Inclusive fitness theory posits that altruistic behaviors, which are directed more likely towards relatives, should be favored by natural selection. However, the prevalence of alternative parenting behaviors in offspring selection, including rejecting their own offspring and accepting the offspring of others, remains poorly understood within the context of parental care evolution. In order to investigate the factors that prompt the occurrence of alternative parenting behaviors, we designed a series of experiments in the Azure-winged Magpie (Cyanopica cyanus). By manipulating the nest spatial position or offspring age/number and parent-offspring familiarity, we addressed how parents provided parental care for the manipulated offspring. In the nest resettlement experiment, the probability of parents rejecting their own offspring significantly increased with nest-moving distances while decreased with offspring ages. In the cross-fostering experiments, the probability of parents provisioning unrelated young significantly decreased with the age difference between cross-fostered chicks. In the nest duplication experiments, where parents were given a choice between familiar offspring and unfamiliar unrelated chicks or between unfamiliar offspring and familiar unrelated chicks, the probability of both alternative parenting behaviors was significantly influenced by the time when parental association with their offspring was deprived. We conclude that as offspring phenotypic traits become individualized and fixed at a special developmental stage, parents gradually acquire the capacity for offspring recognition by associating with them. Any factors that disrupt parent–offspring association or introduce unrelated young into the nest prior to this critical timeline can result in the occurrence of alternative parenting behaviors.

Two questions in the research of animal personality—whether there is a correlation between a personality trait and individual reproductive success, and what is the genetic basis underlying a personality trait—remain unresolved. We addressed these two questions in three shrub-nesting birds, the Azure-winged Magpie (Cyanopica cyanus, AM), White-collared Blackbird (Turdus albocinctus, WB), and Brown-cheeked Laughingthrush (Trochalopteron henrici, BL). The personality type of an individual was first identified according to its response to a territorial intruder. Then, we compared the fleeing distance, breeding parameters, and differential expressed genes (DEGs) in the brain transcriptome between bold and shy breeders. In the three species, bold breeders exhibited more aggressiveness towards an intruder of their territory than did shy breeders. The reproductive success of bold breeders was significantly higher than that of shy breeders in AM but not in WB and BL. The three species shared one DEG, crabp1, which was up-regulated in bold relative to in shy individuals. By regulating the expression of corticotropin-releasing hormone, higher crabp1 gene expression can decrease cellular response to retinoic acid. Therefore, bold individuals are insensitive to external stresses and able to exhibit more aggressiveness to intruders than their shier counterparts. Aggressiveness is beneficial to bold individuals in AM but not in WB and BL because the former could evoke neighbors to make the same response of defending against intruders but the latter could not. Although a personality trait may have the same genetic basis across species, its correlation with reproductive success depends largely on the life history style of a species.