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.

Dodging sexual conflict?—Sub‐adult females of a web‐building spider stay cryptic to mate‐seeking adult males

“…Being cryptic to males is adaptive to sub‐adult females that are in sexual conflict with adult males cohabiting their webs. Cohabiting males kleptoparasitize and curtail the female's opportunity for prey capture (Erez et al, ; Segev et al, ) and mate cannibalism (Biaggio et al, ; Uhl et al, ).…”

“…Similarly, mate‐seeking adult males of web‐building spiders often cohabit the webs of sessile sub‐adult (i.e. penultimate instar) females (Anava & Lubin, ; Bel‐Venner & Venner, ; Biaggio, Sandomirsky, Lubin, Harari, & Andrade, ; Dodson & Beck, ; Eberhard, Guzmàn‐Gòmez, & Catley, ; Fahey & Elgar, ; Jackson, ; Miller & Miller, ; Miyashita & Hayashi, ; Segev, Ziv, & Lubin, ; Uhl et al, ; Watson, ). In this context, sub‐adult females of the linyphiid spider Neriene litigiosa have been particularly well studied (Watson, ).…”

“…Kleptoparasitism (Erez, Schneider, & Lubin, ; Segev et al, ) and diminished risk of sexual cannibalism coupled with maximum life time reproductive fitness (Biaggio et al, ; Uhl et al, ) are distinct benefits for a cohabiting spider male. For example, males of the araneid Argiope bruennichi often cohabit with sub‐adult females and mate with them as they moult to adults, thus greatly reducing the risk of sexual cannibalism (Uhl et al, ).…”

“…For example, males of the araneid Argiope bruennichi often cohabit with sub‐adult females and mate with them as they moult to adults, thus greatly reducing the risk of sexual cannibalism (Uhl et al, ). Similarly, males of the black widow Latrodectus hasselti chew open the cuticle to the epigyne of sub‐adult females and then mate with them, thus avoiding cannibalism (Andrade, ; Biaggio et al, ). However, sexual cannibalism of males can also be considered a trade‐off between a male's paternal investment (self‐sacrifice to nutrient‐provision the female) and increased life time reproductive fitness (Buskirk, Frohlich, & Ross, ).…”

“…Sub‐adult females of some spider taxa incur multiple costs from a cohabitating male, including reduced prey capture, kleptoparasitism by the male with deleterious effects on their nutrient intake and well‐being (Erez et al, ; Segev et al, ; Watson, ), and curtailed opportunity for mate choice or mate cannibalism, losing nutrient intake from cannibalized males (Biaggio et al, ; Buskirk et al, ; Uhl et al, ). On the other hand, females may benefit through “passive” mate choice, essentially mating the cohabiting male that has successfully fended off all rivals (Watson, ).…”