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Sperm competition is a powerful selective force that has shaped sexual traits throughout animal evolution. Yet, how fertilization mode (i.e. external versus internal fertilization) influences the scope and potential for sperm competition to act on ejaculates remains unclear. Here, I examine how fertilization mode shapes ejaculatory responses to sperm competition in fishes, a diverse group that constitute the majority of vertebrate biological diversity. Fishes are an ideal group for this examination because they exhibit a wide range of reproductive behaviours and an unparalleled number of transitions in fertilization mode compared to any other vertebrate group. Drawing on data from cartilaginous and bony fishes, I first show that rates of multiple paternity are higher in internally than externally fertilizing fishes, contrary to the prevailing expectation. I then summarize how sperm competition acts on sperm number and quality in internally and externally fertilizing fishes, highlighting where theoretical predictions differ between these groups. Differences in how ejaculates respond to sperm competition between fertilization modes are most apparent when considering sperm size and swimming performance. Clarifying how fertilization mode influences evolutionary responses in ejaculates will inform our understanding of ejaculate evolution across the animal tree of life. This article is part of the theme issue ‘Fifty years of sperm competition’.

Male genitalia exhibit patterns of divergent evolution driven by sexual selection. In contrast, for many taxonomic groups, female genitalia are relatively uniform and their patterns of evolution remain largely unexplored. Here we quantify variation in the shape of female genitalia across onthophagine dung beetles, and use new comparative methods to contrast their rates of divergence with those of male genitalia. As expected, male genital shape has diverged more rapidly than a naturally selected trait, the foretibia. Remarkably, female genital shape has diverged nearly three times as fast as male genital shape. Our results dispel the notion that female genitalia do not show the same patterns of divergent evolution as male genitalia, and suggest that female genitalia are under sexual selection through their role in female choice. Although male genital shape is known to evolve rapidly in response to sexual selection, relatively little is known about the evolution of female genital shape. Here, the authors show that across onthophagine dung beetles, female genital shape has diverged much more rapidly than male genital shape.

Females of many species mate with multiple males, thereby inciting competition among ejaculates from rival males for fertilization. In response to increasing sperm competition, males are predicted to enhance their investment in sperm production. This prediction is so widespread that testes size (correcting for body size) is commonly used as a proxy of sperm competition, even in the absence of any other information about a species' reproductive behaviour. By contrast, a debate about whether sperm competition selects for smaller or larger sperm has persisted for nearly three decades, with empirical studies demonstrating every possible response. Here, we synthesize nearly 40 years of sperm competition research in a meta-analytical framework to determine how the evolution of sperm number (i.e. testes size) and sperm size (i.e. sperm head, midpiece, flagellum and total length) is influenced by varying levels of sperm competition across species. Our findings support the long-held assumption that higher levels of sperm competition are associated with relatively larger testes. We also find clear evidence that sperm competition is associated with increases in all components of sperm length. We discuss these results in the context of different theoretical predictions and general patterns in the breeding biology and selective environment of sperm. This article is part of the theme issue ‘Fifty years of sperm competition’.

Environmental change frequently drives morphological diversification, including at the cellular level. Transitions in the environment where fertilization occurs (i.e., fertilization mode) are hypothesized to be a driver of the extreme diversity in sperm morphology observed in animals. Yet how fertilization mode impacts the evolution of sperm components—head, midpiece, and flagellum—each with different functional roles that must act as an integrated unit remains unclear. Here, we test this hypothesis by examining the evolution of sperm component lengths across 1103 species of vertebrates varying in fertilization mode (external vs. internal fertilization). Sperm component length is explained in part by fertilization mode across vertebrates, but how fertilization mode influences sperm evolution varies among sperm components and vertebrate clades. We also identify evolutionary responses not influenced by fertilization mode: midpieces evolve rapidly in both external and internal fertilizers. Fertilization mode thus influences vertebrate sperm evolution through complex component- and clade-specific evolutionary responses. The location where fertilization takes place can be highly variable across species, and especially between internal and external fertilizers. Kahrl et al. find that fertilization environment plays a significant role in the evolution and diversification of sperm morphology across vertebrate species.

Domestication is hypothesized to drive correlated responses in animal morphology, physiology and behaviour, a phenomenon known as the domestication syndrome. However, we currently lack quantitative confirmation that suites of behaviours are correlated during domestication. Here we evaluate the strength and direction of behavioural correlations among key prosocial (sociability, playfulness) and reactive (fearfulness, aggression) behaviours implicated in the domestication syndrome in 76,158 dogs representing 78 registered breeds. Consistent with the domestication syndrome hypothesis, behavioural correlations within prosocial and reactive categories demonstrated the expected direction-specificity across dogs. However, correlational strength varied between dog breeds representing early (ancient) and late (modern) stages of domestication, with ancient breeds exhibiting exaggerated correlations compared to modern breeds across prosocial and reactive behaviours. Our results suggest that suites of correlated behaviours have been temporally decoupled during dog domestication and that recent shifts in selection pressures in modern dog breeds affect the expression of domestication-related behaviours independently. Dog breeds differ in evolutionary age and admixture with wolves, enabling comparison across domestication stages. Here, Hansen Wheat et al. show that correlations among behaviours are decoupled in modern breeds compared to ancient breeds and suggest this reflects a recent shift in selection pressure.

Theory predicts a trade-off between investments in precopulatory (ornaments and armaments) and postcopulatory (testes and ejaculates) sexual traits due to the costs associated with their growth and maintenance within the finite energy resources available. Empirical studies, however, have revealed considerable inconsistency in the strength and direction of relationships among these sexual traits. Ambiguity may result from variance in the marginal benefits gained by increasing investments in either pre- or postcopulatory sexual traits. Here, in a broad comparative study, we test the prediction that the relationship between pre- and postcopulatory sexual traits differs among taxa relative to the importance of male–male contest competition within them. We find that covariance between pre- and postcopulatory sexual traits gradually shifts from strongly positive to strongly negative with increasing male–male contest competition. Thus, our findings reveal a potentially unifying explanation for the oftentimes inconsistent relationships in the strength and direction of covariance among sexual traits. Theory predicts trade-offs between investments in precopulatory and postcopulatory sexual traits, but empirical evidence is inconsistent. Here, Lüpold et al. show that the covariance between pre- and postcopulatory sexual traits shifts from positive to negative with increasing male–male competition.

Postcopulatory sexual selection is widely accepted to underlie the extraordinary diversification of sperm morphology. However, why does it favour longer sperm in some taxa but shorter in others? Two recent hypotheses addressing this discrepancy offered contradictory explanations. Under the sperm dilution hypothesis, selection via sperm density in the female reproductive tract favours more but smaller sperm in large, but the reverse in small, species. Conversely, the metabolic constraint hypothesis maintains that ejaculates respond positively to selection in small endothermic animals with high metabolic rates, whereas low metabolic rates constrain their evolution in large species. Here, we resolve this debate by capitalizing on the substantial variation in mammalian body size and reproductive physiology. Evolutionary responses shifted from sperm length to number with increasing mammalian body size, thus supporting the sperm dilution hypothesis. Our findings demonstrate that body-size-mediated trade-offs between sperm size and number can explain the extreme diversification in sperm phenotypes.

Sperm are the most morphologically variable cell type known, despite performing the same functional role of fertilizing eggs across all sexually reproducing species. Sperm morphology commonly varies among individuals, populations, closely related species, and across animal phyla. Sperm morphology has long been used as a tool for placing species in a phylogenetic context and a range of selective forces are hypothesized to influence sperm evolution and diversification. However, we currently lack robust examinations of macroevolutionary (i.e. across phyla) patterns of sperm evolution, due largely to the challenges of comparing sperm morphological data across the animal tree of life. Here we describe the SpermTree database, which currently represents 5,675 morphological descriptions of sperm morphology from 4,705 unique species from 27 animal phyla. This dataset includes measurements of sperm head, midpiece, flagellum and total length, the latter of which spans four orders of magnitude. All entries in the dataset are matched to currently accepted scientific names in taxonomic databases, facilitating the use of these data in analyses examining sperm evolution in animals. Measurement(s) sperm morphology trait • Spermatozoon Technology Type(s) Microscope Device Sample Characteristic - Organism Metazoa Machine-accessible metadata file describing the reported data: https://doi.org/10.6084/m9.figshare.17151347

One of the most common visual adaptations seen in the mesopelagic zone (200-1000 m), where the amount of light diminishes exponentially with depth and where bioluminescent organisms predominate, is the enlargement of the eye and pupil area. However, it remains unclear how eye size is influenced by depth, other environmental conditions and phylogeny. In this study, we determine the factors influencing variability in eye size and assess whether this variability is explained by ecological differences in habitat and lifestyle within a family of mesopelagic fishes characterized by broad intra- and interspecific variance in depth range and luminous patterns. We focus our study on the lanternfish family (Myctophidae) and hypothesise that lanternfishes with a deeper distribution and/or a reduction of bioluminescent emissions have smaller eyes and that ecological factors rather than phylogenetic relationships will drive the evolution of the visual system. Eye diameter and standard length were measured in 237 individuals from 61 species of lanternfishes representing all the recognised tribes within the family in addition to compiling an ecological dataset including depth distribution during night and day and the location and sexual dimorphism of luminous organs. Hypotheses were tested by investigating the relationship between the relative size of the eye (corrected for body size) and variations in depth and/or patterns of luminous-organs using phylogenetic comparative analyses. Results show a great variability in relative eye size within the Myctophidae at all taxonomic levels (from subfamily to genus), suggesting that this character may have evolved several times. However, variability in eye size within the family could not be explained by any of our ecological variables (bioluminescence and depth patterns), and appears to be driven solely by phylogenetic relationships.

Group living species are constantly facing decisions about which conspecifics to associate with. These decisions are likely guided by the benefits and costs of associations. Associating in larger groups can minimize predation risk, while also providing individuals with beneficial social information from conspecifics. By contrast, associating with multiple individuals could also increase potentially costly conflicts over resources and/or mates. Here, we examine male association strategies in a shoaling fish, the pygmy halfbeak ( Dermogenys collettei ), by confronting males with four different social scenarios. We found that males preferentially associated with an opposite sex pair (i.e., a female and a male) over rival males, but showed no preference when choosing between a pair and females. By contrast, the number of presented fish (one or two) did not influence male association preferences, indicating that the observed male behavior was not driven by shoaling behavior. Finally, male association preference correlated with the duration of courtship behavior that the male observed, but only under specific social scenarios. Overall, our data show that males followed informed association strategies that are primarily driven by mating opportunities. Using a simplified social environment, we illuminate which basic rules might drive association behavior in complex social groups.