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Due to the difficulty of simultaneously assessing variation in individual physiology, behaviour and fitness, we often know little about the mechanistic basis of life-history trade-offs and fitness variation. It is similarly challenging to examine how physiological variation in one individual has cascading fitness consequences for others in the social environment. Using a wild-living fish (ocellated wrasse, Symphodus ocellatus), we manipulated a neuropeptide pathway associated with courtship, aggression and parental care in vertebrates (arginine vasotocin, AVT) and directly examined the behavioural and fitness consequences. Nesting males injected with the AVT antagonist increased their paternal care, resulting in increased hatching of offspring and increased reproductive success of all individuals that mated at his nest. By directly examining physiology, behaviour and reproductive success, we revealed how a small change in individual physiology has clear and direct fitness consequences for multiple individuals. © 2019 The Association for the Study of Animal Behaviour

In species with internal fertilization, females can favour certain males over others, not only before mating but also within the female's reproductive tract after mating. Here, we ask whether such directional post-mating (that is, cryptic) female mate choice can also occur in species with external fertilization. Using an in vitro sperm competition experiment, we demonstrate that female ovarian fluid (ovarian fluid) changes the outcome of sperm competition by decreasing the importance of sperm number thereby increasing the relative importance of sperm velocity. We further show that ovarian fluid does not differentially affect sperm from alternative male phenotypes, but generally enhances sperm velocity, motility, straightness and chemoattraction. Under natural conditions, female ovarian fluid likely increases the paternity of the preferred parental male phenotype, as these males release fewer but faster sperm. These results imply females have greater control over fertilization and potential to exert selection on males in species with external fertilization than previously thought possible.

Male–male competition is a well-known driver of reproductive success and sexually selected traits in many species. However, in some species, males work together to court females or defend territories against male competitors. Dominant (nesting) males sire most offspring, but subordinate (satellite) males are better able to obtain fertilizations relative to unpartnered males. Because satellites only gain reproductive success by sneaking, there has been much interest in identifying the mechanisms enforcing satellite cooperation (defense) and reducing satellite sneaking. One such potential mechanism is outside competition: unpartnered satellites can destabilize established male partnerships and may force partnered satellites to restrain from cheating to prevent the dominant male from replacing them with an unpartnered satellite. Here, we manipulated perceived competition in the Mediterranean fish Symphodus ocellatus by presenting an “intruding” satellite male to established nesting and satellite male pairs. Focal satellite aggression to the intruder was higher when focal satellites were less cooperative, suggesting that satellites increase aggression to outside competitors when their social position is less stable. In contrast, nesting male aggression to the intruder satellite increased as spawning activity increased, suggesting that nesting males increase their defense toward outside competitors when their current relationship is productive. We found no evidence of altered spawning activity or nesting/satellite male interactions before and after the presentation. These results collectively suggest that response to outside competition is directly linked to behavioral dynamics between unrelated male partners and may be linked to conflict and cooperation in ways that are similar to group-living species.

Sexual selection arising from sperm competition has driven the evolution of immense variation in ejaculate allocation and sperm characteristics not only among species, but also among males within a species. One question that has received little attention is how cooperation among males affects these patterns. Here we ask how male alternative reproductive types differ in testes size, ejaculate production, and sperm morphology in the ocellated wrasse, a marine fish in which unrelated males cooperate and compete during reproduction. Nesting males build nests, court females and provide care. Sneaker males only “sneak” spawn, while satellite males sneak, but also help by chasing away sneakers. We found that satellite males have larger absolute testes than either sneakers or nesting males, despite their cooperative role. Nesting males invested relatively less in testes than either sneakers or satellites. Though sneakers produced smaller ejaculates than either satellite or nesting males, we found no difference among male types in either sperm cell concentration or sperm number, implying sneakers may produce less seminal fluid. Sperm tail length did not differ significantly among male types, but sneaker sperm cells had significantly larger heads than either satellite or nesting male sperm, consistent with past research showing sneakers produce slower sperm. Our results highlight that social interactions among males can influence sperm and ejaculate production. © 2021 by the authors. Licensee MDPI, Basel, Switzerland.

Abstract Understanding the thermal sensitivity of reproductive interactions is crucial given global warming. Previous studies have almost exclusively focused on interactions before mating, even though important interactions between the sexes also occur after mating (e.g. gamete interactions), which are likely also affected by temperature. Thus, it remains unknown how temperature affects the influence of female reproductive fluid on sperm performance, thereby altering female control over fertilization (cryptic female choice). This gap limits our understanding of how sexual selection changes with seasonal temperature fluctuations and temperatures outside the range of historical norms. We tested how temperatures relevant to current conditions and climate change projections influence the mechanisms underlying cryptic female choice in a marine fish, Symphodus ocellatus . Under typical, cooler thermal conditions, female reproductive fluid enhances sperm velocity and biases fertilization dynamics to favour preferred, dominant males over sneaker males. We find that warmer temperatures decrease female influence on sperm velocity, especially for dominant males. This results in dominant males having slower sperm than sneaker males at warmer temperatures, reducing the expected paternity of preferred, dominant males. Our results highlight that considering the thermal sensitivity of female–male interactions that occur after mating will be essential for understanding how seasonal variation and climate change can influence fertility, reproduction and sexual selection. Read the free Plain Language Summary for this article on the Journal blog.

(1) Understanding the thermal sensitivity of reproductive interactions is crucial given global warming. Previous studies have almost exclusively focused on interactions before mating, even though important interactions between the sexes also occur after mating (e.g., gamete interactions), which are likely affected by temperature. (2) Thus, it remains unknown how temperature affects the influence of female reproductive fluid on sperm performance, thereby altering female control over fertilization (cryptic female choice). This gap limits our understanding of how sexual selection changes with seasonal temperature fluctuations and temperatures outside the range of historical norms. (3) We tested how temperatures relevant to current conditions and climate change projections influence the mechanisms underlying cryptic female choice in a marine fish, Symphodus ocellatus. Under typical thermal conditions, female reproductive fluid enhances sperm velocity and biases fertilization dynamics to favor preferred, dominant males over sneaker males. (4) We find that warmer temperatures decrease female influence on sperm velocity, especially for dominant males. This results in dominant males having slower sperm than sneaker males at warmer temperatures, reducing the expected paternity of preferred, dominant males. (5) Our results highlight that considering the thermal sensitivity of female-male interactions that occur after mating will be essential for understanding how seasonal variation and climate change can influence fertility, reproduction, and sexual selection.

Abstract Reproduction is often more thermally sensitive than survival. Thus, understanding the thermal sensitivity of reproductive interactions is crucial given global warming. However, it is unknown how temperature influences female control over fertilization after mating ( i.e., cryptic female choice). We tested how temperatures relevant to current conditions and climate change projections influence cryptic female choice in a marine fish, Symphodus ocellatus . Under typical conditions, females bias fertilization dynamics to favor dominant males. We find that warmer temperatures decrease female influence on sperm velocity and reduce the expected paternity of dominant males. Our results demonstrate that temperatures relevant to climate change can shift the balance between mate choice and male-male competition. Thus, climate change may influence sexual selection, leading to evolutionary changes in reproductive traits.