Parentage without parental care: What to look for in genetic studies of obligate brood-parasitic mating systems

The Auk 120(1):1-13, 2003

AS IN PREVIOUS decades (King and West 1977, Payne 1977, Brooke and Davies 1989), avian obligate brood parasitism-a reproductive strategy defined by laying and not caring for eggs in nests of other species-has continued to feature prominently in the general scientific literature (e.g. Lotem 1993, Sherry et al. 1993, Reboreda et al. 1996, Marchetti et al. 1998, Kilner et al. 1999, Gibbs et al. 2000, Tewksbury et al. 2002). Because obligate brood parasitic birds constitute only ~1% of all avian species (Ortega 1998, Davies 2000), why are they clearly over-represented in terms of publication?

This question seems to have three answers. First, the prominence of parasitic Old World cuckoos (e.g. Cuculus canorus, Clamator glandarius), cowbirds (Molothrus spp.), indigobirds (Vidua spp.), and, to a much lesser extent, the parasitic Black-headed Duck (Heterocephalus atricapillus), some New World cuckoos, and honeyguides, is partly due to fascination of researchers with the remarkable array of traits that are tied to unusual and successful reproductive habits of those parasites. These adaptations include behavioral strategies (e.g. nest searching, lack of incubation and brooding, increased chick begging intensity, self-referencing in conspecific recognition), life-history components (e.g. timing and speed of egg laying, increased fecundity, shorter incubation periods, faster development), and morphological features (e.g. stronger egg shells, smaller egg-to-body size ratios, mimicry of host eggs or nestlings) that distinguish some or all parasites from other, nonparasitic birds (Friedmann 1929, Rothstein 1990, Hauber et al. 2000, Hauber and Sherman 2001, Dearborn and Lichtenstein 2002).

A second key source of interest concerns interactions between avian brood parasites and their hosts; those interactions have become classic examples and model systems to test predictions of coevolutionary arms race hypotheses (Clayton and Moore 1997, Payne 1997, Rothstein and Robinson 1998, Davies 1999, Stokke et al. 2002). Interspecific comparisons, as well as geographic, seasonal, and long-term intraspecific comparisons of host egg-morphologies, rejection rates of parasitic eggs, and mimicry of host eggs and nestlings (especially by Cuculus and Clamator cuckoos, Molothrus cowbirds, and Vidua finches) have provided evidence for adaptations and counter-adaptations in both hosts and parasites (Davies and Brooke 1988, Moksnes and Roskaft 1995, Hosoi and Rothstein 2000, Cherry and Bennett 2001, Payne et al. 2001, Hauber 2003).

Third, there are conservation implications of parasitism. Brood parasites by definition exploit the parental care of their host species, and by reducing fitness they may create population sinks, especially in areas with high parasitism rates (Robinson et al. 1995). Those concerns are particularly relevant to the management of endangered host species (e.g. Least Bell's Vireo [Vireo bellii pusillus], Griffith and Griffith 2000; Yellow-shouldered Blackbird [Agelaius xanthomus], Wiley et al. 1991, Lopez-Ortiz et al. 2002).

Despite much interest in the evolution, behavior, and development of obligate parasitic birds (Ortega 1998, Rothstein and Robinson 1998, Davies 2000), the genetic revolution in studies of avian mating systems (Sherman 1981, Burke and Bruford 1987) has engulfed the brood parasite camp only since the late 1990s, more than a decade after it started sweeping through studies of nonparasitic bird species. That delay occurred despite early advances in molecular nongenetic approaches that complemented field studies of brood parasitic behaviors. For example, Fleischer (1985) used gel electrophoresis to discriminate yolk allozymes sampled from eggs laid by several female cowbirds. Because yolk and albumin are maternally derived and variable between individual females, such protein electromorph fingerprinting data can identify spatial and temporal laying patterns, egg morphologies, relatedness, and realized fitness of female parasites. That approach has been applied recently in conspecific parasitic waterfowl using a newer nondestructive sampling technique (Ahlund and Andersson 2001, Andersson and Ahlund 2001) and likely has much more to offer to the study of the mating systems of interspecific brood parasites (Sorenson and Payne 2002). In light of recent advances in the use of molecular genetic techniques, we synthesize here the new empirical data on the genetic mating systems of obligate brood parasites, examining those findings within theoretical expectations about the mating systems of species that are freed from the evolutionary constraints of parental care.

MATING SYSTEMS THEORY FOR APPARENTLY NONPARENTAL SPECIES

A mating system describes the behavioral, spatial, and temporal patterns of mating in a population of the same species (Emlen and Oring 1977, Andersson 1994). Quantitatively it includes the order, timing, and number of social and genetic mates and the developmental, morphological, and behavioral traits leading to (or circumventing) mating or fertilization. Postmating behaviors (e.g. mate-guarding, sperm-management, parental care, mate-desertion, divorce) also form an intrinsic component of mating systems because of the potentially causal interaction between alternative postmating strategies and future opportunities for mating (Clutton-Brock 1991, Andersson 1994, Weatherhead et al. 1994, Zuk 2002). As with other population-level traits, the mating system is an epiphenomenon summed across reproductive and social behaviors of the individuals constituting a population. Therefore, in studying sources of variation in mating systems it is necessary to understand mating patterns at the individual level.