Parental role-reversed polyandry and paternity

Male birds may desert their mates whenever they benefit more by deserting and remating than by sharing in the care of their young (Ridley 1978, Wittenberger 1979). In a few species, females desert and remate and males care alone (Emlen and Oring 1977, Ridley 1978, Wittenberger 1979, Erckmann 1983, Oring 1982, 1986). Such a reversal in parental roles is central to the evolution of avian polyandry, and polyandrous mating systems in general. Theoretical studies suggest that polyandry through female desertion can only occur when there is strong selection against desertion by males (Trivers 1972, Williams 1975, Boucher 1976, Dawkins and Carlisle 1976, Maynard Smith 1977, Graul et al. 1977, Lazarus 1990). Three general hypotheses have been proposed to explain the reversal of parental roles among polyandrous birds (see reviews by Ridley 1978, Wittenberger 1979, Erckmann 1983, and Oring 1982, 1986): (1) remating opportunities are greater for deserting females than for deserting males (Maynard Smith 1977); (2) females are less able than males to raise the offspring alone because of the stress of egg laying (Grafen and Sibly 1978); and (3) males benefit from female emancipation from parental care because it enables the female to double clutch or to replace a failed clutch for her mate (Jenni 1974). Recent studies suggest that sex-ratio biases may favor mate desertion by the rarer sex in some facultatively polygamous fish (Keenleyside 1983) and some birds (Beissinger 1987, 1990, Beissinger and Snyder 1987, Benkman 1989, Fujioka 1989), including one species of polyandrous shorebird (Oring et al. 1983). Evidence for these hypotheses is largely inconclusive for most polyandrous shorebirds, the avian group in which polyandry is most prevalent (Jenni 1974, Pitelka et al. 1974, Ridley 1978). The idea that male desertion is constrained by advantages of territoriality (Gross and Sargent 1985) may not apply to polyandrous birds because often they are not territorial, or both sexes may defend all-purpose breeding territories (Oring 1986). In a few cases females may be less able than males to raise the young unaided (Brunton 1988). However, parental constraints are unlikely to be a general explanation for polyandry in shorebirds, because females tend to be larger and more aggressive than males (Jenni 1974, Erckmann 1983). Thus, females should be better at protecting the young than males. Here I suggest that the reversal of parental roles and polyandry in birds may also be favored if males gain a benefit by inseminating the female before she deserts, thus siring at least part of the subsequent brood she lays for another male. Moreover, if the benefit the male expects from inseminating the deserting female is greater than the benefit he expects from deserting and remating, parental role reversal may arise because polyandry is in the male's interest. This could be the case when deserting males have a low probability of remating, when insemination of deserting females results in a high probability of paternity, and when any increase in parental effort caused by the female's desertion has little cost to the male's survival. The feasibility of this hypothesis relies on the ability of female birds to store viable sperm for days or weeks (e.g. Birkhead and M0ller 1992). Moreover, the cost of uniparental care, in terms of the male's survival, appears to be low (e.g. Oring et al. 1983, Oring 1986, Valle 1994). This hypothesis implies that the benefit some males gain through the insemination of their deserting mate will result in decreased paternity for later nesting males, which in turn may decrease a male's willingness to provide parental care (e.g. Trivers 1972, Houston and Davies 1985, Winkler 1987, Richardson and Coetzee 1988, Whittingham et al. 1992, Xia 1992). However, if all males experience a relatively constant average reduction in certainty of paternity in the brood for which they care, decreased certainty of paternity per se may not affect the male's willingness to care (Maynard Smith 1978, Grafen 1980, Werren et al. 1980). This may be the case in populations that breed more or less continuously throughout the year, such as tropical jacanas. However, among populations that breed seasonally, such as the polyandrous arctic shorebirds, males breeding earlier may not only ensure high paternity in their first brood, but also gain extra offspring at the expense of later breeders. Therefore, males that do not mate until later in the season should attempt to improve paternity by mating with previously unmated females and discriminating against formerly mated ones (Whitfield 1990). However, any male breeding late may have little choice of partners. Such males are likely to be younger or of lower quality, and perhaps cannot afford to be too choosy about their mates (but see Whitfield 1990). Furthermore, in arctic shorebirds because rapid reproduction is at a premium due to the shortness of the breeding season, and because unmated females may be in short supply late in the season, late-nesting males may be forced to accept previously mated females. Moreover, high rates of nest failure, weak pair bonding, and recurrent opportunities for renesting