Available online at www.sciencedirect.com ScienceDirect Poison frogs as a model system for studying the neurobiology of parental care Alexandre B Roland and Lauren A O’Connell Parental care is essential for the survival and well-being of example, maternal care is more common in genera with offspring in many species. Understanding the mechanisms internal fertilization or when females are the sole food underlying parental involvement can lend insight into general source as with lactation in mammals. On the other hand, and conserved principles governing the neural basis of a major paternal care is more common in genera with external life history stage, parenthood. While many animal models of fertilization in the form of egg guarding as a way to parental behavior display maternal care, studying male guarantee paternity. Understanding why and how either involvement is challenging. Male parents are usually involved in one or both parent(s) care for offspring requires integrat- a strong relationship with their partner, and this makes ing complementary approaches to answer the proximate separating reproductive and parental mechanisms difficult. and ultimate facets of behavior, best put forth by Niko This separation is possible in poison frogs, where different Tinbergen’s ‘Four Questions’ over 50 years ago [7]: species provide biparental care and male or female uniparental care without pair bonding. Poison frogs provide a great How does parental behavior work? (Mechanism/ comparative framework to study parental care within a causation) relatively simple neural architecture easily amenable in the field How does this behavior develop during the lifetime of and laboratory. an individual? (Ontogeny) Address What is the function of parental behavior? (Adaptive/ FAS Center for Systems Biology, Harvard University, Cambridge, MA survival value) 02138, USA Why did this behavior evolve over the history of a species? (Evolution/Phylogeny) Corresponding author: O’Connell, Lauren A ([email protected]) While many animal models have attempted to address the Current Opinion in Behavioral Sciences 2015, 6:76–81 causes and consequences of variation in parental care, most have fallen short of their utility in answering all four This review comes from a themed issue on Integrated study of animal behavior of Tinbergen’s questions. Thus, our understanding of parental care, especially care of offspring by males, is still Edited by Dustin Rubenstein and Hans Hofmann relatively poor compared to other social behaviors. Ex- ploring the physiological and neural mechanisms under- lying different parental stages within a comparative http://dx.doi.org/10.1016/j.cobeha.2015.10.002 framework could highlight conserved mechanisms pro- 2352-1546/# 2015 Elsevier Ltd. All rights reserved. moting parental care across many species. Parental care in animal models Specialized parental care strategies have evolved across the animal kingdom, yet the underlying mechanisms promoting the convergent evolution of these behavioral Becoming a parent is a considerable life transition and in phenotypes are poorly understood [1,8]. Among verte- many species requires precious time and energy from brate species that show parental care, the diversity of invested parents to raise their offspring. Such transition to strategies is unequally distributed (Figure 1). The physi- parental care behavior requires transformative changes in ological and neural mechanisms that promote parental physiology and neurochemistry to facilitate a switch from care are best understood in rodents, especially in the apathy or aggression toward offspring to the powerful context of maternal care [9] which occurs in roughly bond that most human parents experience. Across the 90% of mammalian species [10]. However, less is known animal kingdom, various parental care strategies (bipa- about the biological basis of paternal care, which is mainly rental and male or female uniparental care) have evolved informed by monogamous and biparental animal models, numerous times in every major lineage [1], exemplifying including Microtus voles, Peromyscus mice, Estrildid the adaptive significance of parental behavior in diverse finches and cichlid fish [11–16]. In these contexts, males ecological contexts. Whether one or both parents will be usually form a pair bond with their partner before engag- involved in offspring care is influenced by many factors ing in parental care, likely modifying neural connectivity including certainty of parentage, the population opera- and gene expression through multiple behavioral transi- tional sex ratio, or the reproductive mode [2–6]. For tions [14,17,18]. Thus, these intermingled behaviors Current Opinion in Behavioral Sciences 2015, 6:76–81 www.sciencedirect.com Poison frog systems neuroscience Roland and O’Connell 77 Figure 1 Mammals Female 100% Biparental Birds Male >99% Crocodilians 100% Reptiles ~3% Amphibians ~10% Fishes ~20% 0 50 100% Current Opinion in Behavioral Sciences Estimated representation of parental care strategies among the major vertebrate lineages. Percentages under each vertebrate lineage are estimated proportions of the number of species with parental care. Bars represent an estimated proportion of each type of parental care system according to species, genera or families displaying parental care within the lineage. Male uniparental care is absent in mammalian and reptilian linages. In birds, about 9% display cooperative breeding and less than 1% does not display parental care through either geothermal heat incubation or brood parasitism. Most fish, amphibians and reptiles (except crocodilians), do not display parental care. Source: Data from Refs. [3,10,23,66]. make the neural bases of parental care difficult to disas- own skin mucus to offspring [10,24]. The most striking sociate from partner affiliation in animals with monoga- example comes from seahorses and pipefishes, where mous mating systems. Some inbred laboratory rodents males possess a brood-pouch that maintains a placenta- demonstrate ‘facultative’ male parental care without pair- like connection to supply offspring with nutrients [25]. bonding [19,20], where within a specific timeframe after Similarly, amphibian parental care involves egg defense, mating, infanticide is suppressed and males sometimes egg incubation (in dorsal pouch, vocal bag or stomach), lick and groom pups in a coordinated care effort with the and tadpole transport and feeding [4,26,27]. Two clades mother [21]. However, even in these species, female that show extreme diversity in parental care within close- involvement in offspring care is obligate and how neural ly related species are cichlid fish (Family Cichlidae [28]) mechanisms promote care for offspring in a single father and poison frogs (Family Dendrobatidae [26]), making without maternal involvement is unknown. them excellent animal models to ask how the brain promotes parental behavior within a comparative context. A good strategy for identifying conserved and causal mechanisms governing parental care is to perform a What poison frogs can teach us about the comparative analysis across closely related species that parenting brain vary in parental care strategies in a manner that is inde- Poison frogs show substantial variation in parental care pendent of pair-bonding. Involvement in offspring care is tactics, including male uniparental care, female uniparen- generally correlated with the natural history of the species tal care, and biparental care [26] (Figure 2d, Phylogeny). and the reproductive benefit for each sex. Most estab- Importantly, both paternal and maternal care occurs with lished animal model systems of parental care have inter- and without pair bonding across different poison frog nal fertilization, which favors female or biparental care species [29]. Most investigations into poison frog behavior presumably due to lack of paternity assurance [22]. Ex- have focused on field observations and manipulations to ternal fertilization in amphibians and fishes provides a study ultimate questions, such as the adaptive value of better substrate for diversification of parental care behav- parenting behavior or the evolution of behavioral diversi- ior. Although most species in these clades do not care for ty within the clade [30,31]. However, studies into proxi- offspring, fish and amphibians offer the greatest diversity mate mechanisms of parental care are sparse even though in parental care strategies (Figure 1), including repeated behavioral diversity of poison frogs nominates these spe- and independent transitions from no offspring care to cies as a promising model system in comparative neuro- biparental care and female or male uniparental care science. Current technological advances, such as high [4,10,23]. Male fish displaying parental care fan and guard throughput sequencing and genome editing methods, eggs, carry their brood in their mouth and even feed their allow researchers to address mechanistic questions in www.sciencedirect.com Current Opinion in Behavioral Sciences 2015, 6:76–81 78 Integrated study of animal behavior Figure 2 (a) Mechanism (b) Ontogeny Medial pallium Habenula Basolateral Periaqueductal Grey Medial Lateral Amygdala Septum Amygdala Ventral Tegmental Area BNS Striatum Nucleus Ventral Preoptic Ventral Accumbens Pallium Area Hypothalamus (c) Adaptive Value (d) Phylogeny Allo bates Epipedobates Phyllobates Dendrobates Oophaga Ranitomeya Clutch size > 10 eggs Clutch size < 10 eggs tadpole group transport transport 1 tadpole at a time Current Opinion in Behavioral