Scott K. Sakaluk

Gecko phonotaxis to cricket calling song: A case of satellite predation

Abstract Insectivorous Mediterranean house geckos, Hemidactylus tursicus, are found in the field close to the burrows of calling male decorated crickets, Gryllodes supplicans. In playback experiments where adult geckos were presented with calls of these crickets or calls of frogs as controls, geckos exhibited positive phonotaxis to broadcast cricket calling song. This indicates that geckos orient to and approach male cricket calls, even though the crickets call from burrows where they are protected from the geckos. However, this behaviour enables the geckos to intercept and consume female crickets that also respond phonotactically to the cricket calls. Thus geckos act as ‘satellite predators’, a situation which may impose sex-biased mortality on female crickets.

FEMALE CONTROL OF SPERM TRANSFER AND INTRASPECIFIC VARIATION IN SPERM PRECEDENCE: ANTECEDENTS TO THE EVOLUTION OF A COURTSHIP FOOD GIFT

Manipulation of ejaculates is believed to be an important avenue of female choice throughout the animal kingdom, but evidence of its importance to sexual selection remains scarce. In crickets, such manipulation is manifest in the premature removal of the externally attached spermatophore, which may afford females an important means of postcopulatory mate choice. We tested the hypothesis that premature spermatophore removal contributes significantly to intraspecific variation in sperm precedence by (1) experimentally manipulating spermatophore attachment durations of competing male Gryllodes sigillatus and (2) employing protein electrophoresis to determine the paternity of doubly mated females. The relative spermatophore attachment durations of competing males had a significant influence on male paternity, but the pattern of sperm precedence deviated significantly from the predictions of an ideal lottery. Instead, paternity data and morphological evidence accorded best with a model of partial sperm displacement derived here. Our model is similar to a displacement model of Parker et al. in that sperm of the second male mixes instantaneously with that of the first throughout the displacement process, but the novel feature of our model is that the number of sperm displaced is only a fraction of the number of sperm transferred by the second male. Regardless of the underlying mechanism, female G. sigillatus can clearly alter the paternity of their offspring through their spermatophore‐removal behavior, and employ such cryptic choice in favoring larger males and those providing larger courtship food gifts. We discuss how female control of sperm transfer and intraspecific variation in sperm precedence may be important precursors to the evolution of gift giving in insects.

Sensory exploitation as an evolutionary origin to nuptial food gifts in insects.

Nuptial food gifts given by males to females at mating are widespread in insects, but their evolutionary origin remains obscure. Such gifts may arise as a form of sensory trap that exploits the normal gustatory responses of females, favouring the selective retention of sperm of gift–giving males. I tested this hypothesis by offering foreign food gifts, synthesized by males of one cricket species, to females of three nongift–giving species. Females provisioned with novel food gifts were ‘fooled’ into accepting more sperm than they otherwise would in the absence of a gift. These results support the hypothesis that nuptial food gifts and post–copulatory female mating preferences coevolve through a unique form of sensory exploitation.

Females use self-referent cues to avoid mating with previous mates

Females of many species mate repeatedly throughout their lives, often with many different males (polyandry). Females can secure genetic benefits by maximizing their diversity of mating partners, and might be expected, therefore, to forego matings with previous partners in favour of novel males. Indeed, a female preference for novel mating partners has been shown in several taxa, but the mechanism by which females distinguish between novel males and previous mates remains unknown. We show that female crickets (Gryllodes sigillatus) mark males with their own unique chemical signatures during mating, enabling females to recognize prior mates in subsequent encounters and to avoid remating with them. Because self-referent chemosensory cues provide females with a simple, but reliable mechanism of identifying individuals with whom they have mated without requiring any special cognitive ability, they may be a widespread means by which females across a broad range of animal mating systems maximize the genetic benefits of polyandry.

Sperm competition and the evolution of nuptial feeding behavior in the cricket, Gryllodes supplicans (Walker)

The pattern of sperm predominance in doubly mated female crickets, Gryllodes supplicans, was investigated using a radiation‐sterility technique. Female G. supplicans made significant use of sperm from both males in fertilizing eggs; overall, first males to mate enjoyed a small advantage, fertilizing about 60% of the offspring produced subsequent to the second mating. The combined use of the sperm of both males in fertilizing eggs occurred soon after the second mating; evidently, mixing of ejaculates within a females spermatheca does occur.

Repeated matings offset costs of reproduction in female crickets

SummaryCourtship food gifts can be a significant source of nutrition to females and costly for males to produce; hence, costs of reproduction should be reduced for multiple-mating females and increased for multiplemating males in a gift-giving species. We tested this hypothesis by experimentally manipulating mating opportunities of males and females of two cricket species,Gryllodes sigillatus, a gift-giving species andGryllus veletis, a non-gift-giving species. Females of both species consume the externally attached spermatophore after mating, but inG. sigillatus, the sperm-containing ampulla is accompanied by a large gelatinous spermatophylax. In both species, survival of mated females given limited access to males was reduced relative to virgin females, thus suggesting a cost of reproduction to females. However, females given unlimited mating opportunities lived as long as virgins and also produced significantly more offspring than limited-access females. These results suggest that benefits of repeated matings, particularly those arising through spermatophore consumption, offset costs of reproduction in females. Lack of a treatment by species interaction suggests that females of both species derive nutritional benefits through spermatophore consumption, and that any additional advantage to the consumption of the spermatophylax inG. sigillatus is offset by more frequent mating byG. veletis females. In contrast to females, varying mating opportunities had no effect on male survival, suggesting that mating effort is not very costly to males. Male survival increased linearly with body mass but only when males were food-deprived, suggesting that larger males possess greater initial energy reserves to sustain their longevity when food-stressed.

The Gin Trap as a Device Facilitating Coercive Mating in Sagebrush Crickets

Female sagebrush crickets (Cyphoderris strepitans) feed on males’ fleshy hind wings during copulation and ingest haemolymph from the wounds they inflict. At the same time, males physically secure females using a specialized, abdominal pinching organ known as a gin trap. Although the gin trap clearly serves a reproductive role, its precise functional significance remains unknown. The objective of the present study was to determine the adaptive significance of the gin trap by independently manipulating the ability of males to provision and secure females during copulation. When the hind wings of males were left intact, there was no difference in the mating success of males with functional and experimentally disabled gin traps, respectively. However, when males’ hind wings were removed, males with functional gin traps experienced a significantly higher mating success than those whose gin traps had been disabled. We conclude that the gin trap functions as a device by which males with insufficient hind-wing material are able to force copulations upon females unwilling to accept their spermatophores.

Post-copulatory mate guarding in decorated crickets

Abstract Although post-copulatory mate guarding occurs in a variety of crickets, its adaptive significance remains largely unknown. Mate guarding may function to prevent females from prematurely removing the externally attached sperm ampulla, thereby ensuring maximum insemination. This hypothesis was tested in decorated crickets, Gryllodes supplicans , by comparing ampulla retention times of females guarded by their mates with those of unguarded females. There was no difference in ampulla attachment duration between the two groups, thus falsifying the ‘ampulla-retention assurance’ hypothesis. Two additional hypotheses related to the function of mate guarding were also tested: (1) mate guarding allows a male to remain in close proximity to his mate during the time it takes to produce a new spermatophore and (2) guarding functions to deter rivals from courting the recently mated female. The ‘spermatophore renewal’ hypothesis was rejected because the average inter-copulatory interval of males greatly exceeded the average guarding duration. The ‘courtship reduction’ hypothesis was supported by four lines of evidence: (1) guarded females were less likely to be courted by intruders than were females whose mates had been removed, (2) unguarded females mounted intruders significantly more often than guarded females, (3) the ampullae of unguarded females were more likely to be partially dislodged by the copulatory attempts of intruding males than were those of guarded females, and (4) guarded females were more likely to be maximally inseminated than were unguarded females.

Hydration benefits to courtship feeding in crickets.

The spermatophore transferred by male decorated crickets (Gryllodes sigillatus) at mating includes a large gelatinous spermatophylax that the female consumes after copulation. Although previous studies have shown that G. sigillatus females gain no nutritional benefits from consuming food gifts, there may be other benefits to their consumption. We examined potential hydration benefits to females by experimentally manipulating both the availability of water and the number of food gifts that females consumed, and by measuring their effect on female fitness. Analysis of the number of nymphs produced by females revealed a significant interaction between the number of spermatophylaxes consumed and water availability. When spermatophylaxes were not provided, females given water ad libitum produced significantly more nymphs than females subjected to water stress. Female longevity was significantly affected by water availability, with an increase in the availability of water corresponding to a significant increase in female longevity. These data suggest that female G. sigillatus accrue fitness benefits by consuming spermatophylaxes when alternative sources of water are unavailable. In addition, females appear to allocate water contained in spermatophylaxes towards reproduction as opposed to survival.

POLYANDRY AND FITNESS OF OFFSPRING REARED UNDER VARYING NUTRITIONAL STRESS IN DECORATED CRICKETS

Abstract.— Females, by mating with more than one male in their lifetime, may reduce their risk of receiving sperm from genetically incompatible sires or increase their prospects of obtaining sperm from genetically superior sires. Although there is evidence of both kinds of genetic benefits in crickets, their relative importance remains unclear, and the extent to which experimentally manipulated levels of polyandry in the laboratory correspond to those that occur in nature remain unknown. We measured lifetime polyandry of free‐living female decorated crickets, Gryllodes sigillatus, and conducted an experiment to determine whether polyandry leads to an increase in offspring viability. We experimentally manipulated both the levels of polyandry and opportunities for females to select among males, randomly allocating the offspring of experimental females to high‐food‐stress or low‐food‐stress regimes to complete their development. Females exhibited a high degree of polyandry, mating on average with more than seven different males during their lifetime and up to as many as 15. Polyandry had no effect on either the developmental time or survival of offspring. However, polyandrous females produced significantly heavier sons than those of monandrous females, although there was no difference in the adult mass of daughters. There was no significant interaction between mating treatment and offspring nutritional regimen in their effects on offspring mass, suggesting that benefits accruing to female polyandry are independent of the environment in which offspring develop. The sex difference in the extent to which male and female offspring benefit via their mothers polyandry may reflect possible differences in the fitness returns from sons and daughters. The larger mass gain shown by sons of polyandrous females probably leads to their increased reproductive success, either because of their increased success in sperm competition or because of their increased life span.