Sperm Storage Costs Determine Survival and Immunocompetence in Newly Mated Queens of the Leaf-Cutting Ant Atta colombica

In the leaf-cutting ant Atta colombica, queens receive ejaculates from multiple males during one single mating event early in their lives. A queen’s fertility and fitness therefore depend on maximizing the number of sperm cells she can store and maintain inside her spermatheca. Previous studies implied significant physiological mating costs, either originating from energetic investments maximizing sperm survival, or from resolving sexual conflicts to terminate male-driven incapacitation of rival sperm via serine proteases found in seminal fluid. Here we conducted an artificial insemination experiment, which allowed us to distinguish between the effects of sperm and seminal fluid within the queen’s sexual tract on her survival and immunocompetence. We found significantly higher mortality in queens that we had inseminated with sperm, independently of whether seminal fluid was present or not. Additionally, after receiving sperm, heavier queens had a higher probability of survival compared to lightweight queens, and immunocompetence decreased disproportionally for queens that had lost weight during the experiment. These findings indicate that queens pay significant physiological costs for maintaining and storing sperm shortly after mating. On the other hand, the presence of seminal fluid within the queens’ sexual tract neither affected their survival nor their immunocompetence. This suggests that the energetic costs that queens incur shortly after mating are primarily due to investments in sperm maintenance and not costs of terminating conflicts between competing ejaculates. This outcome is consistent with the idea that sexually selected traits in social insects with permanent castes can evolve only when they do not affect survival or life-time fitness of queens in any significant way.

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.

Males increase their fitness by choosing large females in the common bedbug Cimex lectularius

Mate choice is often a role assigned to females. Already Darwin realised that males are eager to copulate, and females are choosy. However, male mate choice is not as rare as assumed. Males should choose females if females vary in quality, i.e., fecundity. Indeed, males often choose larger mates and through this preference increase fitness benefits. In addition, if mating costs reduce the number of copulations a male can potentially perform, he should be choosy. Bedbug females vary in their fecundity and female size is positively related to fecundity. Male bedbugs are limited in seminal fluid availability and, hence, the number of consecutive matings they can perform. Traumatic insemination gives males full control over mating, therefore low female mating resistance could further allow males to be choosy. Here, using mate choice arenas, we investigated if male bedbugs prefer to mate with large females. We observed mating behaviour and measured female fecundity to investigate potential male fitness benefits. Males chose to mate with large females 1.8 times more often than small females and large females laid significantly more eggs than small females. Our study provides first evidence for male mate choice based on female body size in bedbugs and males can increase their fitness by mating large females. It has to be further established if male mate choice is driven by mating costs in terms of ejaculate investment and if such male mate choice based on female size could be a driver of sexual size dimorphism in bedbugs.

Costs and benefits of mating with fertilized females in a species with first male sperm precedence

SummaryDifferent patterns of sperm precedence are expected to result in specific mating costs and benefits for each sex, generating different selection pressures on males and females. However, most studies concern species with mixed paternity or last male sperm precedence, neglecting species with first male sperm precedence, in which only the first mating is effective.Here, we measured costs and benefits of multiple mating for both sexes of the spider mite Tetranychus urticae. First, we assessed the stability of the sperm precedence pattern, by mating females to one, two or several males, immediately after the first mating or 24 hours later. We found complete first male precedence, independently of the mating interval and the number of matings. Females paid a cost of polyandry, as multiply-mated females laid fewer eggs than once-mated females. However, while first males had reduced survival when exposed to an intermediate number of virgin females, second males paid no additional costs by matings with several mated females. Moreover, by mating multiply with mated females, males decreased the total number of offspring sired by first males, which suggests that these matings may entail a relative benefit for second males, despite being ineffective.Our results show that complex costs and benefits may arise in males in species with first male precedence. How these costs and benefits affect the maintenance of selection for polyandry remains an open question.

Evolution of male and female choice in polyandrous systems

We study the evolution of male and female mating strategies and mate choice for female fecundity and male fertilization ability in a system where both sexes can mate with multiple partners, and where there is variation in individual quality (i.e. in the availability of resources individuals can allocate to matings, mate choice and production of gametes). We find that when the cost of mating differs between sexes, the sex with higher cost of mating is reluctant to accept matings and is often also choosy, while the other sex accepts all matings. With equal mating costs, the evolution of mating strategies depends on the strength of female sperm limitation, so that when sperm limitation is strong, males are often reluctant and choosy, whereas females tend to accept available matings. Male reluctance evolves because a male's benefit per mating diminishes rapidly as he mates too often, hence losing out in the process of sperm competition as he spends much of his resources on mating costs rather than ejaculate production. When sperm limitation is weaker, females become more reluctant and males are more eager to mate. The model thus suggests that reversed sex roles are plausible outcomes of polyandry and limited sperm production. Implications for empirical studies of mate choice are discussed.

Male moths that shed their genital spines inside the female: A survey of male mating costs and material investment during copulation

In some insects, males produce costly ejaculates that reduce the typical sexual imbalance in potential reproductive rates thus influencing the mode and intensity of sexual selection. In Lepidoptera, in particular, males tend to invest heavily in mate searching, courtship and ejaculate production; furthermore, in some species males shed genital spines (deciduous cornuti) within the female genital tract during copulation. We studied experimentally the potential mating costs incurred by males of a moth with deciduous cornuti, Amorbia cuneana (Tortricidae). In the first experiment, we tested the prediction that mating costs result in a reduction in male longevity and survival rate. Our results did not support this prediction because virgin and mated males had similar longevity and survival rate. This result is somewhat surprising considering the substantial resource investment in mating found in the second experiment. In their first mating males invested in the ejaculate 9% of their body weight and transferred virtually all their deciduous cornuti; furthermore, few males were able to mate a second time (although we do not know if this was due to female rejection), these males produced smaller ejaculates and there was no evidence of cornuti regrowth. We hypothesize that reduced mating opportunities have selected for males that are ready to transfer large ejaculates at any moment and thus against the diversion of resources from reproductive tissues to somatic maintenance in unmated males; the transfer of the full set of deciduous cornuti in first copulations is consistent with this hypothesis.

Male moths that shed their genital spines inside the female: A survey of male mating costs and material investment during copulation

In some insects, males produce costly ejaculates that reduce the typical sexual imbalance in potential reproductive rates thus influencing the mode and intensity of sexual selection. In Lepidoptera, in particular, males tend to invest heavily in mate searching, courtship and ejaculate production; furthermore, in some species males shed genital spines (deciduous cornuti) within the female genital tract during copulation. We studied experimentally the potential mating costs incurred by males of a moth with deciduous cornuti, Amorbia cuneana (Tortricidae). In the first experiment, we tested the prediction that mating costs result in a reduction in male longevity and survival rate. Our results did not support this prediction because virgin and mated males had similar longevity and survival rate. This result is somewhat surprising considering the substantial resource investment in mating found in the second experiment. In their first mating males invested in the ejaculate 9% of their body weight and transferred virtually all their deciduous cornuti; furthermore, few males were able to mate a second time (although we do not know if this was due to female rejection), these males produced smaller ejaculates and there was no evidence of cornuti regrowth. We hypothesize that reduced mating opportunities have selected for males that are ready to transfer large ejaculates at any moment and thus against the diversion of resources from reproductive tissues to somatic maintenance in unmated males; the transfer of the full set of deciduous cornuti in first copulations is consistent with this hypothesis.

Costs of deception and learned resistance in deceptive interactions

The costs that species suffer when deceived are expected to drive learned resistance, although this relationship has seldom been studied experimentally. Flowers that elicit mating behaviour from male insects by mimicking conspecific females provide an ideal system for such investigation. Here, we explore interactions between a sexually deceptive daisy with multiple floral forms that vary in deceptiveness, and the male flies that pollinate it. We show that male pollinators are negatively impacted by the interaction, suffering potential mating costs in terms of their ability and time taken to locate genuine females within deceptive inflorescences. The severity of these costs is determined by the amount of mating behaviour elicited by deceptive inflorescences. However, inexperienced male flies exhibit the ability to learn to discriminate the most deceptive inflorescences as female mimics and subsequently reduce the amount of mating behaviour they exhibit on them with increased exposure. Experienced males, which interact with sexually deceptive forms naturally, exhibit similar patterns of reduced mating behaviour on deceptive inflorescences in multiple populations, indicating that pollinator learning is widespread. As sexually deceptive plants are typically dependent on the elicitation of mating behaviour from male pollinators for pollination, this may result in antagonistic coevolution within these systems.