Do the Size and Age of Mating Plugs Alter Their Efficacy in Protecting Paternity?
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Behav Ecol Sociobiol (2014) 68:1321–1328 DOI 10.1007/s00265-014-1742-7 ORIGINAL PAPER Do the size and age of mating plugs alter their efficacy in protecting paternity? Katrin Kunz & Melanie Witthuhn & Gabriele Uhl Received: 19 November 2013 /Revised: 28 April 2014 /Accepted: 9 May 2014 /Published online: 10 June 2014 # Springer-Verlag Berlin Heidelberg 2014 Abstract An obvious means to secure paternity is the pro- of theoretical considerations on the evolution of effective duction of a mating plug that blocks the female genital open- mating plugs. ing after mating. Although the mechanical efficacy and per- sistence of plugs on/in the female genital openings are key Keywords Mating plug . Sexual selection . Sperm traits that determine the degree of paternity protection, these competition . Monopolization . Paternity protection . Dwarf factors have hardly been explored. We therefore investigated spider . Erigoninae the influence of the size of the amorphous plug material (experimentally terminated mating duration as a proxy) and age of the mating plug (time interval between copulations with Introduction two successive males) on the efficacy of the plug by analysing the mating success of subsequent males in the dwarf spider In polyandrous species, post-copulatory male-male competi- Oedothorax retusus (Linyphiidae: Erigoninae). Overall, sub- tion occurs if sperm of different males are stored within the sequent males attempted to mate in 82 % of trials but only female genital tract (Parker 1970). Polyandry is widespread in 32.5 % of these resulted in copulation, demonstrating that the various animal taxa and has led to numerous behavioural, plugs are effective safeguards against remating. Remating physiological and morphological male adaptations against probability was significantly higher after previous short cop- sperm competition (Birkhead and Møller 1998;Parker1998; ulations (~small plug size) compared to long copulations Simmons 2001; Eberhard 2009). Adaptations can be offensive (~large plug size). In the small plug group, fresh plugs (short by reducing mating success of previous males or defensive by remating intervals) were significantly less effective compared impeding or reducing further matings of the female (Parker to older plugs. In the large plug group, remating probability 1970). Offensive adaptations are, for example, when rival was similarly low over all remating intervals. The observed sperm are scraped out of the female genital tract (Simmons copulations, however, do not necessarily result in sperm trans- 2001), displaced and/or replaced (e.g. Gack and Peschke fer, since sperm masses were found on the plugged female 1994) or sealed off with a hardening ejaculate (Diesel 1990). genital area. Our study on O. retusus shows that mating plugs A classical defensive male adaptation against multiple female are a powerful mechanical safeguard whose efficacy varies mating is the production of a mating plug. Mating plugs are with plug size and age. We discuss these findings in the light structures that mechanically block female genital openings after mating and reduce female remating probabilities or im- pede further matings, thereby securing paternity of the plug- producing male (Simmons 2001). Mating plugs are known Communicated by M. Elgar : : from virtually all animal groups (Birkhead and Møller 1998). K. Kunz (*) M. Witthuhn G. Uhl However, material on or in the female genital openings is Zoological Institute and Museum, Department of General and often assumed to function as a mating plug without investi- Systematic Zoology, University of Greifswald, Anklamer Straße 20, 17489 Greifswald, Germany gating whether it actually limits remating probability of the e-mail: [email protected] female. The materials may serve other functions than paternity G. Uhl protection such as preventing sperm leakage and may even be e-mail: [email protected] produced by the female (e.g. Aisenberg and Barrantes 2011). 1322 Behav Ecol Sociobiol (2014) 68:1321–1328 Moreover, even if the materials were demonstrated to serve as be used as a proxy for plug size and (ii) on plug age taken as the paternity protection devices, the conditions and constraints time interval between first copulation and the second mating that shape their efficacy are still largely underexplored. trial (15 min; 1 h; 1 day; 3 days after mating; after oviposition). Supposed mating plugs were found in many spider families Since cleaning behaviour by the female may potentially alter (Austad 1984; Uhl et al. 2010). The genital morphology of plug presence and size, we observed if females cleaned the entelegyne spiders seems to promote the occurrence of mating genital region during 1 h post-mating. When subsequent males plugs since females possess three genital openings—two are attempted or succeeded in remating, we investigated the con- used for copulation and one for oviposition (Uhl et al. 2010). dition of the mating plugs under the SEM. In order to test if This allows the male to obstruct the copulatory ducts without female receptivity and attractiveness to males may depend on impeding oviposition. Further, spiders possess a high potential plug size and age, we further registered aggressive behaviour for sperm competition since females frequently mate with by females towards males and male courtship probability. several males, and sperm can be stored over long periods of time in the female genital tract (Elgar 1998). Supposed mating plugs in spiders consist primarily of amorphous material but Material and methods can also consist of parts of or complete male pedipalps, the secondary copulatory organs (Uhl et al. 2010). Recently, Study species: O. retusus genital fragments were shown to be effective plugs in the orb-weaver Argiope keyserlingi (Herberstein et al. 2012). The dwarf spider O. retusus belongs to the Erigoninae (Miller However, in many species, several male fragments can be and Hormiga 2004) which is the largest group within the found in the female genital system, demonstrating that subse- Linyphiidae. We used males and females that were raised in quent matings are possible (Uhl et al. 2010). the laboratory from egg sacs of females caught along the Here, we focus on amorphous materials on/in the female banks of the river Rhine south of Bonn, Germany (50° 43′ genital opening since this type of potential mating plug is 00.26″ N, 7° 08′ 25.11″ E–50° 42′ 57.40″ N, 7° 08′ 36.70″ E). particularly widespread in the animal kingdom including spi- Adult spiders were kept individually in 25 ml plastic con- ders (Uhl et al. 2010). When the material is transferred from tainers equipped with a moist layer of gypsum at a temperature the male to the female, it must be transferred in a liquid state of 23/17 °C (day/night) and 70 % humidity. They were fed and has to solidify to a certain degree if it is meant to withstand weekly with four to six fruit flies, Drosophila melanogaster. penetration or removal by a rival male. We therefore hypoth- Spiderlings were fed ad libitum on springtails, Sinella esize that plugs are not as effective immediately after their curviseta, until the subadult stage (Kunz et al. 2012). placement compared to after curing. Since a plug only helps to secure paternity if it remains functional until oviposition, the Courtship and copulation in O. retusus degree of persistence of the material is a further crucial aspect that determines paternity success. Furthermore, plug efficacy Courtship in O. retusus starts with the male vibrating his may strongly depend on plug size if large amounts of material opisthosoma. As soon as the male achieves the contralateral are more difficult to remove compared to small amounts (e.g. mating position, he stretches one of his pedipalps (secondary Masumoto 1993; Polak et al. 2001). In the butterfly Cressida copulatory organs) towards the external female genital struc- cressida, large mating plugs even present lifelong chastity ture (epigyne) and tries to insert into one of two female belts (Orr and Rutowski 1991). copulatory openings. Copulation starts when the male suc- In this study, we follow up on findings in the dwarf spider cessfully inserts a pedipalp into the corresponding female Oedothorax retusus (Linyphiidae: Erigoninae) in which an copulatory opening and the hematodocha (membranous part amorphous mass is found on the female copulatory opening of the sperm transfer organ) inflates. The insertion mode is after mating (Uhl and Busch 2009). Mating plugs are signif- ipsilateral, meaning that the right pedipalp is inserted into the icantly larger after longer matings which allows using copu- right female copulatory opening, which is typical for lation duration as a proxy for plug size (Uhl and Busch 2009). entelegyne spiders (Huber and Senglet 1997). A mating plug When experimentally terminating matings after 1 or 3 min, in O. retusus appears as a transparent mass shortly after small mating plugs proved to be ineffective but large plugs copulation that transforms into solid opaque material (Kunz prevented remating of the female in 93 % of cases. In this and Witthuhn, personal observations). previous study, all remating trials were staged within 15 min. However, in order to understand the full potential and limita- Influence of plug size and age on paternity protection tions of mating plugs, we need to assess how plug size, plug age and their interaction determine plug efficacy. We investigated plug efficacy of O. retusus by staging We hypothesize that mating plug efficacy in O. retusus remating trials that varied in plug size as determined by first depends (i) on first mating duration (short, long) which can male copulation durations (Uhl and Busch 2009) and plug age Behav Ecol Sociobiol (2014) 68:1321–1328 1323 as determined by latencies between first and second matings. Scanning electron microscopy To make sure that both first and second males used the same of the two female genital openings, one of the two pedipalps of Female opisthosomata (N=143) of those trials in which each male was amputated on the same side.