Exclusive male care despite extreme female promiscuity and low paternity in a marine snail

Center for Population Biology, Department of Evolution and Ecology, College of Biological Sciences, University of California, 1 Shields Ave, Davis, CA, 95616, USA.
Ecology Letters (Impact Factor: 10.69). 07/2012; 15(10):1167-73. DOI: 10.1111/j.1461-0248.2012.01841.x
Source: PubMed


Males exhibit striking variation in the degree to which they invest in offspring, from merely provisioning females with sperm, to providing exclusive post-zygotic care. Paternity assurance is often invoked to explain this variation: the greater a male's confidence of paternity, the more he should be willing to provide care. Here, we report a striking exception to expectations based on paternity assurance: despite high levels of female promiscuity, males of a marine snail provide exclusive, and costly, care of offspring. Remarkably, genetic paternity analyses reveal cuckoldry in all broods, with fewer than 25% of offspring being sired by the caring male, although caring males sired proportionally more offspring in a given clutch than any other fathers did individually. This system presents the most extreme example of the coexistence of high levels of female promiscuity, low paternity, and costly male care, and emphasises the still unresolved roles of natural and sexual selection in the evolution of male parental care.

Download full-text


Available from: Richard K Grosberg, Jun 11, 2014
  • Source
    • "As a result, classical parental care theory predicts that, all else being equal, males should provide less parental care when offspring are less likely to be their own (Trivers 1972; Sheldon 2002; Kokko & Jennions 2008). However, empirical evidence in support of this prediction is equivocal (Alonzo & Klug 2012; Kamel & Grosberg 2012; Griffin et al. 2013) suggesting that all else is often not equal. For example, although counter-intuitive, the relationship between the probability of paternity and paternal effort in the current reproductive attempt may be negative rather than positive (Queller 1997; Houston & McNamara 2002; Kokko & Jennions 2008). "
    [Show abstract] [Hide abstract]
    ABSTRACT: According to classical parental care theory males are expected to provide less parental care when offspring in a brood are less likely to be their own, but empirical evidence in support of this relationship is equivocal. Recent work predicts that social interactions between the sexes can modify co-evolution between traits involved in mating and parental care as a result of costs associated with these social interactions (i.e. sexual conflict). In burying beetles (Nicrophorus vespilloides), we use artificial selection on a paternity assurance trait, and crosses within and between selection lines, to show that selection acting on females, not males, can drive the co-evolution of paternity assurance traits and parental care. Males do not care more in response to selection on mating rate. Instead, patterns of parental care change as an indirect response to costs of mating for females.
    Ecology Letters 04/2014; 17(7). DOI:10.1111/ele.12284 · 10.69 Impact Factor
  • Source
    • "Since only a fraction of each brood was analyzed, the number of males contributing to each brood may be an underestimate of the true number of sires. The frequency of multiple paternity detected in R. venosa (89.5%) is low compared with some previously studied marine gastropods, such as Littorina saxatilis (100%) [42], Solenosteira macrospira (100%) [20], and Busycon carica (92%) [18], but higher than that of Neptunea arthritica (77%) and Aplysia californica (76%) [16]. Although there is no evidence that a R. venosa female does not obtain courtship feeding, nuptial gifts, or paternal care from multiple mating, we consider that the direct benefits obtained by a female from this behavior is more likely fertilization assurance. "
    [Show abstract] [Hide abstract]
    ABSTRACT: Inferring of parentage in natural populations is important in understanding the mating systems of a species, which have great effects on its genetic structure and evolution. Muricidae, a large group (approximately 1,600 species) of marine gastropods, are poorly investigated in patterns of multiple paternity and sperm competition based on molecular techniques. The veined Rapa whelk, Rapana venosa, a commercially important muricid species with internal fertilization, is an ideal species to study the occurrence and frequency of multiple paternity and to facilitate understanding of their reproductive strategies. We developed five highly polymorphic microsatellites in R. venosa and applied them to identify multiple paternity in 19 broods (1381 embryos) collected from Dandong, China. Multiple paternity was detected in 17 (89.5%) of 19 broods. The number of sires per brood ranged from 1 to 7 (4.3 on average). Of the 17 multiply sired broods, 16 (94.1%) were significantly skewed from equal paternal contributions, and had a dominant sire which was also dominant in each assayed capsule. Our results indicate that a high level of multiple paternity occurs in the wild population of R. venosa. Similar patterns of multiple paternity in the 2-6 assayed capsules from each brood imply that fertilization events within the body of a female occur mostly (but not entirely) as random draws from a "well-but-not-perfectly blended sperm pool" of her several mates. Strongly skewed distributions of fertilization success among sires also suggest that sperm competition and/or cryptic female choice might be important for post-copulatory paternity biasing in this species.
    PLoS ONE 01/2014; 9(1):e86508. DOI:10.1371/journal.pone.0086508 · 3.23 Impact Factor
  • Source
    [Show abstract] [Hide abstract]
    ABSTRACT: A recent research paper reports an extreme mating pattern in a marine snail.We raise a number of caveats and suggest possible follow-up experiments.We emphasize nonmodel organisms can provide novel insights into behaviour.
Show more