SR: Post-copulation sexual selection Flashcards
Individuals in socially monogamous species may participate in copulations outside of the pair bond, resulting in extra-pair offspring. Although males benefit from such extra-pair behavior if they produce more offspring, the adaptive function of infidelity to females remains elusive.
Here we show that female participation in extra-pair copulations, combined with a genetically loaded process of sperm competition, enables female finches to target genes that are optimally compatible with their own to ensure fertility and optimize offspring viability. Such female behavior, along with the postcopulatory processes demonstrated here, may provide an adaptive function of female infidelity in socially monogamous animals.
Mate compatibility is signaled by head color, which is determined by a Z-linked gene: Females are hemizygous for this gene (Zr black, ZR red), whereas male genotypes can be homozygous ZrZr (black), ZRZR (red), or heterozygous ZRZr (red). Individuals demonstrate precopulatory mate pref- erences for their own morph type; however, per- haps because of constraints on preferred-mate availability, up to 30% of breeding pairs in wild populations are mixed morph (9).
Extra-pair paternity is determined by the relative genetic compatibility of the WP and EP male with the female. In each predicted context (A to D), the number of eggs fertilized by the social and extra- pair male is shown in laying order, and the average number of copulations each day is provided (above the graph). Conservatively, given that females may store sperm from their social mate (from day –5 to day 1), when both the social and extra-pair males were (A) compatible or (B) incompatible, 4.1 to 5.8% of copulations by the extra-pair male resulted in (A) 28.6% and (B) 27.3% of the offspring produced from the
potentially fertilizable eggs (days 2 to 9; extra-pair males were unable to fertilize eggs laid on days 1 and 2). In contrast, (C) 6.1% of copulations by compatible extra-pair males resulted in 76.5% of the offspring produced when the social mate was incompatible, whereas (D) 3.9% of extra-pair copulations by incompatible extra-pair males resulted in no fertilized eggs when the social mate was compatible. WPC, within-pair copulations; EPC, extra-pair copulations.
We tested for adaptive female participation in extra-pair copulations by presenting captive fe- male Gouldian finches breeding in genetically compatible (social partner of the same genotype) and incompatible social pairs (social partner of different morph), with an opportunity to seek an extra-pair copulation with either a compatible or incompatible male (10). On the day after the female-initiated egg laying (day 1; day 0 = day the first egg is laid), the birds in the social pair were physically and visually separated by an opaque divider, which split the cage in half, and a virgin male in breeding condition was placed with the female for 60 min. In the context of selection for compatible genes (1), this experimental design pro- vided a predicted adaptive context (incompatible social partner and compatible extra-pair partner), a maladaptive context (compatible social partner and incompatible extra-pair partner), and two se- lectively neutral situations (both social and extra- pair partners either incompatible or compatible) (Fig. 1).
Despite morph-assortative mate preferences (9) and selection against mixed morph mating (11), surprisingly, females across all experimental contexts were equally likely to engage in extra- pair behavior [c2 = 0.87, degrees of freedom (df ) = 3, P = 0.83]. Overall, 77.5% (31 of 40) of females copulated with the extra-pair male
Sperm storage mediated by cryptic female choice for nuptial gifts
Maria J. Albo1,2, Trine Bilde1 and Gabriele Uhl3 2013
Females Use Multiple Mating and Genetically Loaded Sperm Competition to Target Compatible Genes
Sarah R. Pryke, Lee A. Rollins, Simon C. Griffith 2010
Polyandrous females are expected to discriminate among males through postcopulatory cryptic mate choice. Yet, there is surprisingly little unequivo- cal evidence for female-mediated cryptic sperm choice. In species in which nuptial gifts facilitate mating, females may gain indirect benefits through preferential storage of sperm from gift-giving males if the gift signals male quality. We tested this hypothesis in the spider Pisaura mirabilis by quantify- ing the number of sperm stored in response to copulation with males with or without a nuptial gift, while experimentally controlling copulation duration. We further assessed the effect of gift presence and copulation duration on egg- hatching success in matings with uninterrupted copulations with gift- giving males.
We show that females mated to gift-giving males stored more sperm and experienced 17% higher egg-hatching success, compared with those mated to no-gift males, despite matched copulation durations. Uninterrupted copulations resulted in both increased sperm storage and egg-hatching success. Our study confirms the prediction that the nuptial gift as a male signal is under positive sexual selection by females through cryptic sperm storage. In addition, the gift facilitates longer copulations and increased sperm transfer providing two different types of advantage to gift-giving in males.
Cryptic mate choice refers to sexual selection during mating (syncopulatory) or afterwards (postcopulatory) that leads to differences in sperm use among com- peting males [1–5]. Species in which nuptial gifts are transferred during mating [6] are particularly promising for studying cryptic mate choice, because gifts that are nutritious to females may be an honest signal of male quality [7]. If nuptial gifts are honest signals of good hunting ability and this trait is heritable, females would benefit from biasing paternity towards males that offer gifts [8]. The potential for acquiring benefits of cryptic choice is particularly high when there is variance in the quality of the nuptial gift
Gift-giving may, for example, be a target for sexually antagonistic coevolution, which favours the evolution of deceit or fake gifts, reducing the benefit of precopulatory female mate choice [9–12]. However, females may counteract deceit by favouring males that present genuine nuptial gifts during or after mating [12]. In nuptial gift-giving species, female preference for genuine gifts is thus expected to favour the evolution of cryptic female mate choice. Whereas the influence of the gift-giving trait on male mating success and the potential for males to exploit female preference for nuptial gifts have attracted much interest [9,11,12], remarkably little is known about cryptic female choice for nuptial gifts.
Cryptic female mate choice should be very common precisely because it is occurring in the genital tract, where females are expected to be
more in control of internal processes after copulation than males
it is intrinsically difficult to control for strategic male sperm allocation [27], and hence to disentangle male- and female-driven processes [28]. Unequivocal evidence of female sperm choice was shown in crickets [25,26], where males form a spermatophore before they encounter the female, and therefore are unable to strategically mediate sperm allocation in response to female phenotype. Preferential storage of sperm from unre- lated males [25], or conspecific males [26], could therefore be attributed to cryptic female choice.
We tested the hypothesis that the nuptial gift is a target of cryptic female choice in the polyandrous spider Pisaura mirabilis (Pisauridae). In this species, males often offer an insect prey wrapped in white silk as a nuptial gift, which the female feeds on during copulation [29]. While it is poss- ible for males to copulate without a gift, gift-giving males experience dramatically higher mating success [12,30,31]. Furthermore, males that offer a nuptial gift achieve longer copulations (100 min on average) than males without a gift (10 min on average), leading to a higher number of fertilized eggs for gift-giving males [12,30,32].
Females appear to have full control over both the initiation and termination of mating [12,30]. Spiders are excellent models for testing female cryp- tic sperm choice, because males use external sperm transfer by modified intromittent organs, the pedipalps, which are loaded with sperm prior to mate searching [33], thus limiting the scope for strategic sperm allocation. Females store sperm from multiple males in sperm storage organs, the sper- matheca, for later fertilization of eggs when she produces an egg-sac.
We tested the effect of gift presence on the number of sperm stored by the female by experimentally terminating copulation duration in males with a gift (GT) to match the average duration of shorter copulations with males without a gift (NG). Following copulation, we determined the number of sperm in the female sperm storage organs. If females bias sperm storage towards males that offer a gift, females in the GT group were expected to store more sperm than females in the NG group. To examine the relationship between copulation duration and sperm storage, we also determined the number of sperm stored after uninter- rupted copulations with gift-giving males (G). Finally, we examined the effect of gift presence and copulation duration on female fecundity and egg-hatching success in an additional set of females mated to NG, GT and G males to gain further insight into benefits of providing a nuptial gift
We collected juveniles and subadults of P. mirabilis (Clerck, 1757) in April 2011 at the Mols Laboratory near Aarhus, Denmark. In the laboratory at Aarhus University, spiders were housed indivi- dually in vials (30 ml) containing moist moss (Sphagnum spp.). Water was provided regularly to maintain humidity. We
raised individuals at room temperature (23.4 + 0.18C) and natural photoperiod and fed them with blowflies (Calliphora sp.) three times per week until maturation.
Males court females by offering the nuptial gift held in their che- licerae while waving their pedipalps (male intromittent organs). Once the female accepts and grasps the gift with her chelicerae, the male initiates sperm transfer by performing alternate inser- tions of the pedipalps into the female genital tract. During copulation, the male retains contact with the gift with the tarsal claws of his third pair of legs, while the female is consum- ing it.
After each insertion, the male returns to a face-to-face position with the female, grabbing the gift with his chelicerae. No courtship in the form of pedipalp waving is performed before the second (and possibly subsequent) palp insertion. Copulation occurs in a similar way in matings with no gift, although these males experience a much reduced acceptance rate [29,34]. In staged mating trials, we registered the number of pedipalp insertions and copulation duration. Copulation dur- ation was recorded from pedipalp insertion until pedipalp disengagement and was calculated as the sum of the duration of all insertions occurring within a trial. Total copulation duration thus represents the time of potential sperm transfer.
Our experimental design included three groups. NG males (n 1⁄4 53) offered no gift and were allowed to copulate without interruption; copulation duration (mean+s.e.): 10.4+1.6min, number of insertions (mean + s.e.): 2.0 + 0.2. GT males (n 1⁄4 39) offered a nuptial gift and had copulation experimentally termi- nated after 10 min to match the average copulation duration of NG males. G males (n 1⁄4 36) offered a gift and were allowed to perform uninterrupted copulations; copulation duration (mean+s.e.): 86.0+6.0 min; number of insertions (mean+s.e.): 4.2+0.6.
Experimental manipulation of the GT group was based on the average copulation duration and number of inser- tions found in the NG group, thus allowing two pedipalp insertions. In the GT group, we terminated the first insertion after 5 min using a paintbrush. Subsequently, we allowed the male to resume copulation and perform the second insertion for another 5 min before the final separation. We analysed the number of sperm transferred in a subset of females, and fecund- ity and egg-hatching success in another subset of females from each of the three experimental groups (see details below).
Staged mating experiments were carried out in May 2011. A female was placed in a transparent plastic cage (22 17 6 cm) with paper-covered bottom at least an hour prior to the exper- iment, allowing her to deposit silk threads. We then removed the female and exposed the male to the female silk for 15 min. In the GT and G groups, a housefly (Musca domestica) was added to the cage which the male caught for gift construction.
After 15 min, we gently reintroduced the female into the cage and mating trials started. NG males were exposed to the same procedure but with no prey available. Male spiders load their pedipalps
(intromittent organs) with sperm after the final moult, and thus prior to mate search and production of nuptial gifts [34]. With this design, we aimed to minimize any effect of the presence or absence of the gift on differential loading of the pedipalps. Males were randomly allocated to the three treatment groups. Individuals used in the experiments were virgins and used only once.
Females were frozen at 2508C between 3 and 6 h after mating (NG: N1⁄439; GT: N1⁄420; G: N1⁄418). For counting the number of sperm transferred, specimens were transferred to the Univer- sity of Greifswald, where the female sperm storage organs were dissected out under a stereomicroscope (ZEISS) and treated by following a protocol established for P. mirabilis ([35], modified after [36]).
The female spermathecae were transferred to 20 ml of saline solution (Casytone, Scha ̈ rfe System). To homogenize samples, we ruptured the spermathecae with forceps and applied ultrasonic treatment. We avoided sample loss by using indirect ultrasonic processing in a cup booster designed for small volumes (Bandelin UW 2070). Ultrasonication was done twice for 30 s at 50% power with a break of 30 s to avoid over- heating of the sample. Afterwards, we centrifuged samples at 5000 g for 1 min and vortexed for 1 min. We placed 10 ml on each counting chamber of the haematocytometer (1 mm Neu- bauer). The sperm were counted in 16 squares under a microscope 400 (Olympus).
The number of sperm in the female spermatheca differed significantly among the three experimental groups (GLM, x2 1⁄4 174442.1, p , 0.0001, d.f. 1⁄4 2, N 1⁄4 52; figure 1a), and was significantly lower in the NG group compared with
the GT group (x2 1⁄4 12165.4, p , 0.0001, d.f. 1⁄4 1, NNG 1⁄4 14, NGT 1⁄4 20; figure 1a). Females in uninterrupted matings with gift-giving males G stored significantly higher numbers of sperm compared with females from the NG and GT groups (x2 1⁄4 162 276.8, p , 0.0001, d.f. 1⁄4 1, p , 0.0001, NG 1⁄4 18, NNG þ GT 1⁄4 34; figure 1a). In the G group, copula- tions resulted in significantly more sperm stored in the female genital tract (Linear regression, effect of copula- tion duration on log sperm number: F1⁄411.6, p1⁄40.004, NG1⁄418; figure 2a). No parametric linear relationship was found in the group of males with no gift (N 1⁄4 39, figure 2a).
Generalized linear models showed that the hatching success differed significantly among groups (x2 1⁄4 235.9, p , 0.0001, d.f. 1⁄4 2; N 1⁄4 51; figure 1b) and was lower in the NG compared with the GT group (x2 1⁄4 92.7, p , 0.0001, d.f. 1⁄4 1, NNG 1⁄4 14, NGT 1⁄4 19). Females in the G group experienced the highest hatching success compared with NG and GT females (x2 1⁄4143.2, p,0.0001, d.f.1⁄41, NG 1⁄418, NNGþGT 1⁄433). We found a positive relationship between copulation duration and hatching success (NG and G pooled, NNGþG 1⁄4 32, GLM binominal: x2 1⁄4 139.9, p , 0.0001; figure 2b).
