Jennifer C. Perry

The seminal symphony: How to compose an ejaculate

Ejaculates are fundamental to fitness in sexually reproducing animals: males gain all their direct fitness via the ejaculate and females require ejaculates to reproduce. Both sperm and non-sperm components of the ejaculate (including parasperm, seminal proteins, water, and macromolecules) play vital roles in postcopulatory sexual selection and conflict, processes that can potentially drive rapid evolutionary change and reproductive isolation. Here, we assess the increasing evidence that considering ejaculate composition as a whole (and potential trade-offs among ejaculate components) has important consequences for predictions about male reproductive investment and female responses to ejaculates. We review current theory and empirical work, and detail how social and environmental effects on ejaculate composition have potentially far-reaching fitness consequences for both sexes.

Condition-dependent ejaculate size and composition in a ladybird beetle

Sexually selected male ejaculate traits are expected to depend on the resource state of males. Theory predicts that males in good condition will produce larger ejaculates, but that ejaculate composition will depend on the relative production costs of ejaculate components and the risk of sperm competition experienced by low- and high-condition males. Under some conditions, when low condition leads to poorer performance in sperm competition, males in low condition may produce ejaculates with higher sperm content relative to their total ejaculate and may even transfer more sperm than high-condition males in an absolute sense. Previous studies in insects have shown that males in good condition transfer larger ejaculates or more sperm, but it has not been clear whether increased sperm content represents a shift in allocation or simply a larger ejaculate, and thus the condition dependence of ejaculate composition has been largely untested. We examined condition dependence in ejaculate by manipulating adult male condition in a ladybird beetle (Adalia bipunctata) in which males transfer three distinct ejaculate components during mating: sperm, non-sperm ejaculate retained within the female reproductive tract, and a spermatophore capsule that females eject and ingest following mating. We found that high condition males indeed transferred larger ejaculates, potentially achieved by an increased rate of ejaculate transfer, and allocated less to sperm compared with low-condition males. Low-condition males transferred ejaculates with absolutely and proportionally more sperm. This study provides the first experimental evidence for a condition-dependent shift in ejaculate composition.

The Ontogeny and Evolution of Sex-Biased Gene Expression in Drosophila melanogaster

Sexually dimorphic phenotypes are thought to largely result from sex differences in gene expression, and genes with sex-biased expression have been well characterized in adults of many species. Although most sexual dimorphisms manifest in adults, many result from sex-specific developmental trajectories, implying that juveniles may exhibit significant levels of sex-biased expression. However, it is unclear how much sex-biased expression occurs before reproductive maturity and whether preadult sex-biased genes should exhibit the same evolutionary dynamics observed for adult sex-biased genes. In order to understand the continuity, or lack thereof, and evolutionary dynamics of sex-biased expression throughout the life cycle, we examined sex-biased genes in pre-gonad tissue of two preadult stages and compared them with the adult gonad of Drosophila melanogaster. We found that the majority of the genome is sex-biased at some point in the life cycle, with some genes exhibiting conserved sex-biased expression and others displaying stage-specific sex bias. Our results also reveal a far more complex pattern of evolution for sex-biased genes throughout development. The most rapid evolutionary divergence occurred in genes expressed only in larvae within each sex, compared with continuously expressed genes. In females—but not males—this pattern appeared to be due to relaxed purifying selection in larva-limited genes. Furthermore, genes that retained male bias throughout life evolved more rapidly than stage-specific male-biased genes, due to stronger purifying selection in stage-specific genes. However, female-biased genes that were specific to larvae evolved most rapidly, a pattern that could not be definitively attributed to differences in adaptive evolution or purifying selection, suggesting that pleiotropic constraints on protein-coding sequences can arise when genes are broadly expressed across developmental stages. These results indicate that the signature of sex-specific selection can be detected well before reproductive maturity and is strongest during development.

Emerging issues in the evolution of animal nuptial gifts.

Uniquely positioned at the intersection of sexual selection, nutritional ecology and life-history theory, nuptial gifts are widespread and diverse. Despite extensive empirical study, we still have only a rudimentary understanding of gift evolution because we lack a unified conceptual framework for considering these traits. In this opinion piece, we tackle several issues that we believe have substantively hindered progress in this area. Here, we: (i) present a comprehensive definition and classification scheme for nuptial gifts (including those transferred by simultaneous hermaphrodites), (ii) outline evolutionary predictions for different gift types, and (iii) highlight some research directions to help facilitate progress in this field.

SEXUAL CONFLICT AND ANTAGONISTIC COEVOLUTION ACROSS WATER STRIDER POPULATIONS

Microevolutionary studies have demonstrated sexually antagonistic selection on sexual traits, and existing evidence supports a macroevolutionary pattern of sexually antagonistic coevolution. Two current questions are how antagonistic selection within‐populations scales to divergence among populations, and to what extent intraspecific divergence matches species‐level patterns. To address these questions, we conducted an intraspecific comparative study of sexual armaments and mating behaviors in a water strider (Gerris incognitus) in which male genitals grasp resistant females and female abdominal structures help ward off males. The degree of exaggeration of these armaments coevolves across species. We found a similar strong pattern of antagonistic coevolution among populations, suggesting that sexual conflict drives population differentiation in morphology. Furthermore, relative exaggeration in armaments was closely related to mating outcomes in a common environment. Interestingly, the effect of armaments on mating was mediated by population sexual size dimorphism. When females had a large size advantage, mating activity was low and independent of armaments, but when males had a relative size advantage, mating activity depended on which sex had relatively exaggerated armaments. Thus, a strong signal of sexually antagonistic coevolution is apparent even among populations. These results open opportunities to understand links between sexual arms races, ecological variation, and reproductive isolation.

Condition-dependent female remating resistance generates sexual selection on male size in a ladybird beetle

Behavioural resistance to remating by females is common, but the causes and consequences of resistance are rarely explained. Prominent hypotheses include resistance as a means of avoiding costly and superfluous mating, or as a means of biasing mating towards high-quality males. In species in which males produce nutritious nuptial gifts, females may further modulate resistance according to their need for nutrition. We investigated these hypotheses in the ladybeetle Adalia bipunctata, in which females frequently display vigorous resistance before copulation and ingest a spermatophore after copulation. In two experiments, we manipulated female nutritional state, depriving or satiating females for a short (16 h) or long (96 h) interval before a remating trial. We found that food-deprived females resisted mating more frequently and for longer periods than satiated females and consequently remated less frequently. This condition dependence of resistance supports the hypothesis that resistance functions to reduce superfluous and costly mating. Our finding that food-deprived females were more resistant suggests that mating imposes energetic costs, and that nuptial feeding does not offset these costs. In a third experiment, we investigated whether the extent of resistance depended on male size or whether resistance itself biased mating towards large males. The extent of female resistance was independent of male size, but resistance itself resulted in a mating bias towards large males. In summary, our results support the hypotheses that females resist mating simply because it is costly and superfluous, and that a side effect of resistance is sexual selection for large male size.

The cost of being an omnivore: mandible wear from plant feeding in a true bug.

Evolutionary and ecological transitions from carnivorous to omnivorous feeding may be constrained by the ability of the animal to cope with disparate types of foods, even if preadaptations for such behaviour exist. The omnivorous true bug, Dicyphus hesperus (Hemiptera: Miridae) requires both animals (small, soft-bodied insects) and plants in its diet and obtains the majority of its dietary and metabolic water from plant feeding. Serrations on the lateral margins of the mandibular stylets wear with age, and this wear is exacerbated when the insects feed on plants compared to those provided free water and no plants. D. hesperus that feed on plants attack fewer prey but consumed similar amounts of prey tissue compared to individuals that were provided free water. Although others have shown mandible wear for plant-chewing animals we show for the first time that plant feeding can impose similar wear on plant-piercing animals as well.

Experimental evolution of a novel sexually antagonistic allele.

Evolutionary conflict permeates biological systems. In sexually reproducing organisms, sex-specific optima mean that the same allele can have sexually antagonistic expression, i.e. beneficial in one sex and detrimental in the other, a phenomenon known as intralocus sexual conflict. Intralocus sexual conflict is emerging as a potentially fundamental factor for the genetic architecture of fitness, with important consequences for evolutionary processes. However, no study to date has directly experimentally tested the evolutionary fate of a sexually antagonistic allele. Using genetic constructs to manipulate female fecundity and male mating success, we engineered a novel sexually antagonistic allele (SAA) in Drosophila melanogaster. The SAA is nearly twice as costly to females as it is beneficial to males, but the harmful effects to females are recessive and X-linked, and thus are rarely expressed when SAA occurs at low frequency. We experimentally show how the evolutionary dynamics of the novel SAA are qualitatively consistent with the predictions of population genetic models: SAA frequency decreases when common, but increases when rare, converging toward an equilibrium frequency of ∼8%. Furthermore, we show that persistence of the SAA requires the mating advantage it provides to males: the SAA frequency declines towards extinction when the male advantage is experimentally abolished. Our results empirically demonstrate the dynamics underlying the evolutionary fate of a sexually antagonistic allele, validating a central assumption of intralocus sexual conflict theory: that variation in fitness-related traits within populations can be maintained via sex-linked sexually antagonistic loci.

The evolution of index signals to avoid the cost of dishonesty

Animals often convey useful information, despite a conflict of interest between the signaller and receiver. There are two major explanations for such ‘honest’ signalling, particularly when the size or intensity of signals reliably indicates the underlying quality of the signaller. Costly signalling theory (including the handicap principle) predicts that dishonest signals are too costly to fake, whereas the index hypothesis predicts that dishonest signals cannot be faked. Recent evidence of a highly conserved causal link between individual quality and signal growth appears to bolster the index hypothesis. However, it is not clear that this also diminishes costly signalling theory, as is often suggested. Here, by incorporating a mechanism of signal growth into costly signalling theory, we show that index signals can actually be favoured owing to the cost of dishonesty. We conclude that costly signalling theory provides the ultimate, adaptive rationale for honest signalling, whereas the index hypothesis describes one proximate (and potentially very general) mechanism for achieving honesty.

Developmental environment mediates male seminal protein investment in Drosophila melanogaster

Summary Males of many species fine‐tune their ejaculates in response to sperm competition risk. Resource availability and the number of competitors during development can also strongly influence sperm production. However, despite the key role of seminal proteins in mediating reproductive processes, it is unclear whether seminal protein investment is dependent on the developmental environment. We manipulated the developmental environment of Drosophila melanogaster by rearing flies at low and high density. As expected, this resulted in large and small (i.e. high and low condition) adult phenotypes, respectively. As predicted, large males produced more of two key seminal proteins, sex peptide (SP) and ovulin, and were more successful at obtaining matings with both virgin and previously mated females. However, there was only a weak and non‐significant trend for large males to transfer more absolute quantities of SP at mating, and thus, small males ejaculated proportionally more of their stored accessory gland SP resources. Males transferred more receptivity‐inhibiting SP to large females. Despite this, large females remated more quickly than small females and thus responded to their developmental environment over and above the quantity of SP they received. The results are consistent with two non‐mutually exclusive hypotheses. First, flies might respond to condition‐dependent reproductive opportunities, with (i) small males investing heavily in ejaculates when mating opportunities arise and large males strategically partitioning SP resources and (ii) small females remating at reduced rates because they have higher mating costs or need to replenish sperm less often. Second, flies may be primed by their larval environment to deal with similar adult population densities, with (i) males perceiving high density as signalling increased competition, leading small males to invest proportionally more SP resources at mating and (ii) females perceiving high density as signalling abundant potential mates, leading to a higher sexual receptivity threshold. Thus, by influencing the mating frequencies of both sexes, as well as the quantity of seminal proteins produced by males and received by females, the developmental environment is likely to have far‐reaching and sex‐specific consequences for sexual selection and sexual conflict.