Differential allocation in a gift-giving spider: males adjust their reproductive investment in response to female condition

Background When males are selective, they can either reject low-quality females or adjust their reproductive investment in response to traits that indicate female quality (e.g., body size or condition). According to the differential allocation hypothesis, males increase their reproductive investment when paired with high-quality females (positive differential allocation) or increase their reproductive investment when paired with low-quality females (negative differential allocation). This hypothesis has been proposed for monogamous species with biparental care, and most empirical studies focus on birds. Here we used the polygamous spider Paratrechalea ornata, in which males offer prey wrapped in silk as nuptial gifts, to test whether males adjust their reproductive investment in gift size, pre-copulatory and copulatory courtship, and sperm transfer in response to female body condition. Results Males exposed to females in good body condition added more flies to the gift, stimulated these females longer with abdominal touches during pre-copulatory courtship, and had longer pedipalp insertions than males exposed to females in poor body condition. Female condition affected neither silk investment in nuptial gift wrapping nor the quantity of sperm transferred by males. Finally, females in good body condition oviposited faster after copulation and laid more eggs than females in poor body condition. Conclusions We provide experimental evidence that males of a gift-giving spider exhibit positive differential allocation in three key aspects of their reproductive investment: the size of the nutritious gift, duration of pre-copulatory courtship, and duration of pedipalp insertions, which is regarded as a form of copulatory courtship in spiders. This positive differential allocation is likely associated with the benefits of copulating with females in good body condition. These females are more fecund and oviposit faster after copulation than females in poor body condition, which under natural field conditions probably reduces the risk of multiple matings and thus the level of sperm competition faced by the males. As a final remark, our findings indicate that the hypothesis of differential allocation also applies to species with a scramble competition mating system, in which males heavily invest in nuptial gift construction, but not in parental care.

Condition-dependent differences in male vibratory pre-copulatory and copulatory courtship in a nuptial gift-giving spider

Condition-dependent secondary sexual traits and signals are often crucial for mate choice decisions. Nuptial gifts, provided by the male to the female during mating, may represent an indicator of male condition, especially if production of the gift is energetically costly. Additionally, other signalling modalities may well play a role in mate choice in such systems. Females of the nursery web spider Pisaura mirabilis preferably mate with males that provide a prey item wrapped in silk. Apart from the nuptial gift, vibrational signals employed during courtship and mating may reveal additional information about male condition. We tested condition-dependence of male vibrational signals of well-fed versus starved males, when in contact with female dragline silk and during mating trials. Our results show that vibrational signals are produced in P. mirabilis, both during pre-copulatory courtship and during copulation. Male courtship signals were condition-dependent: males in good condition initiated signalling earlier and emitted more vibrational pulses than poor-condition males. They were also more likely to be accepted by the female for copulation. We additionally identified vibrational signals during copulation. These signals were different from pre-copulatory courtship vibrations but did not differ between the treatment groups. This study shows that vibrational communication plays an important role before and during copulation in P. mirabilis. It sets the stage for further experiments on spider biotremology associated with nuptial gift giving behaviour. Significance statement Male courtship behaviour can indicate a male’s condition and quality and be subject to female mate choice. Vibrational communication during mating plays a crucial role in many animal species. Spiders are known to be extremely sensitive towards vibrations, and there is evidence that vibratory signals are also used during courtship. Here, we study the nuptial gift-giving spider Pisaura mirabilis in which courtship entails providing a nuptial gift by the male to the female. The gift quality determines on the probability and duration of mating. We investigated the role of vibrational behaviour in this species by standardizing nuptial gifts. Our study demonstrates that vibratory signals comprise information about the male’s condition, that signals are also produced during mating and that courtship and copulatory signals are strikingly different. We suggest that vibrational communication provides important condition-dependent traits for female mate choice in addition to the nuptial gift.

Female perception of copulatory courtship by male titillators in a bushcricket

Males of the bushcricket Metrioptera roeselii bear paired titillators that are spiny genital structures supposedly functioning as copulatory courtship devices. During copulation, the male inserts its titillators into the female's genital chamber, where they rhythmically tap on the sensilla-covered dorsal surface of the genital fold. Here, we investigated the stimulatory function of male titillators during mating in M. roeselii . Tracer backfills of presumptive mechanosensory sensilla at the female genital fold revealed a thick bundle of sensory axons entering the last unfused abdominal ganglion (AG-7). Electrophysiological recordings of abdominal nerves demonstrated that females sense mechanical stimulation at their genital fold. The mechanosensory responses, however, were largely reduced by the insecticide pymetrozine that selectively blocks scolopidia of internal chordotonal organs but not campaniform and hair sensilla on the outer cuticle surface. In mating experiments, the females showed resistance behaviours towards males with asymmetrically shortened titillators, but the resistance was largely reduced when mechanoreceptors at the female's genital fold were either pharmacologically silenced by pymetrozine or mechanically blocked by capping with UV-hardened glue. Our findings support the hypothesis that the male titillators in these bushcrickets may serve as copulatory courtship devices to mechanically stimulate the female genitalia to reduce resistance behaviour.

Sexual behavior of the desert locust during intra-and inter-phase interactions

Mating and reproduction behaviors and strategies are fundamental aspects of an organism’s evolutionary and ecological success. In locusts, intra- as well as inter-phase reproductive interactions among gregarious and solitarious locust populations have a major impact on the locust population dynamics. However, practically all previous work on locust sexual behavior has been limited to the gregarious phase. Here we provide a first detailed description of pre-copulatory behavior of solitarious desert locusts. We compare our findings with those of previous reports of pre-copulatory behavior of gregarious locusts, focusing on the behavioral elements that serve in inter-sex signaling and communication. We also studied inter-phase (mixed pairs) reproductive interactions. Solitarious males were found to invest more in pre-copulatory courtship and signaling compared to their gregarious counterparts; and the solitarious females played a comparatively more dominant role in the inter-sex communication. The solitarious females were also less prone to demonstrate the typical rejection-related behavioral patterns displayed by the gregarious females. As a consequence of the particular characteristic behavior of each phase, the most successful among intra- and inter-phase pairs were gregarious males with solitary females. Least successful were solitary males encountered with gregarious females, indicating a strong asymmetry in inter-phase reproductive interactions. We discuss these results in the context of non-random or assortative mating in locust mixed or sympatric solitarious-gregarious populations.

Serotonergic activation during courtship and aggression in the brown anole,Anolis sagrei

The role of serotonin (5-hydroxytryptamine, 5-HT) in social behavior regulation is not fully understood. While 5-HT release in nuclei of the social behavior network has generally been associated with inhibition of aggressive behavior across multiple classes of vertebrates, less is known about its effects on sexual, especially non-copulatory courtship display behaviors. Furthermore, most research has examined effects at 5-HT release sites, while studies examining the behavioral relevance of source cell populations have generated contradictory findings. This study utilized immunohistochemistry to examine the colocalization of 5-HT with Fos, an immediate early gene product and marker of neural activity, in the raphe and superior reticular nuclei of male brown anoles (Anolis sagrei) exposed to either aggression, courtship, or control social interactions. Supporting previous research, copulation was associated with a decrease in 5-HT activity, while a novel link between 5-HT activity and latency to non-copulatory courtship was also found. Within the aggression group, intensity and frequency of behavior were both associated with decreased 5-HT activity. An effect of social context was also seen, with anoles exposed to either courtship or aggression encounters showing decreased 5-HT activity in certain raphe and superior reticular nuclei populations compared to controls. Interestingly, context effects and behavioral effects were seen at separate brain nuclei, suggesting the presence of separate systems with distinct functional roles.