High paternity without paternity-assurance behavior in the purple sandpiper, a species with high paternal investment

ELIN P. PIERCE1 AND JAN T. LIFJELD

ABSTRACT.-Among birds, males investing highly in paternal care should be under particularly strong selection pressure to prevent extrapair paternity in their broods. Current literature implies that to obtain a high certainty of paternity, males should invest in paternity-assurance behaviors, and this makes them more likely to increase their investment in reproduction. The Purple Sandpiper (Calidris maritima) is a relatively long-lived arctic shorebird with a socially monogamous pair bond and strong mate and territory fidelity by both sexes. Paternal investment is high because males alone perform all of the brood care from hatching to fledging. We investigated the mating strategies of male and female Purple Sandpipers through genetic analysis and examined the possibility that this species exhibits paternity-assurance behaviors. We found no evidence that males exhibited behaviors such as frequent copulation or mate guarding during their mate's fertile period. Furthermore, high rates of copulation were not necessary for pairs to achieve complete fertility of the clutch. Multilocus DNA fingerprinting revealed little evidence for extrapair fertilizations: only 1 of 82 offspring was sired by an extrapair male. These results suggest that male and female Purple Sandpipers rarely seek extrapair copulations (EPCs). In contrast to several recent studies with similar findings, we believe that the apparent rarity of EPCs results because females have few genetic or other benefits to gain from seeking them. Thus, paternity-assurance behaviors by male Purple Sandpipers were not necessary for achieving full paternity of the clutch, and such behaviors cannot be said to have led to the observed high level of paternal investment in reproduction. Uniparental brood care, however, is associated with a high certainty of paternity in this species. Received 3 June 1997, accepted 13 November 1997.

STUDIES OF SPECIES that combine paternity data with information on the social and ecological factors that may affect paternity are essential for understanding the adaptive value of parental investment and thus the evolution of mating systems. Knowledge of the extent of extrapair reproductive activities can shape our evaluation of the costs and benefits of parental care (Reyer et al. 1997). Pairs in socially monogamous avian species were previously assumed to mate exclusively with each other, but recent studies have shown that in many species, individuals engage in extrapair reproductive activities (Westneat et al. 1990, Birkhead and Moller 1992). Although the number of such studies is increasing, most of them focus on passerines (Moller and Briskie 1995). One group of nonpasserines, the shorebirds, exhibit the greatest variation among birds in mating systems and in the relative amount of parental investment by the sexes (Oring 1982); the latter is one of the most important factors determining the intensity of sexual selection (Trivers 1972). For monogamous shorebirds in particular, few studies have presented behavioral data (e.g. Nol 1985, Ens 1991), and fewer still have presented both behavioral and genetic data on aspects of mating strategies (e.g. sperm competition; Heg et al. 1993), although such studies recently have been conducted on some nonmonogamous shorebirds (e.g. Oring et al. 1994, Lank et al. 1995, Owens et al. 1995, Lanctot et al. 1997).

Our goals in this study were to: (1) investigate the possibility that Purple Sandpipers (Calidris maritima) exhibit paternity-assurance behaviors; and (2) examine parentage, the resuit of male and female mating strategies, through genetic analysis (minisatellite DNA fingerprinting). The Purple Sandpiper is a relatively long-lived shorebird (commonly >7 years) in which males and females form socially monogamous pair bonds and show strong annual fidelity to nesting territories and mates (Pierce unpubl. data). Males exhibit typical sex roles in that they defend large territories on the tundra and court females (Pierce 1997). Purple Sandpipers in Svalbard were found to make only one nesting attempt per season, during which the sexes shared incubation equally overall (Pierce 1997). At hatching, however, the sex roles are atypical because females leave the nest, and males assume all brood-care duties alone until the chicks reach independence about 24 to 34 days later (Pierce 1997). Males thus invest highly in parental care. In the Purple Sandpiper, as in other species with extensive paternal care, males potentially have much to lose from extrapair paternity (EPP) within their brood because their investment in parental care presumably is costly, and it may occur at the expense of seeking additional mating opportunities (Emlen and Oring 1977, CluttonBrock and Parker 1993, Owens et al. 1995). Males of avian species with sex-role reversed parental care should, therefore, be under especially strong selection pressure to prevent their mates from copulating with other males, i.e. males that care for extrapair young should be selected against (Oring 1982, 1986; Oring et al. 1994). In most social systems, females have the opportunity to mate with several males (Oring et al. 1994), and male behaviors that increase the likelihood of paternity, such as mate guarding, should be favored by natural selection (e.g. Trivers 1972, Westneat et al. 1990, Birkhead and Moller 1992).