Positive allometry of sexually selected traits: Do metabolic maintenance costs play an important role?

Sexual selection drives the evolution of some of the most exaggerated traits in nature. Studies on sexual selection often focus on the size of these traits relative to body size, but few focus on energetic maintenance costs of the tissues that compose them, and the ways in which these costs vary with body size. The relationships between energy use and body size have consequences that may allow large individuals to invest disproportionally more in sexually selected structures, or lead to the reduced per-gram maintenance cost of enlarged structures. Although sexually selected traits can incur energetic maintenance costs, these costs are not universally high; they are dependent on the relative mass and metabolic activity of tissues associated with them. Energetic costs of maintenance may play a pervasive yet little-explored role in shaping the relative scaling of sexually selected traits across diverse taxa. Also see the video abstract here: https://youtu.be/JyuoQIeA33Q.

Extreme variation in testes size in an insect is linked to recent mating activity.

Ample sperm production is essential for successful male reproduction in many species. The amount of sperm a male can produce is typically constrained by the size of his testes, which can be energetically expensive to grow and maintain. Although the economics of ejaculate allocation has been the focus of much theoretical and empirical literature, relatively little attention has been paid to individual adult variation and plasticity at the source of sperm production, the testes themselves. We experimentally address this issue using the insect Narnia femorata Stål (Hemiptera: Coreidae). We established the metabolic cost of testicular tissue and then quantified variation in individual testes mass in response to multiple mate quality and quantity treatments. We uncovered extreme variation across individuals and considerable short-term effects of mating activity on testes dry mass. Importantly, the observed variation in testes mass was associated with notable fitness consequences; females paired with males with larger testes had greater hatching success. Overall, pairing with a female resulted in a 11% reduction in dry testes mass. Despite this apparent considerable mating investment, we found no evidence of strategic allocation to higher quality females or longer-term changes in testes mass. The dynamic nature of testes mass and its metabolic cost is vital to consider in the context of re-mating rates, polyandry benefits and general mating system dynamics both in this species and more broadly.

Muscle mass drives cost in sexually selected arthropod weapons.

Sexually selected weapons often function as honest signals of fighting ability. If poor-quality individuals produce high-quality weapons, then receivers should focus on other, more reliable signals. Cost is one way to maintain signal integrity. The costs of weapons tend to increase with relative weapon size, and thereby restrict large weapons to high-quality individuals who can produce and maintain them. Weapon cost, however, appears to be unpredictably variable both within and across taxa, and the mechanisms underlying this variation remain unclear. We suggest variation in weapon cost may result from variation in weapon composition-specifically, differences in the amount of muscle mass directly associated with the weapon. We test this idea by measuring the metabolic cost of sexually selected weapons in seven arthropod species and relating these measures to weapon muscle mass. We show that individuals with relatively large weapon muscles have disproportionately high resting metabolic rates and provide evidence that this trend is driven by weapon muscle mass. Overall, our results suggest that variation in weapon cost can be partially explained by variation in weapon morphology and that the integrity of weapon signals may be maintained by increased metabolic cost in species with relatively high weapon muscle mass.

The hidden cost of sexually selected traits: the metabolic expense of maintaining a sexually selected weapon.

Sexually selected weapons are among the most exaggerated traits in nature. Sexual selection theory frequently assumes a high cost of this exaggeration; yet, those costs are rarely measured. We know very little about the energetic resources required to maintain these traits at rest and the difference in energetic costs for the largest individuals relative to the smallest individuals. Knowledge in this area is crucial; resting metabolic rate can account for 30-40% of daily energy expenditure in wild animals. Here, we capitalized on the phenomenon of autotomy to take a unique look at weapon maintenance costs. Using Leptoscelis tricolor (Hemiptera: Coreidae), we measured CO2 production rates before and after a weapon was shed. Males in this insect species use enlarged hind femora as weapons in male-male combat, and yet can shed them readily, without regeneration, upon entrapment. We found that metabolic rate decreased by an average of 23.5% in males after leg loss and by 7.9% in females. Notably, larger males had less of a drop in metabolic rate per gram of weapon lost. Our findings suggest that sexually selected weapons contribute to a large portion of resting metabolic rate in males, but these costs do not scale in direct proportion to size; larger males can have larger weapons for a reduced metabolic cost. These energetic maintenance costs may be integral to the evolution of the allometries of sexually selected weapons, and yet they remain largely unexplored.

Extreme range in adult body size reveals hidden trade-offs among sexually selected traits.

Sexually selected weapons used to monopolize mating opportunities are predicted to trade-off with traits used in competition for fertilization. Yet, the limited size range typically found among adults of a species often precludes clear comparisons between population-level and individual-level relative trait investment. The jousting weevil, Brentus anchorago (Coleoptera: Brentidae), varies more than 26-fold in body mass, which is among the most extreme adult body size ranges of any solitary terrestrial species. We reveal a trade-off at a population level: hypermetric scaling in male weapons (slope = 1.59) and a closely mirrored reversal in allocation to postcopulatory traits (slope = 0.54). Yet, at the individual level, we find the opposite pattern; males that invest relatively more in weapons for their size class also invest more in postcopulatory traits. Across 36 dung beetle and 41 brentine weevil species, we find the allometric slope explains more trait variation at larger body size ranges; in brentines, population-level scaling patterns become more detectable in species with a larger range in adult body size. Our findings reveal that population-level allometries and individual-level trade-offs can both be important in shaping relative trait allocation; we highlight that the adult body size range is rarely examined but may be integral to gaining a deeper understanding of trade-offs in reproductive allocation.

Selection on weapon allometry in the wild.

Allometry is the scaling relationship between a trait and body size. This relationship can often explain considerable morphological variation within and among species. Nevertheless, much remains unknown about the factors that underlie allometric patterns. For example, when different allometric relationships are observed amongst closely related species, these differences are regularly considered to be products of selection. However, directional selection on allometry (particularly the slope) has rarely been tested and observed in natural populations. Here, we investigate selection on the scaling relationship between weapon size and body size (i.e., weapon allometry) in a wild population of giant mesquite bugs, Pachylis neocalifornicus (previously Thasus neocalifornicus). Males in this species use their weapons (enlarged femurs) to compete with one another over access to resources and females. We found that large males with relatively large weapons successfully secured access to mates. However, we also found that small males with relatively small weapons could access mates as well. These two patterns together can increase the allometric slope of the sexually selected weapon, suggesting a straightforward process by which the allometric slope can evolve.

Can Sex-Specific Metabolic Rates Provide Insight Into Patterns of Metabolic Scaling?

Females and males can exhibit striking differences in body size, relative trait size, physiology and behavior. As a consequence the sexes can have very different rates of whole-body energy use, or converge on similar rates through different physiological mechanisms. Yet many studies that measure the relationship between metabolic rate and body size only pay attention to a single sex (more often males), or do not distinguish between sexes. We present four reasons why explicit attention to energy-use between the sexes can yield insight into the physiological mechanisms that shape broader patterns of metabolic scaling in nature. First, the sexes often differ considerably in their relative investment in reproduction which shapes much of life-history and rates of energy use. Second, males and females share a majority of their genome but may experience different selective pressures. Sex-specific energy profiles can reveal how the energetic needs of individuals are met despite the challenge of within-species genetic constraints. Third, sexual selection often pushes growth and behavior to physiological extremes. Exaggerated sexually selected traits are often most prominent in one sex, can comprise up to 50% of body mass and thus provide opportunities to uncover energetic constraints of trait growth and maintenance. Finally, sex-differences in behavior such as mating-displays, long-distance dispersal and courtship can lead to drastically different energy allocation among the sexes; the physiology to support this behavior can shape patterns of metabolic scaling. The mechanisms underlying metabolic scaling in females, males and hermaphroditic animals can provide opportunities to develop testable predictions that enhance our understanding of energetic scaling patterns in nature.

White Paper: An Integrated Perspective on the Causes of Hypometric Metabolic Scaling in Animals.

Larger animals studied during ontogeny, across populations, or across species, usually have lower mass-specific metabolic rates than smaller animals (hypometric scaling). This pattern is usually observed regardless of physiological state (e.g. basal, resting, field, maximally-active). The scaling of metabolism is usually highly correlated with the scaling of many life history traits, behaviors, physiological variables, and cellular/molecular properties, making determination of the causation of this pattern challenging. For across-species comparisons of resting and locomoting animals (but less so for across populations or during ontogeny), the mechanisms at the physiological and cellular level are becoming clear. Lower mass-specific metabolic rates of larger species at rest are due to a) lower contents of expensive tissues (brains, liver, kidneys), and b) slower ion leak across membranes at least partially due to membrane composition, with lower ion pump ATPase activities. Lower mass-specific costs of larger species during locomotion are due to lower costs for lower-frequency muscle activity, with slower myosin and Ca++ ATPase activities, and likely more elastic energy storage. The evolutionary explanation(s) for hypometric scaling remain(s) highly controversial. One subset of evolutionary hypotheses relies on constraints on larger animals due to changes in geometry with size; for example, lower surface-to-volume ratios of exchange surfaces may constrain nutrient or heat exchange, or lower cross-sectional areas of muscles and tendons relative to body mass ratios would make larger animals more fragile without compensation. Another subset of hypotheses suggests that hypometric scaling arises from biotic interactions and correlated selection, with larger animals experiencing less selection for mass-specific growth or neurolocomotor performance. A additional third type of explanation comes from population genetics. Larger animals with their lower effective population sizes and subsequent less effective selection relative to drift may have more deleterious mutations, reducing maximal performance and metabolic rates. Resolving the evolutionary explanation for the hypometric scaling of metabolism and associated variables is a major challenge for organismal and evolutionary biology. To aid progress, we identify some variation in terminology use that has impeded cross-field conversations on scaling. We also suggest that promising directions for the field to move forward include: 1) studies examining the linkages between ontogenetic, population-level, and cross-species allometries, 2) studies linking scaling to ecological or phylogenetic context, 3) studies that consider multiple, possibly interacting hypotheses, and 4) obtaining better field data for metabolic rates and the life history correlates of metabolic rate such as lifespan, growth rate and reproduction.

The evolution of autotomy in leaf-footed bugs.

Sacrificing body parts is one of many behaviors that animals use to escape predation. This trait, termed autotomy, is classically associated with lizards. However, several other taxa also autotomize, and this trait has independently evolved multiple times throughout Animalia. Despite having multiple origins and being an iconic antipredatory trait, much remains unknown about the evolution of autotomy. Here, we combine morphological, behavioral, and genomic data to investigate the evolution of autotomy within leaf-footed bugs and allies (Insecta: Hemiptera: Coreidae + Alydidae). We found that the ancestor of leaf-footed bugs autotomized and did so slowly; rapid autotomy (<2 min) then arose multiple times. The ancestor likely used slow autotomy to reduce the cost of injury or to escape nonpredatory entrapment but could not use autotomy to escape predation. This result suggests that autotomy to escape predation is a co-opted benefit (i.e., exaptation), revealing one way that sacrificing a limb to escape predation may arise. In addition to identifying the origins of rapid autotomy, we also show that across species variation in the rates of autotomy can be explained by body size, distance from the equator, and enlargement of the autotomizable appendage.

Adult nutrition, but not inbreeding, affects male primary sexual traits in the leaf-footed cactus bug Narnia femorata (Hemiptera: Coreidae).

Adverse conditions may be the norm rather than the exception in natural populations. Many populations experience poor nutrition on a seasonal basis. Further, brief interludes of inbreeding can be common as population density fluctuates and because of habitat fragmentation. Here, we investigated the effects of poor nutrition and inbreeding on traits that can be very important to reproductive success and fitness in males: testes mass, sperm concentration, and sperm viability. Our study species was Narnia femorata, a species introduced to north-central Florida in the 1950s. This species encounters regular, seasonal changes in diet that can have profound phenotypic effects on morphology and behavior. We generated inbred and outbred individuals through a single generation of full-sibling mating or outcrossing, respectively. All juveniles were provided a natural, high-quality diet of Opuntia humifusa cactus cladode with fruit until they reached adulthood. New adult males were put on a high- or low-quality diet for at least 21 days before measurements were taken. As expected, the low-quality diet led to significantly decreased testes mass in both inbred and outbred males, although there were surprisingly no detectable effects on sperm traits. We did not find evidence that inbreeding affected testes mass, sperm concentration, and sperm viability. Our results highlight the immediate and overwhelming effects of nutrition on testes mass, while suggesting that a single generation of inbreeding might not be detrimental for primary sexual traits in this particular population.