RESUMEN

Past reproductive effort allows males to assess their ability to acquire mates, but it also consumes resources that can reduce their future competitive ability. Few studies have examined how a male's reproductive history affects his subsequent mate choice, and, to date, no study has determined the relative contribution of past mating behavior and past ejaculate production because these two forms of investment are naturally highly correlated. Here, we disentangled the relative effects of past mating behavior and past ejaculate production in mosquitofish (Gambusia holbrooki) by experimentally preventing some males from ejaculating when trying to mate. We assessed the effect of mating behavior on mate choice by comparing males that had previously been with or without access to females and male rivals for 8 and 16 weeks and assessed the effect of ejaculation on mate choice by comparing males that either could or could not ejaculate when they had access to females for 16 weeks. Reproductive treatment did not affect male attractiveness, but it did affect male mate choice. Somewhat surprisingly, in five of the six treatment-by-age at testing combinations, males preferred a female in the vicinity of a male rival over a solitary female. This preference was marginally stronger for males that had previously engaged in mating behavior but were unaffected by past ejaculate production. We discuss the potential benefits to males of associating with another male when seeking mates. This is the first study to quantify the relative influence of pre- and post-copulatory reproductive investment on male mate choice.

RESUMEN

Many studies ask whether young or older males are better at acquiring mates. Even so, how age affects reproductive success is still poorly understood because male age and mating history are confounded in most studies: older males usually have more mating experience. To what extent does mating history rather than age explain variation in male mating success? And how do mating history and male age determine paternity when there is also postcopulatory sexual selection? Here, we experimentally manipulated the mating history of old and young males in the eastern mosquitofish (Gambusia holbrooki). We then recorded male mating behavior and share of paternity (1259 offspring from 232 potential sires) when they competed for mates and fertilizations. Old males, and males with no mating experience, spent significantly more time approaching females, and attempting to mate, than did young males and those with greater mating experience. Male age and mating history interacted to affect paternity: old males benefited from having previous mating experience, but young males did not. Our results highlight that the age-related changes in male reproductive traits and in paternity that have been described in many taxa may be partly attributable to male mating history and not simply to age itself.

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RESUMEN

Older males often perform poorly under post-copulatory sexual selection. It is unclear, however, whether reproductive senescence is because of male age itself or the accumulated costs of the higher lifetime mating effort that is usually associated with male age. To date, very few studies have accounted for mating history and sperm storage when testing the effect of male age on sperm traits, and none test how age and past mating history influence paternity success under sperm competition. Here, we experimentally manipulate male mating history to tease apart its effects from that of age on ejaculate traits and paternity in the mosquitofish, Gambusia holbrooki. We found that old, naive males had more sperm than old, experienced males, while the reverse was true for young males. By contrast, neither male age nor mating history affected sperm velocity. Finally, using artificial insemination to experimentally control the number of sperm per male, we found that old males sired significantly more offspring than young males independently of their mating history. Our results highlight that the general pattern of male reproductive senescence described in many taxa may often be affected by two naturally confounding factors, male mating history and sperm age, rather than male age itself.

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Female behavior changes profoundly after mating. In Drosophila, the mechanisms underlying the long-term changes led by seminal products have been extensively studied. However, the effect of the sensory component of copulation on the female's internal state and behavior remains elusive. We pursued this question by dissociating the effect of coital sensory inputs from those of male ejaculate. We found that the sensory inputs of copulation cause a reduction of post-coital receptivity in females, referred to as the "copulation effect." We identified three layers of a neural circuit underlying this phenomenon. Abdominal neurons expressing the mechanosensory channel Piezo convey the signal of copulation to female-specific ascending neurons, LSANs, in the ventral nerve cord. LSANs relay this information to neurons expressing myoinhibitory peptides in the brain. We hereby provide a neural mechanism by which the experience of copulation facilitates females encoding their mating status, thus adjusting behavior to optimize reproduction.

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In insects, like in other animals, experience-based modulation of preference, a form of phenotypic plasticity, is common in heterogeneous environments. However, the role of multiple fitness-relevant experiences on insect preference remains largely unexplored. For the multivoltine polyphagous moth Spodoptera littoralis we investigated effects of larval and adult experiences on subsequent reproductive behaviours. We demonstrate, for the first time in male and female insects, that mating experience on a plant modulates plant preference in subsequent reproductive behaviours, whereas exposure to the plant alone or plant together with sex pheromone does not affect this preference. When including larval feeding experiences, we found that both larval rearing and adult mating experiences modulate host plant preference. These findings represent the first evidence that host plant preferences in polyphagous insects are determined by a combination of innate preferences modulated by sensory feedback triggered by multiple rewarding experiences throughout their lifetime.

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In the present study, we report that contact with isolated female antenna significantly increases both the pheromone 3-hydroxy-2-butanone (3H-2B) release and the hemolymph JH III level in all examined aggressive posture-adopting (AP) and NP (non-AP-adopting) socially naïve males, with significantly faster concomitant pre-mating wing-raising behavior in AP as compared to NP males. 3H-2B release and JH III level were significantly increased after mating in both AP and NP males. A positive correlation was observed between mating experience and dominant status. Furthermore, mated-AP males initiated fights more rapidly and fought for a significantly longer duration than mated-NP males; retention with the paired female for 24h did not affect this increase. JH III level and 3H-2B release were significantly increased in dominant males as compared to subordinates. These results suggest that prior mating experience in invertebrates may enhance aggression in subsequent male-male encounters, with accompanying physiological (hormone and pheromone) responses.

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