Sex roles

10.4.3 Sex roles

Sex differences in mating competition largely de- pend on the operational sex ratio (Kvarnemo and Ahnesjö 1996; see Section 10.2.1). Species where males are most competitive over matings are said to have conventional sex roles (Vincent et al. 1992). This does not necessarily imply that male mate choice and female competition over matings are absent in these species. These behaviours are, however, usually less obvious and have often been overlooked in studies of sexual selection (Cunningham and Birkhead 1998). When male po- tential reproductive rate is not so high and female variation in quality is substantial, males are ex- pected to be choosy. In fish, several studies have demonstrated male choice for large and more fecund females (reviewed in Andersson 1994). Female competition over males is expected if there is a shortage of males or if variation in male quality is large (reviewed in Berglund et al. 1993). In the lat- ter case females are expected to compete over the most preferred males, so showing competitive mate choice. An example of male shortage comes

from a population of the peacock blenny, Salaria pavo , where nest sites are scarce (Almada et al. 1995). In this species, males take up nests and pro- vide uniparental care. Accordingly, nest-holding males are hard to find and females compete in- tensely for access to these males. Females may also compete over resources necessary for reproduction as in the coho salmon, Oncorynchus kisutch, where females compete over oviposition sites (Fleming and Gross 1994).

Although most species have conventional sex roles, there are examples from different taxa, in- cluding fish, where the sex roles are reversed. Here females are the predominant competitors over matings. For example, in the pipefish Syngnathus typhle , the form and extent of male parental care decreased the relative potential reproductive rates of males below that of females (Berglund et al. 1989) (Fig. 10.4). This, in turn, influenced the operational sex ratio so that willing females were in excess (Berglund and Rosenqvist 1993). This caused males to be choosier and females more competitive (Berglund 1991). Consequently, females should be subject to stronger sexual selec- tion than males, and females more than males should evolve behaviours and structures aiding them in mating competition (e.g. Berglund et al. 1997). Several other fish species also exhibit sex- role reversal, for example the pipefish Nerophis ophidion (Rosenqvist 1990), the black-chinned tilapia, Sarotherodon melanotheron (Balshine- Earn and McAndrew 1995) and the goby Eucyclo- gobius newberryi (Swenson 1997). Note that paternal care per se does not cause sex-role rever- sal: the majority of caring fish species have exclu- sive paternal care but sex roles are typically not reversed (Fig. 10.1). This is probably because the usual forms of care, such as guarding and fanning, allow the male to accept several clutches and does not depress his potential reproductive rate below that of the females. Even the extreme form of pa- ternal care found in pipefishes and seahorses does not necessarily cause sex-role reversal: seahorses typically have conventional sex roles (Vincent et al. 1992; Vincent 1994).

Behavioural Ecology of Reproduction

235

Chapter 10

Fig. 10.4 Potential reproductive 6 rate in females of the pipefish

Syngnathus typhle . Females could fill on average two males 4 during the time of an average male

No. of females

pregnancy (45 days) when provided with an excess of mates. 2 Thus, females have a potential reproductive rate twice as high as that of males. (Source: after

0 0 Berglund et al. 1989; reproduced 1 2 3 4 by permission of the University of

No. of filled males within 45 days

Chicago Press.)

10.5 MATING PATTERNS

petition except for sperm competition. This may explain the lack of sexual dimorphism in this

The diversity of mating patterns, ranging from species. promiscuity to monogamy, is to a large extent ex-

Leks are areas where males aggregate and dis- plained by sex differences in mating competition play to females, which come there to mate only and resource distribution. Often, females distrib- (Höglund and Alatalo 1995). Females receive noth- ute themselves according to resources, such as ing but sperm from the males, and do not leave eggs food, shelter or breeding sites, while males distrib- or young on the males’ territories. A spectacular ute themselves according to female distribution. example is the bower-building cichlid, Cyrtocara Males may compete for the resources females need eusinostomus , in Lake Malawi, where up to 50 000 or try to monopolize females directly (Emlen and males may display simultaneously along a 4-km Oring 1977; Reynolds 1996). As resources vary in long arena. After mating, the female, who does all space and time, mating patterns may too, depend- the brooding, leaves the lek with the eggs in her ing on economic defendability (see Section 10.2.2). mouth (McKaye et al. 1990). Cod, Gadus morhua, This may, for example, explain the occurrence of may provide another example, with aggregated ‘resource-defence polygyny’. While this scheme males courting females vocally and by fin displays explains broad mating patterns, additional infor- (Nordeide and Folstad 2000). mation about parental care and sex differences in

Resource-defence polygyny is common in fish costs and benefits of mate choice and competition because, in many species, males defend a spawning are needed to understand the details of interac- site or build a nest where females lay their eggs. tions between the sexes (Reynolds 1996).

This is widespread among, for example, gobies, Promiscuous group-spawning is common in sticklebacks, labrids and damselfish. Female- many pelagic fish, probably because resources defence polygyny is much rarer but has been found are widely distributed in time and space and not in two simultaneously hermaphroditic sea basses, economically defendable. Many commercial fish the barred serrano, Serranus fasciatus, and the species may fall into this category, such as herring, lantern bass, S. baldwini. Males defend groups of Clupea harengus , which gather in large numbers female-acting hermaphrodites with small and col- to spawn. There are probably few options for exer- lectively defendable home ranges (Petersen 1987). cising mate choice or engaging in intrasexual com- In S. fasciatus, groups of females form with the

Behavioural Ecology of Reproduction

dominant individual acting as a pure male. anew. A female cannot search for a new mate while Subordinates spawn as females but retain their retaining hydrated eggs, as these must be released functional testes without using them much. How- within a short period. However, one can wonder ever, these ‘females’ may streak: a subordinate whether preparatory periods select for monogamy can hide close to a pair about to spawn and dash in or whether monogamy permits the female to to release sperm at the right time (Petersen 1990). have preparatory periods. Whatever the reason, For a review of alternative mating tactics see seahorses and monogamous pipefish seem to be Hutchings (Chapter 7, this volume).

examples of animals where ‘pure’ genetic mono-

A few fish species are monogamous. In the gamy can be found, as evidenced by microsatellite Midas cichlid, Cichlasoma citrinellum, parents analysis in the Western Australian seahorse H. stay together to defend their territory both against angustus (Jones et al. 1998). other Midas cichlids and to protect their larvae

Communal breeding has evolved in several from predators, including conspecifics. A single fish species with parental care and is especially parent is unlikely to be able to accomplish this suc- common in the Cyprinidae and the Cichlidae cessfully (e.g. Keenleyside 1991). Monogamy is a (Taborsky 1994; Wisenden 1999). Two common fixed trait in this species: even if the sex ratio and forms are ‘non-reproducing’ helpers that assist a density are experimentally manipulated to pro- reproducing couple in raising their offspring, and mote polygyny, monogamy reigns (Rogers 1987).

parental fish that adopt and raise other individuals’

Biparental care is, however, not the only factor offspring (alloparents). Several advantages have that promotes monogamy. Males may be kept been proposed to explain ‘helping’. If helpers are from access to several females by dominant males related to the individuals they assist, kin selection and may have to resort to monogamy or not mate may explain this phenomenon. Thus helpers at all, as in the cichlid Lamprologus brichardi propagate their own genes by helping relatives, as (Limberger 1983). In marine fishes, monogamy is in the cichlid Lamprologus brichardi (Taborsky commonly associated with difficulties in finding and Limberger 1981). Helpers may also benefit by and keeping more than one mate. Monogamy may being included in a group and gain access to shel-

be influenced by territoriality, low population ters or feeding sites if such are scarce (Taborsky density, and restricted or slow movement. In two 1984). Further, helpers may reproduce by stealing species of coral-dwelling hawkfishes, Neocirrhites fertilizations from the territorial male, as in the armatus and Oxycirrhites typus, males were cichlid Neolamprologus pulcher (Dierkes et al. monogamous if suitable corals were small or rare, 1999). Alloparents may benefit if larger schools of but maintained groups of females among large offspring reduce the per-capita predation by dilut- or abundant corals (Donaldson 1989). In the ing the risk or by confusing the predator (reviewed simultaneous hermaphrodite Serranus fasciatus, in Pitcher and Parrish 1993). In addition, predation pairs spawn monogamously under low population risk may be diverted from the parent’s young to the densities, taking turns to act as males and females alien young, as in convict cichlids (Wisenden and (Petersen 1990).

Keenleyside 1993). However, alloparenting need

Reproductive synchrony between males and fe- not always be adaptive but can simply be mis- males may select for monogamy. In the pipefish directed care, as when mouth-brooding cichlids Corythoichthys intestinalis (Gronell 1984) and in are parasitized by the catfish Synodontis multi- two seahorses, Hippocampus fuscus and H. whitei punctatus (Sato 1986). (Vincent et al. 1992; Vincent and Sadler 1995),

Some species of fish do not have sex at all. females need to hydrate their eggs for some time Examples include some minnows of the genus before depositing them in the male brood pouch. Phoxinus and the topminnow genus Poeciliopsis. Under monogamy, the female hydrates eggs while The latter contains both sexual and asexual the male broods the previous clutch. Once the species. The asexual all-female species were male has given birth, the pair is ready to mate formed by hybridization between two sexual top-

Chapter 10

minnow species and are triploid. Sperm from one driven either by sexual selection or by natural of the ancestral species is still required to initiate selection for fecundity advantages. reproduction but is not incorporated into the off-

Protogyny, in which individuals start as spring (Vrijenhoek 1979). Males of the ancestral females and then switch to males, is the common- species still benefit from spawning with the asexu- est form of hermaphroditism, exemplified by al females because females of their own species groupers (Epinephilinae), parrotfishes (Scaridae) copy the mate choice of the asexual females and many wrasses (Labridae). This sexually select- (Schlupp et al. 1994). These fish are often infected

ed life-history trait is explained by the ‘size-advan- by trematode larvae (Uvulifer sp.) and may develop tage model’ (Fig. 10.5; Ghiselin 1969; reviewed in the black spot disease. Theory attempting to ex- Warner 1988b). In species with strong competition plain why sex is advantageous suggests that asexu- als should be more parasitized than sexuals, and that variation in parasite level should be higher in

(a)

sexuals. This has been confirmed for an assem-

Polygyny potential high

blage of one sexual and two asexual topminnow species (Lively et al. 1990). Further, when the sexual species was inbred following a popula- tion bottleneck, parasite levels rose, suggesting that a lowered genetic variability increases susceptibility.