Does maternal care evolve through egg recognition or directed territoriality?

Abstract

The mechanism that facilitates the evolution of maternal care is ambiguous in egg-laying terrestrial vertebrates: does the ability of mothers to recognize their own eggs lead them under some circumstances to begin providing care or can maternal care evolve from simply being in close proximity to the eggs (e.g. through territorial behaviour)? This question is difficult to answer because in most species, parental care is either absent altogether or present; in only a few species we have the opportunity to observe intraspecific variation in the expression of parental care. We studied a population of long-tailed skinks (Eutropis longicaudata) in which females have recently evolved maternal care from a noncaring state. Females on Orchid Island, Taiwan, remain with their eggs during incubation and when doing so, actively deter egg predation by egg-eating snakes (Oligodon formosanus); in all other populations, females lack post-ovipositional maternal care. Nest-guarding females on Orchid Island (i) showed antipredator behaviours only in the original nest site in which they laid eggs, even after we removed all of the eggs or substituted them with those of a conspecific; (ii) protect any eggs present inside the original nest site (even when the eggs belong to a conspecific); and (iii) develop this behaviour while gravid (i.e. prior to laying eggs). This supports the hypothesis that long-tailed skinks cannot recognize their own eggs, suggesting that maternal care is a directed form of territoriality only expressed towards egg-eating snakes and only during reproduction. Nest guarding is among the most primitive forms of parental care, and the recent evolution of this behaviour in a single population provides insight into one of the mechanisms by which parental care can originate in terrestrial vertebrates.

Live bearing promotes the evolution of sociality in reptiles

“…The most parsimonious explanation is that live birth results in a higher recurrence of physical association between parents and neonates, allowing for more consistent selection on social interactions among related individuals 1 , 2 , 5 , 21 (see also ref. 22 ). This may be particularly important in squamate reptiles which, in contrast to many birds and mammals, have relatively low costs of tolerating juveniles 23 , 24 .…”

Predation drives interpopulation differences in parental care expression

“…In this population, mothers nesting within concrete retaining walls remain at the nest during incubation and actively deter egg‐eating snakes ( Oligodon formosanus Günther 1872) from entering the nest and consuming the eggs (Huang ; Supplementary Information S1). Antisnake behaviour is only expressed while gravid, immediately prior to oviposition (Huang & Pike ). By contrast, females nesting in natural habitats nearby (beneath rocks and logs) never guard their eggs during incubation (Huang & Pike ).…”

Do Brooding Pythons Recognize their Clutches? Investigating External Cues for Offspring Recognition in the Children's Python, Antaresia childreni

“…The type of parent–offspring recognition a species uses suggests different evolutionary pathways (Huang & Pike ). Indirect offspring recognition in a species may imply that parental care was driven by nest‐site defense.…”

“…The evolution of offspring recognition is driven by two nesting scenarios (Huang & Pike 2011). Direct offspring recognition is expected to occur in species with a high risk of misdirected care, such as exists in colonial nesting species (Medvin & Beecher 1986;Pitcher et al 2012) or species with high rates of nest parasitism (Stokke et al 2007).…”

“…Where it does occur, little is known about offspring recognition. The few existing studies on the subject, focusing on scincid lizards, suggest that indirect offspring recognition is important in reptile parental care (Vitt & Cooper ; Huang & Pike ). Pythons provide the most complex form of post‐paritive parental care described among reptiles in that females tightly coil around their clutch typically until hatching.…”