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Copulation with immature females increases male fitness in cannibalistic widow spiders.

ABSTRACT: Copulatory cannibalism of male 'widow' spiders (genus Latrodectus) is a model example of the extreme effects of sexual selection, particularly in L. hasselti and L. geometricus where males typically facilitate cannibalism by females and mate only once. We show that these males can increase their reproductive success by copulating with final-instar, immature females after piercing the female's exoskeleton to access her newly developed sperm storage organs. Females retain sperm through their final moult and have similar fecundity to adult-mated females. This is an adaptive male tactic because immature mating increases insemination success relative to adult mating (which predicts higher paternity) and moreover, rarely ends in cannibalism, so males can mate again. Although successful only during a brief period before the female's final moult, males may employ this tactic when they associate with final-instar females in nature. Consistent with this, one-third of L. hasselti females collected as immatures in nature were already mated. Immature mating alters sexual selection on these otherwise monogynous males, and may explain male traits allowing facultative polygyny in Latrodectus Since male cohabitation with immature females is common among invertebrates, immature mating may be a widespread, previously unrecognized mating tactic, particularly when unmated females are of high reproductive value.

SUBMITTER: Biaggio MD

PROVIDER: S-EPMC5046930 | biostudies-literature | 2016 Sep

REPOSITORIES: biostudies-literature

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Copulation with immature females increases male fitness in cannibalistic widow spiders.

Biaggio M Daniela MD Sandomirsky Iara I Lubin Yael Y Harari Ally R AR Andrade Maydianne C B MC

Biology letters 20160901 9

Copulatory cannibalism of male 'widow' spiders (genus Latrodectus) is a model example of the extreme effects of sexual selection, particularly in L. hasselti and L. geometricus where males typically facilitate cannibalism by females and mate only once. We show that these males can increase their reproductive success by copulating with final-instar, immature females after piercing the female's exoskeleton to access her newly developed sperm storage organs. Females retain sperm through their final ...[more]

PMID: 27651535

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Project description:BackgroundMating generally occurs after individuals reach adulthood. In many arthropods including spiders, the adult stage is marked by a final moult after which the genitalia are fully developed and functional. In several widow spider species (genus Latrodectus), however, immature females may mate a few days before they moult to adulthood, i.e. in their late-subadult stage. While the "adult" mating typically results in cannibalism, males survive the "immature" mating. During both "immature" and "adult" matings, males leave parts of their paired copulatory organs within female genitalia, which may act as mating plugs. To study potential costs and benefits of the two mating tactics, we investigated female genital morphology of the brown widow spider, L. geometricus. Light microscopy, histology and micro-computed tomography of early-subadult, late-subadult and adult females were conducted to determine the overall pattern of genital maturation. We compared genitalia of mated late-subadult and adult females to reveal potential differences in the genitalic details that might indicate differential success in sperm transfer and different environments for sperm storage and sperm competition.ResultsWe found that the paired sperm storage organs (spermathecae) and copulatory ducts are developed already in late-subadult females and host sperm after immature mating. However, the thickness of the spermathecal cuticle and the staining of the secretions inside differ significantly between the late-subadult and adult females. In late-subadult females mating plugs were found with higher probability in both spermathecae compared to adult females.ConclusionsSperm transfer in matings with late-subadult females follows the same route as in matings with adult females. The observed differences in the secretions inside the spermathecae of adult and late-subadult females likely reflect different storage conditions for the transferred sperm which may lead to a disadvantage under sperm competition if the subadult female later re-mates with another male. However, since males mating with late-subadult females typically transfer sperm to both spermathecae they might benefit from numerical sperm competition as well as from monopolizing access to the female sperm storage organs. The assessment of re-mating probability and relative paternity will clarify the costs and benefits of the two mating tactics in light of these findings.

Project description:IntroductionFemale spiders are fine-tuned to detect and quickly respond to prey vibrations, presenting a challenge to courting males who must attract a female's attention but not be mistaken for prey. This is likely particularly important at the onset of courtship when a male enters a female's web. In web-dwelling spiders, little is known about how males solve this conundrum, or about their courtship signals. Here we used laser Doppler vibrometry to study the vibrations produced by males and prey (house flies and crickets) on tangle webs of the western black widow Latrodectus hesperus and on sheet webs of the hobo spider Tegenaria agrestis. We recorded the vibrations at the location typically occupied by a hunting female spider. We compared the vibrations produced by males and prey in terms of their waveform, dominant frequency, frequency bandwidth, amplitude and duration. We also played back recorded male and prey vibrations through the webs of female L. hesperus to determine the vibratory parameters that trigger a predatory response in females.ResultsWe found overlap in waveform between male and prey vibrations in both L. hesperus and T. agrestis. In both species, male vibrations were continuous, of long duration (on average 6.35 s for T. agrestis and 9.31 s for L. hesperus), and lacked complex temporal patterning such as repeated motifs or syllables. Prey vibrations were shorter (1.38 - 2.59 s), sporadic and often percussive. Based on the parameters measured, courtship signals of male L. hesperus differed more markedly from prey cues than did those of T. agrestis. Courtship vibrations of L. hesperus males differed from prey vibrations in terms of dominant frequency, amplitude and duration. Vibrations of T. agrestis males differed from prey in terms of duration only. During a playback experiment, L. hesperus females did not respond aggressively to low-amplitude vibrations irrespective of whether the playback recording was from a prey or a male.ConclusionsUnlike courtship signals of other spider species, the courtship signals of L. hesperus and T. agrestis males do not have complex temporal patterning. The low-amplitude 'whispers' of L. hesperus males at the onset of courtship are less likely to trigger a predatory response in females than the high-amplitude vibrations of struggling prey.

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Copulation with immature females increases male fitness in cannibalistic widow spiders.

Publications

Copulation with immature females increases male fitness in cannibalistic widow spiders.

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