Why do male terrestrial isopods (Isopoda: Oniscidea) not guard females?

Precopulatory mate guarding is a male strategy by which female mates are monopolized and is thought to evolve when female receptivity is temporally restricted (Parker 1974; Grafen & Ridley 1983) thus producing a male-biased operational sex ratio (cf. Clutton-Brock & Vincent 1991; Jormalainen et al. 1994). In many aquatic isopods and amphipods, the female is considered receptive only during parturial moult (summarized in Ridley 1983; cf. Table 1), when the marsupium (brood pouch) is developed. In amphipods, sperm is transferred directly into the marsupium to fertilize the simultaneously introduced eggs. By contrast, male isopods exhibit internal insemination and transfer sperm into the female oviduct where it meets the eggs when they are released into the marsupium. This reproductive strategy requires the female be in the parturial moult, since it is probably only then that the morphology of the female’s genital openings makes them accessible to male genitalia (e.g. Ridley 1983). Precopulatory mate guarding has been described in many species of aquatic isopods and amphipods (Table 1), often occurring when female receptivity is restricted. During precopula, both sexes are closely attached to each other and may stay in what is called ‘amplexus’ for several hours, days, or even weeks. In a recent review, Jormalainen (1998) not only summarized the suggested reasons for, and consequences of, monopolization of females by mate-guarding males, but also stressed the idea of precopulatory mate guarding producing intersexual conflict in these species. Initially, precopulatory mate guarding had been assumed to be simply a cost–benefit decision on the part of the male (Parker 1974). However, there may be energetic costs of precopulatory mate guarding in both sexes. In this respect, remarkable differences between species exist, depending on precopulatory behaviour (Table 1). Costs for females may lead to an intersexual conflict over the beginning and the duration of precopula (for summary, see Jormalainen 1998). Thus, females of several species resist the attempts of males to form precopulatory pairs, at least in the early stages of their reproductive cycle (Table 1). Female resistance may in fact be a form of indirect selection for males of higher quality (Ward 1984; Jormalainen et al. 1992; Jormalainen & Merilaita 1993), since only those males are accepted as mates that are strong and/or agile enough to overcome female resistance. If female receptivity is restricted temporally to the parturial intramoult (see above), females will be expected to be temporally monogamous within a single reproductive cycle. However, evidence for multiple mating of females and sperm storage has been presented for several isopod species (cf. Table 1). In sperm-storing terrestrial isopods, for instance, stored spermatozoa remain capable of fertilizing eggs for several months (e.g. Porcellio laevis: Longo et al. 1998) and may be used for successive broods (Heeley 1941; Vandel 1941; Lueken 1962; Johnson 1982). By contrast, sperm is retained for only a couple of weeks, but not over successive broods, in aquatic species (e.g. Thermosphaeroma thermophilum: Jormalainen et al. 1999; but see Veuille 1980, for Jaera albifrons). This difference between aquatic and terrestrial species has important implications for the effectiveness, and thus the evolutionary stability, of mate guarding. Monopolization of females prior to, or after, insemination is ineffective if the female has already stored active sperm from previous matings. As this is often the case in terrestrial isopods, we may expect mate guarding to have been lost during evolution in terrestrial species owing to the higher costs and unlikely reproductive gain. In terrestrial isopods (Isopoda: Oniscidea), the position of the male on the back of the female during mating strongly resembles the clasping (‘amplexus’) of marine and freshwater isopods during precopula (e.g. Johnson 1985). However, with the exception of supralittoral species of the genus Ligia (Ligiidae) which represent prototypal oniscid isopods (Schmalfuss 1978, 1989; Carefoot & Taylor 1995) and of one species of the genus Helleria (Tylidae), no hint of precopulatory mate guarding has been presented in Oniscidea thus far (Table 1). Since phylogenetic relatives of Oniscidea, for example Valvifera and ‘Flabellifera’, as well as prototypal terrestrial species, do guard mates, males of the common ancestor of oniscid isopods, being monophyletic, probably guarded their mates too. A similar evolutionary loss of precopulatory mate guarding is obvious when comparing aquatic and Correspondence: M. Zimmer, Zoologisches Institut: Limnologie, Biologiezentrum, Christian-Albrechts-Universität, Olshausenstr. 40, D-24098 Kiel, Germany (email: mzimmer@zoologie.uni-kiel.de).