The origin of parental care in birds: a reassessment

Birds’ reproductive biology is unique in several respects, including patterns of parental care. Biparental care is the norm in birds; it occurs in more than 90% of living species (Kendeigh, 1952), whereas in all other animal groups, if biparental care occurs at all, it is much less common than is uniparental paternal or maternal care (Clutton-Brock, 1991). The reasons for this peculiar pattern are still not fully understood. The studies on avian parental care usually assumed that biparental care was primitive in birds, and theoretical effort was concentrated on finding ways to explain how unaided male or female care could have evolved from it (references in Wesolowski, 1994). The problem of how this avian biparental care system has evolved in the first place was usually completely ignored. Fortunately this situation has been changing lately. Several studies pursued problems of the evolutionary origins of parental care by attempting to reconstruct the earliest stages of parental care in birds. The first serious attempt to derive parental care origins from the reptilian state was made by Kavanau (1987). He proposed that the appearance of parental care and further changes in its mode in stem reptiles constituted the first major event in avian evolution. In other words, the first step on the way leading to birds was the achievement of advanced biparental care (consisting of egg guarding, as well as grooming, protecting, and escorting of young) by stem reptiles. All other changes, such as attaining homeothermy and the ability to fly, came later. So the first birds would have been biparental with precocial young. Kavanau also proposed that the main force behind the evolution of flight was the need in arboreal reptiles to gain rapid access to ground nests. Van Rhijn (1984, 1990), El_ zanowski (1985), and Handford and Mares (1985) were the first to suggest that the earliest form of parental care in birds was unaided male care derived from lack of care in the reptilian ancestors. Following their arguments and other sources of information, I proposed a multistage model of the origin of parental care and the evolution of parental roles in birds (Wesolowski, 1994) as an alternative to Kavanau’s scenario. It assumed that powered flight evolved for reasons independent of reproduction, and that parental care evolved as a response to it, within a framework of limitations set by adaptations to aerial locomotion. The unique system of care was then explained in terms of evolutionary responses to the design constraints created by, and ecological opportunities associated with, the origin of flight. It was proposed that evolution proceeded initially through stages without parental care (main adaptations to flight appeared then) but with increasing investment in eggs, resulting in the appearance of sequential ovulation and of very large eggs, thus producing young able to fly shortly after hatching. It was suggested that parental care appeared only at that stage, and that it was unaided paternal care (preserved in some groups). Biparental care then evolved from unaided male care. This model was corroborated and extended by Ligon (1999). Moreover, results of an analysis of incubation patterns in extant birds by Vehrencamp (2000) also suggested that the ancestral state for birds was sole male incubation, from which several forms of shared incubation and female only care have arisen. However, several investigators (Burley and Johnson, 2002; Prum, 2002; Tullberg et al., 2002; Varricchio et al., 1999) have recently challenged the no care to male care first hypothesis and proposed that parental care is primitive in Archosuaria. They propose—analogously to Kavanau’s (1987) model—that changes in the mode of parental care in some ordinary reptiles constituted the first major event in avian evolution; that is, the first step along the way leading to birds was the achievement of advanced biparental care (consisting of egg guarding, incubation, as well as protecting and escorting of young) by reptiles. The ability to fly came later, without a tight relationship to the parental care mode. Tullberg et al. (2002) and Burley and Johnson (2002) claim to reject the male care first scenarios, and the latter investigators write, ‘‘Arguments for the male care first hypothesis have not been presented in any detail. , and thus they cannot be inspected closely. Proponents of the male care first hypothesis need to articulate scenarios that would obviate these problems. ’’ Being one of them, I feel called to the blackboard. I begin these comments by addressing the strength and validity of the main paleontological, phylogenetic, and cost/ benefit arguments put forward in favor of the maternal care first scenarios. I conclude by proposing a set of minimum requirements that any comprehensive theory of the origin of parental care should fulfill. As not all investigators using terms such as ‘‘parental care,’’ ‘‘incubation,’’ or (in a paleontological context) even ‘‘bird’’ or ‘‘avian’’ mean the same, it is necessary to define these terms to avoid ambiguities. In the present discussion, ‘‘parental care’’ will be limited to behavioral aspects of the enhancement of egg and/or young survival by parents, taking place in the postoviposition period (Wesolowski, 1994); ‘‘bird’’ or ‘‘avian,’’ to the first organisms capable of powered flight and all of their ancestors; and ‘‘incubation’’ to direct transfer of heat from parent’s body to eggs.