Sensory Mechanisms of Parent-Offspring Recognition in Fishes, Amphibians, and Reptiles.

Parental care is important for offspring survival and success. Recognition of offspring by parents is critical to ensure parents direct care behaviors at related offspring and minimize energy lost by caring for unrelated young. Offspring recognition of parents prevents possible aggressive interactions between young and unrelated adults and allows offspring to direct begging behaviors toward the correct adult. Despite its importance and widespread nature, much of the current research has focused on a small range of species, particularly mammals and birds. We review the existing literature on the sensory mechanisms of parent-offspring recognition in fishes, amphibians, and reptiles. Within these groups, there is diversity in the presence and strategies for parent-offspring recognition. Future studies should continue to identify these mechanisms, as well as the neural and endocrine underpinnings in non-model organisms to expand our knowledge of this behavior and inform our understanding of the evolution of parent-offspring recognition.

Neural activation patterns associated with mouthbrooding, maternal care, infanticide and fry release in an African cichlid fish.

Parental care has evolved several times and is present across taxa. Parental care behaviors, such as food provisioning and protection, are critical for offspring success. However, infanticide can co-exist with parental care in the same species. The mechanisms underlying the switch from care to consumption and from offspring dependence to independence are relatively unknown, especially in fishes, the oldest and largest group of vertebrates. Mouthbrooding, an extreme example of parental care present in dozens of genera of fishes, provides an excellent opportunity to investigate the brain regions important for parental care. The maternal mouthbrooding African cichlid fish Astatotilapia burtoni broods developing young inside the mouth for approximately 14 days, then provides post-release maternal care by protecting fry inside the mouth when threatened. Following the post-release maternal care phase, females can exhibit infanticide and consume their own offspring. We used immunohistochemistry for the neural activation marker pS6 to identify differences in neural activation among mouthbrooding, maternal-care-providing and infanticide-exhibiting females, and between pre- and post-release fry. We identified five brain regions (Dc-5, ATn, nPPa, Vd-c and Dl-g) that are differentially activated among mouthbrooding, maternal care and infanticide females as well as six regions (Dm, Vv, Vd, Vs-m, TPp, PGZ and INL of retina) differentially activated between pre- and post-release fry. This study identifies both shared and distinct circuitry that may support transitions between parental care states and from care to infanticide, as well as regions in developed fry that support the transition from pre- to post-release.

Behavior and neural activation patterns of non-redundant visual and acoustic signaling during courtship in an African cichlid fish.

Animals evolve mechanisms to send and receive communication signals through multiple sensory channels during crucial behavioral contexts such as aggression and reproduction. This ensures the transmission of important context-dependent signals that supply either the same (redundant) or different (non-redundant) information to the receiver. Despite the importance of multimodal communication, there are relatively few species in which information on sender signals and receiver responses are known. Further, little is known about where context-dependent unimodal and multimodal information is processed in the brain to produce adaptive behaviors. We used the African cichlid, Astatotilapia burtoni, to investigate how unimodal and multimodal signals are processed within the female brain in a reproductive context. During courtship, dominant males produce low frequency sounds in conjunction with visual displays (quivers) directed towards receptive gravid females. We compared affiliation behaviors and neural activation patterns in gravid females exposed to visual, acoustic and visual-acoustic signals from courting dominant males. Females displayed reduced affiliation in auditory-only conditions, but similar affiliation during visual and visual-acoustic conditions, demonstrating that visual-acoustic signaling from males is non-redundant but vision dominates. Using the neural activation marker cfos, we identified differential activation in specific socially relevant brain nuclei between unimodal and multimodal conditions and distinct neural co-activation networks associated with each sensory context. Combined with our previous work on chemosensory signaling, we propose that A. burtoni represents a valuable vertebrate model for studying context-dependent behavioral and neural decision making associated with non-redundant multimodal communication.

Expression and localization of neuronal nitric oxide synthase in the brain and sensory tissues of the African cichlid fish Astatotilapia burtoni.

Nitric oxide (NO) produced by the enzyme neuronal nitric oxide synthase serves as an important neurotransmitter in the central nervous system that is involved in reproductive regulation, learning, sensory processing, and other forms of neural plasticity. Here, we map the distribution of nnos-expressing cells in the brain and retina of the cichlid fish Astatotilapia burtoni using in situ hybridization. In the brain, nnos-expressing cells are found from the olfactory bulbs to the hindbrain, including within specific nuclei involved in decision-making, sensory processing, neuroendocrine regulation, and the expression of social behaviors. In the retina, nnos-expressing cells are found in the inner nuclear layer, presumably in amacrine cells. We also used quantitative PCR to test for differences in nnos expression within the eye and olfactory bulbs of males and females of different reproductive states and social statuses. In the eye, males express more nnos than females, and socially dominant males express more nnos than subordinate males, but expression did not differ among female reproductive states. In the olfactory bulbs, dominant males had greater nnos expression than subordinate males. These results suggest a status-specific function for NO signaling in the visual and olfactory systems that may be important for sensory perception related to mating or territorial interactions to maintain the social hierarchy. The widespread distribution of nnos-expressing cells throughout the cichlid brain is similar to that in other teleosts, with some conserved localization patterns across vertebrates, suggesting diverse functions for this important neurotransmitter system.

Endocrine and neuroendocrine regulation of social status in cichlid fishes.

Position in a dominance hierarchy profoundly impacts group members' survival, health, and reproductive success. Thus, understanding the mechanisms that regulate or are associated with an individuals' social position is important. Across taxa, various endocrine and neuroendocrine signaling systems are implicated in the control of social rank. Cichlid fishes, with their often-limited resources of food, shelter, and mates that leads to competition, have provided important insights on the proximate and ultimate mechanisms related to establishment and maintenance of dominance hierarchies. Here we review the existing information on the relationships between endocrine (e.g., circulating hormones, gonadal and other tissue measures) and neuroendocrine (e.g., central neuropeptides, biogenic amines, steroids) systems and dominant and subordinate social rank in male cichlids. Much of the current literature is focused on only a few representative cichlids, particularly the African Astatotilapia burtoni, and several other African and Neotropical species. Many hormonal regulators show distinct differences at multiple biological levels between dominant and subordinate males, but generalizations are complicated by variations in experimental paradigms, methodological approaches, and in the reproductive and parental care strategies of the study species. Future studies that capitalize on the diversity of hierarchical structures among cichlids should provide insights towards better understanding the endocrine and neuroendocrine mechanisms contributing to social rank. Further, examination of this topic in cichlids will help reveal the selective pressures driving the evolution of endocrine-related phenotypic traits that may facilitate an individual's ability to acquire and maintain a specific social rank to improve survival and reproductive success.