Paternity and the evolution of parental care

Biology Dept., University of Utah, Salt Lake City, Utah 84112, U.S.A.
Journal of Theoretical Biology (Impact Factor: 2.12). 03/1980; 82(4):619-631. DOI: 10.1016/0022-5193(80)90182-4


It is generally believed that level of paternity (the proportion of zygotes in a brood that were fertilized by the male providing parental care) has an important role in the evolution of parental care. We have used population genetics models to investigate this role. The models indicate that only in mating systems where a parental male “sacrifices” promiscous matings can paternity influence the evolution of male parental care. This is because level of paternity can reflect the number of opportunities for these promiscuous fertilizations. For example, high paternity can mean few opportunities and therefore a low cost for paternal care.Certain behaviors may preadapt a species for the evolution of male parental care because they decrease the costs of providing care. For example, in fish species where male care has evolved from spawning territories, the very establishment of territories may have precluded males from gaining promiscuous matings, thereby eliminating the promiscuity costs and facilitating the evolution of care. Without a promiscuity cost, level of paternity will not have influenced the evolution of male care in fishes.Because paternity has limited influence in the evolution of male care, differences in reliability of parentage between males and females are unlikely to explain the prevalence of female care. Our analysis suggests that paternity differences between species cannot serve as a general explanation for the observed patterns of parental care behavior.

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Available from: Richard Shine
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    • "In many socially monogamous and cooperatively breeding species, males' mating success may be constrained by such factors as the need for bi-parental care and female–female competition. Under such conditions, it may pay males to invest in current offspring, even if this comes at some expense to future mating opportunities (Maynard Smith 1977; Queller 1997; Werren et al. 1980). Our analysis suggests that this may also be true in some polygynous species. "
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    ABSTRACT: Sexual selection theory predicts that males in polygynous species of mammals will invest more reproductive effort in mate competition than parental investment. A corollary to this prediction is that males will mount a stress response when their access to mates is threatened. Indeed, numerous studies have shown that males exhibit elevated stress hormones, or glucocorticoids (GCs), when their access to females, or a proxy to this access like dominance rank, is challenged. In contrast, the relationship between stress hormones and paternal effort is less obvious. We report results from a study of wild male chacma baboons indicating that males experienced elevated GC levels during periods of social instability following the immigration of a dominant male. These effects were strongest in males whose mating opportunities were at greatest risk: high-ranking males and males engaged in sexual consortships. Males involved in friendships with lactating females, a form of paternal investment, also experienced high GC levels during these periods of instability. There was a tendency for males with lactating female friends to reduce their time spent in consortships during unstable periods, when the risk of infanticide was high. Thus, even in a highly polygynous mammal, males may have to balance paternal effort with mating effort. Males who invest entirely in mating effort risk losing the infants they have sired to infanticide. Males who invest in paternal care may enhance their offspring’s survival, but at the cost of elevated GC levels, the risk of injury, and the loss of mating opportunities.
    Full-text · Article · Dec 2014 · Behavioral Ecology and Sociobiology
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    • "This role of the oxytocin system facilitating paternal care also parallels the role of oxytocin in maternal care (Francis et al., 2000). We therefore tentatively suggest that as paternal care evolved numerous times independently in different vertebrate lineages (likely as a consequence of very different selection pressures and ecological constraints; see Werren et al., 1980), ancient neuroendocrine and neuroanatomical substrates were recruited repeatedly to converge on similar social phenotypes. Complementary studies in birds and amphibians are urgently needed in order to determine to what extent other independent evolutionary transitions to paternal care relied on such deep molecular and neural homologies (Shubin et al., 2009). "
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    ABSTRACT: While the survival value of paternal care is well understood, little is known about its physiological basis. Here we investigate the neuroendocrine contributions to paternal care in the monogamous cichlid, Amatitlania nigrofasciata. We first explored the dynamic range of paternal care in three experimental groups: biparental males (control fathers housed with their mate), single fathers (mate removed), or lone males (mate and offspring removed). We found that control males gradually increase paternal care over time, whereas single fathers increased care immediately after mate removal. Males with offspring present had lower levels of circulating 11-ketotestosterone (11-KT) yet still maintained aggressive displays toward brood predators. To determine what brain regions may contribute to paternal care, we quantified induction of the immediate early gene c-Fos, and found that single fathers have more c-Fos induction in the forebrain area Vv (putative lateral septum homologue), but not in the central pallium (area Dc). While overall preoptic area c-Fos induction was similar between groups, we found that parvocellular preoptic isotocin (IST) neurons in single fathers showed increased c-Fos induction, suggesting IST may facilitate the increase of paternal care after mate removal. To functionally test the role of IST in regulating paternal care, we treated biparental males with an IST receptor antagonist, which blocked paternal care. Our results indicate that isotocin plays a significant role in promoting paternal care, and more broadly suggest that the convergent evolution of paternal care across vertebrates may have recruited similar neuroendocrine mechanisms.
    Full-text · Article · Apr 2012 · Hormones and Behavior
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    • "For example, altruistic behaviors such as parental care are more likely to be favored in populations that are 'viscous' (i.e., have low dispersal; Hamilton 1964; van Baalen and Jansen 2006; West et al. 2007) if the benefits of care are not outweighed by costs associated with increased competition among closely related individuals (Kelly 1992; West et al. 2002). Some studies have also focused on the relationship between the evolution of parental care and ectothermy (Hopson 1973; Case 1978; Gross and Shine 1981; discussed in Clutton-Brock 1991), fertilization mode (Werren et al. 1980; Gross and Shine 1981; Beck 1998; Mank et al. 2005), and egg size (Smith and Fretwell 1974; Shine 1978; Sargent et al. 1987; Winemiller and Rose 1992). However, as of yet, no studies have identified the most general life-history conditions (i.e., stage-specific mortality, maturation, and reproductive rates) that are likely to favor the evolution of parental care (or other altruistic behaviors among closely related kin). "
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    ABSTRACT: Patterns of parental care are strikingly diverse in nature, and parental care is thought to have evolved repeatedly multiple times. Surprisingly, relatively little is known about the most general conditions that lead to the origin of parental care. Here, we use a theoretical approach to explore the basic life-history conditions (i.e., stage-specific mortality and maturation rates, reproductive rates) that are most likely to favor the evolution of some form of parental care from a state of no care. We focus on parental care of eggs and eggs and juveniles and consider varying magnitudes of the benefits of care. Our results suggest that parental care can evolve under a range of life-history conditions, but in general will be most strongly favored when egg death rate in the absence of care is high, juvenile survival in the absence of care is low (for the scenario in which care extends into the juvenile stage), adult death rate is relatively high, egg maturation rate is low, and the duration of the juvenile stage is relatively short. Additionally, parental care has the potential to be favored at a broad range of adult reproductive rates. The relative importance of these life-history conditions in favoring or limiting the evolution of care depends on the magnitude of the benefits of care, the relationship between initial egg allocation and subsequent offspring survival, and whether care extends into the juvenile stage. The results of our model provide a general set of predictions regarding when we would expect parental care to evolve from a state of no care, and in conjunction with other work on the topic, will enhance our understanding of the evolutionary dynamics of parental care and facilitate comparative analyses.
    Full-text · Article · Sep 2009 · Evolution
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