Evolution of nuptial gifts and its coevolutionary dynamics with male-like persistence traits of females for multiple mating

Background Many male animals donate nutritive materials during courtship or mating to their female mates. Donation of large-sized gifts, though costly to prepare, can result in increased sperm transfer during mating and delayed remating of the females, resulting in higher paternity. Nuptial gifting sometimes causes severe female-female competition for obtaining gifts (i.e., sex-role reversal in mate competition) and selection on females to increase their mating rate, changing the intensity of sperm competition and the resultant paternity gains. We built a theoretical model to simulate such coevolutionary feedbacks between nuptial gift size (male trait) and propensity for multiple mating (female trait). Donation of nuptial gifts sometimes causes development of female persistence trait for gift acquisition. We also analyzed the causes and consequences of this type of traits, taking double receptacles for nutritious seminal gifts, which are known to occur in an insect group with a “female penis” (Neotrogla spp.), as an illustrative example. Results Our individual-based simulations demonstrated that female-female competition for male-derived nutrients always occur when the environment is oligotrophic and mating costs are low for females. However, a positive correlation between donated gift size and the resultant paternity gain was a requisite for the co-occurrence of large gifts and females’ competitive multiple mating for the gifts. When gift donation satisfied female demands and thus resulted in monandry, exaggeration of nuptial gift size also occurred under the assumption that the last male monopolizes paternity. The evolution of double slots for gift acquisition and digestion (female persistence trait) always occurred when males could not satisfy the demands of females for gifts. However, through coevolutionary reduction in male gift size, fixation of this trait in a population drastically reduced the average female fitness. Conclusion Sperm usage patterns, which have rarely been examined for animals with nuptial gifts, can be a critical factor for determining the extent of exaggeration in nuptial gifting. Sex-role reversals in mate competition, as a result of donation of nuptial gifts from males to females, can involve the evolution of male-like, persistent traits in females that reduce population productivity, as is the case with persistence traits in males.

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.

Thermal Preferences of Cowpea Seed Beetles (Callosobruchus maculatus): Effects of Sex and Nuptial Gift Transfers

The thermal environment influences insect performance, but the factors affecting insect thermal preferences are rarely studied. We studied Callosobruchus maculatus seed beetles and hypothesized that thermal preferences are influenced by water balance, with individuals with limited water reserves preferring cooler habitats to reduce evaporative water loss. Adult C. maculatus, in their flightless morph, do not consume food or water, but a copulating male provides a female with a nuptial gift of ejaculate containing nutrients and water. We hypothesized that gift recipients would prefer warmer habitats than gift donors and that both sexes would plastically adjust their thermal preferences according to the size of the transferred gift. We measured the thermal preference in each sex in individuals that were mated once or were unmated. In the mated group, we measured the sizes of the nuptial gifts and calculated proportional body mass changes in each mate during copulation. Supporting the role of water balance in thermal preference, females preferred warmer habitats than males. Nevertheless, thermal preferences in either sex were not affected by mating status or gift size. It is likely that high rates of mating and gift transfers in C. maculatus living under natural conditions promoted the evolution of constitutive sex-dependent thermal preferences.

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.

Evolution of nuptial gifts and its coevolutionary dynamics with “masculine” female traits for multiple mating

ABSTRACTMany male animals donate nutritive materials during courtship or mating to their female mates. Donation of large-sized gifts, though costly to prepare, can result in increased sperm transfer during mating and delayed remating of the females, resulting in a higher paternity Nuptial gifting sometimes causes severe female-female competition for obtaining gifts (i.e., sex-role reversal in mate competition) and female polyandry, changing the intensity of sperm competition and the resultant paternity gains. We built a theoretical model to analyze such coevolutionary feedbacks between nuptial gift size (male trait) and propensity for multiple mating (female trait). Our genetically explicit, individual-based computer simulations demonstrate that a positive correlation between donated gift size and the resultant paternity gain is a requisite for the co-occurrence of large-sized gifts and females’ competitive multiple mating for the gifts. When donation of gifts imposes monandry, exaggeration in nuptial gift size also occurs under the assumption that the last male monopolizes paternity. We also analyzed the causes and consequences of the evolution of a female persistence trait in trading of nuptial gifts, that is, double receptacles for nuptial gifts known to occur in an insect group with a “female penis” (Neotrogla spp.).

How Does the Male Penisfilum Enter the Female Copulatory Pore in Hangingflies?

Hangingflies are characterized by the interesting nuptial feeding behavior and unusual belly-to-belly hanging mating position. However, the mating behavior and the copulatory mechanism remain poorly known for Bittacidae, especially how the elongated male penisfilum enters the copulatory pore of the female. In this study, the mating behavior and copulatory mechanism of Terrobittacus implicatus (Huang and Hua, 2006) were investigated to reveal the functional morphology of hangingfly genitalia. The results show that the male provides a prey as a nuptial gift to the female and twists his abdomen about 180° to form a belly-to-belly hanging mating position. During the penisfilum-entering process, the male epandrial lobes clamp the female subgenital plate with the aid of the female abdomen swelling. Then the male locates the female copulatory pore through his upper branch of the proctiger and inserts his penisfilum into the female spermathecal duct in cooperation with the short setae on the groove of the proctiger. The female subgenital plate where the epandrial lobes clamp is strongly sclerotized and melanized. The copulatory mechanism of Terrobittacus is briefly discussed.