Challenging monogamy in a spider with nontraditional sexual behavior

Abstract

Each species and sex can develop different reproductive strategies to optimize their fitness while assigning reproductive effort. Allocosa senex is a sex-role reversed spider whose males construct long burrows in the sand. They wait for wandering females to approach, assess their sexual partners and donate their constructions to females after copulation. Females stay in the burrow and lay their egg-sac. When offspring are ready for dispersion, females leave the burrow and gain access to new mating opportunities. Males are choosy during mate courtship, preferring to mate with virgin females over copulated ones, which can even be cannibalized if males reject them. This situation turns new mating opportunities dangerous for copulated females. We wondered whether a copulated female inside the previous mate's burrow responds to courtship from a new male and if this new male can copulate, avoiding burrow construction costs. We also explored whether courtship and copulation behaviors during the first sexual encounter affected the probability of occurrence of a second copulation. For that purposes we exposed copulated females inside male burrows to new males (non-donor males). Males could locate and court females inside the previous male's burrow, and females accepted a second copulation. Hence, A. senex females are not monogamous as was expected but increase their reproductive success by copulating with non-donor males. Also, males can develop opportunistic tactics, suggesting a more dynamic mating system for this sex-role reversed spider than assumed.

Figure 1

Scheme of the experiment (above) and flow chart of trials outcome (below). The illustration on (A) represents the first sexual encounter with a burrow-donor male, and the illustration on (B) represents the second sexual encounter with a non-donor burrow male. Arrows indicate the progression of events and/or the circumstances in which they occurred. The numbers of trials are given in parentheses. Since in numerous trials some individuals did not interact with each other and/or did not perform any movement at all, to calculate the real probabilities of courtship and copulation during the sexual encounters, we sub-selected from the total number of interactions those in which at least one of the individuals noticed the other one. We considered the following indicator criteria: (1) the individual remained outside the burrow entrance for at least 5 s, and/or (2) the individual inside the burrow moved towards the burrow entrance.

Figure 2

Courtship and copulation probabilities during first and second sexual encounters of behavioral trials. (A) Female courtship probability, (B) male courtship probability, (C) copulation probability. The gray bars represent the confidence intervals of the marginal mean and black arrows stand for comparisons between means. If the arrow of one mean overlaps with another one, it means there were no significant differences according to Tukey's test and with an alpha value of 0.05.