics of reproduction across different species. Thus, females incur in clear mating costs produced by male spiny genitalia and toxic male ejaculates but also, can garner important benefits from large male ejaculates as they provide females with nutrients and water (6). For males, mating costs can result from allocation to large ejaculates, typical of high competition over reproduction at high densities, or from male searching, typical of low population densities (6).

Using this rich set of data, Arnqvist et al. (6) provide compelling evidence that metabolism offers a mechanistic basis that links ecology with life history and the economics of reproduction to drive female–male coevolution (Fig. 1B). They show that metabolic rate correlates with life history as predicted and that such correlated evolution is driven by ecology. Namely, seed beetle species subject to high resource competition evolved slow metabolic rates and POLS, while species subject to low resource competition evolved fast metabolic rates and POLS. They also found that the economics of mating evolved antagonistically in males and females and, importantly, did so in a correlated fashion with metabolic rate, POLS, and ecology. This strongly suggests that, through its effects on metabolic rate, ecology drives the evolution of the economics of mating and life histories and ultimately, female–male coevolution. Finally and in consonance with the idea that males are under stronger sexual selection for faster POLS than females, Arnqvist et al. (6) show that metabolic rate evolved more rapidly in males than in females. Overall, this ambitious study nicely shows that by determining resource use, ecology seems to constrain the metabolic rate in seed beetles, which in turn, appears to drive the evolution of life histories and mating systems (Fig. 1B).

Along with recent theoretical developments (16–21), the above findings place metabolism as a causative nexus in the evolutionary interplay between ecology, life history, and sexual selection and suggest it may thus help us explain why sexual dimorphism unfolds so differently across the tree of life. In doing so, they open up a series of intriguing and promising research avenues for the immediate future. For example, given its direct effects on metabolism and its potential for sex-specific effects in the context of sexual selection (23), temperature could in principle orchestrate female–male coevolution and POLS. The idea that ecology can trigger complex cascading effects on POLS and sexual selection via its effects on metabolism also suggests that, by changing how males and females acquire resources, initial ECD may set off the evolution of sexual dimorphism by sexual selection and even prompt a feedback dynamic between the two processes (7). Perhaps placing the spotlight on metabolism may also aid our understanding of how organisms with a shared genome can develop in such spectacularly different ways. As a corollary, lest we forget, Arnqvist et al. (6) also incidentally remind us of the extraordinary value that long-term studies have in ecology and evolution in an era in which such studies are increasingly rare.