An integrated understanding of paternal care in mammals: lessons from the rodents

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1 Journal of Zoology. Print ISSN REVIEW An integrated understanding of paternal care in mammals: lessons from the rodents T. L. Rymer 1,2,3 & N. Pillay 1 1 School of Animal, Plant and Environmental Sciences, University of the Witwatersrand, Johannesburg, South Africa 2 College of Science and Engineering, James Cook University, Cairns, QLD, Australia 3 Centre for Tropical Environmental and Sustainability Sciences, James Cook University, Cairns, QLD, Australia Keywords adaptation; constraints; fitness; proximate ultimate; rodents; paternal care; parental care. Correspondence Tasmin L. Rymer, College of Science and Engineering, James Cook University, PO Box 6811, Cairns, QLD 4870, Australia. Tel: tasminrymer@jcu.edu.au Editor: David Hone Received 17 November 2017; revised 26 April 2018; accepted 2 May 2018 doi: /jzo Abstract Mammalian paternal care is rare, and often considered synonymous with social monogamy. Numerous hypotheses have been proposed to explain the evolution and function of paternal care in mammals, many assuming that males are important for offspring survival, with accompanying costs and benefits to fathers and mothers. Most hypotheses are taxon-centric, focusing primarily on three mammalian orders. Consequently, there is no definitive one size fits all hypothesis that adequately explains the evolution of mammalian paternal care. Here, we review both proximate (ontogeny, mechanisms) and ultimate (adaptive significance, evolution) questions to provide an integrated perspective of paternal care, focussing on the rodents. Firstly, we describe the behavioural machinery, and then the neuroendocrine, genetic end environmental factors that regulate and modulate paternal care. We suggest that the behavioural machinery of parental care is conserved in both males and females, although parental care is regulated in a sex- and species-specific manner. Secondly, we provide hypotheses for the evolution and function of paternal care. In contrast to previous studies, we consider seven adaptive hypotheses that explore the possibility of paternal care benefiting the offspring, mothers and/or fathers. We also consider three constraints hypotheses. We suggest that paternal care does not have to incur a survival benefit to offspring to evolve. Instead, the combined benefits to fathers, mothers and offspring should out-weigh the costs to fathers of providing care. Our suggestions for integrating proximate and ultimate explanations for why and how male rodents provide paternal care are applicable across taxa. Integrating these explanations is complicated because the adaptive consequences are context and species-specific. Therefore, future research should integrate these approaches within and between a wide array of taxa. Introduction Paternal care is any non-gametic investment by fathers postfertilization that directly (e.g. huddling, Woodroffe & Vincent, 1994) or indirectly (e.g. alarm calling, Malcolm, 1985), influences offspring growth, survival and/or development. It is rare (5 10% of mammalian species; Woodroffe & Vincent, 1994), possibly because males do not associate with offspring prenatally (Maynard Smith, 1977). Paternal care is often considered synonymous with social monogamy, although it occurs in only 59% of socially monogamous species (Lukas & Clutton-Brock, 2013). Numerous hypotheses are proposed to explain the evolution of mammalian paternal care, the majority assuming fitness benefits to offspring (Bredy et al., 2004) and parents (Woodroffe & Vincent, 1994). However, costs of paternal care are considerable (e.g. lost mating opportunities, Woodroffe & Vincent, 1994), so paternal care likely evolves when the benefits of providing care outweigh the costs (Gubernick & Teferi, 2000). While mammalian mothers are constrained to care for offspring (Gittleman & Thompson, 1988), males are not similarly constrained and can seek additional matings (Woodroffe & Vincent, 1994). Yet, this cannot explain why paternal care occurs in some species. Here, we integrate Tinbergen s (1963) proximate ultimate four-question approach (ontogeny, causation, survival value and evolution) in the context of paternal care in rodents. We focus on rodents because they are generally the best studied mammalian order regarding paternal care. We first provide an integrated perspective on the ontogeny and causal mechanisms of paternal care in rodents. Distinguishing between these proximate questions is challenging. Tinbergen (1963) defined the Journal of Zoology (2018) ª 2018 The Zoological Society of London 1

2 Paternal care in rodents T. L. Rymer and N. Pillay ontogeny of behaviour in the context of the machinery, mainly the brain and central nervous system. However, other ontogenetic factors can modify the machinery, leading to behavioural changes. We then review the evolution and adaptive significance of paternal care in rodents. In contrast to previous studies, we consider the possibility of paternal care benefiting offspring, mothers and fathers. Finally, we integrate proximate and ultimate reasons to explain mammalian paternal care generally. Development and expression of paternal care The behavioural phenotype results from complex genotype environment interactions, the components of which are difficult to tease apart (Plomin & Hershberger, 1991). To understand how paternal behaviour is expressed and regulated, the requisite behavioural machinery must first be identified. A concern with understanding proximate mechanisms of paternal behaviour is that much of our understanding stems from studies of laboratory rodents that are not naturally paternal. While some studies on naturally paternal species support these laboratory rodent studies, the existence of a universal proximate mechanism across and within taxa is unlikely, and might be species-specific. We provide a broad review of these mechanisms, but are mindful that these are non-exhaustive nor currently resolved. The behavioural machinery of paternal care Paternal care in naturally biparental species (e.g. California mice Peromyscus californicus, Lee & Brown, 2002; prairie voles Microtus ochrogaster, Kirkpatrick et al., 1994a) is regulated by the neuronal complex involving the medial preoptic area (MPOA), bed nucleus of the stria terminalis (BNST) and amygdala, although this regulation is species-specific. For example, lesions of the MPOA and basolateral amygdala negatively impact some paternal behaviours in California mice (e.g. licking and sniffing, Lee & Brown, 2002, 2007), but not in prairie voles, where, instead, lesions to the medial nucleus (MeA) and corticomedial amygdala negatively affect total contact time with pups (Kirkpatrick et al., 1994a). The vomeronasal system is also involved in the regulation and expression of parental care in some naturally paternal species (e.g. prairie voles, Kirkpatrick et al., 1994b; Kirkpatrick, Kim & Insel, 1994c). The vomeronasal organ (VNO) detects and transfers olfactory signals to the amygdala and BNST via the accessory olfactory bulb (Kohl, Autry & Dulac, 2016), and olfactory bulbectomy reduces paternal care in male prairie voles (Kirkpatrick et al., 1994b). The proposed pathway described in laboratory mice involves the MPOA receiving these impulses, activating MPOA neurons expressing Galanin (Wu et al., 2014), which then activate lateral preoptic area and substantia innominata neurons (Numan et al., 1988), triggering ventral tegmental area neurons (Keverne & Curley, 2004). This area is associated with reinforcement learning, with pups being a strong reinforcing stimulus to males (mandarin voles Lasiopodomys mandarinus, Wang et al., 2012). Ontogenetic factors influencing the behavioural machinery The behavioural machinery underlying parental care is functionally similar in males and females, suggesting conservative neuroendocrinological regulation (see Dulac, O Connell & Wu, 2014; and Rilling & Young, 2014). However, sex-specific patterns of gonadal hormone secretion during ontogeny may accompany MPOA and BNST neural development (e.g. guinea pigs Cavia porcellus, Hines et al., 1985). Some biparental species (e.g. Siberian Phodopus sungorus and Djungarian Phodopus campbelli hamsters) show sexually dimorphic expression of oestrogen receptor alpha immunoreactive neurons (ERa-IRs) in several brain regions (e.g. BNST) that receive pup-related sensory input from the VNO (Cushing & Wynne-Edwards, 2006), suggesting sex differences in olfactory perception (Zilkha, Scott & Kimchi, 2017). Therefore, hormone activity during development could differentially organize the neural circuitry underlying the expression of parental behaviour in adult males and females, as suggested for prairie voles (Timonin, 2008). Factors influencing the onset, activation and maintenance of paternal care Neuroendocrine factors Neural pathways for paternal care are first organized hormonally in the embryo, and later activated in adulthood (Wynne- Edwards & Timonin, 2007). However, while organizational effects might influence the physical machinery of the synonymous maternal care pathway in males, they are not necessarily required for later activation of the pathway (Timonin, 2008), or maintenance of paternal care once initiated (Gubernick, Schneider & Jeannote, 1994). Several hormones are implicated in the onset and/or maintenance of paternal care. However, their roles are equivocal (Wynne-Edwards & Timonin, 2007), species-specific (Bales & Saltzman, 2016), and their effects are likely influenced by trade-offs with hormones associated with other functions (e.g. competitive ability, Wingfield, Lynn & Soma, 2001). The four most influential hormones are discussed briefly. Oestrogens alter the expression of paternal care in California mice (Trainor & Marler, 2002), but results are equivocal for other biparental species (e.g. prairie voles, Lonstein & de Vries, 1999; mandarin voles, Song et al., 2010). Oestrogens may be important in the maintenance of paternal care in biparental species, since brain regions other than the MPOA (e.g. arcuate nucleus of the hypothalamus) show increased numbers of ERa-IRs in response to offspring presence (Song et al., 2010). Oxytocin (OT) is associated with paternal care in meadow Microtus pennsylvanicus (Parker et al., 2001) and prairie (Kenkel et al., 2012) voles, suggesting its importance in activating and maintaining paternal care (Bales & Saltzman, 2016). However, results are equivocal, with offspring-related stimuli triggering increased OT expression in the paraventricular (PVN) 2 Journal of Zoology (2018) ª 2018 The Zoological Society of London

3 T. L. Rymer and N. Pillay Paternal care in rodents and supraoptic nuclei of virgin male mandarin voles (Song et al., 2010), but not California mice (de Jong et al., 2009). Vasopressin (AVP) enhances paternal care in meadow voles (Parker et al., 2001), but results are equivocal for prairie voles (Lonstein & de Vries, 1999; Bales & Saltzman, 2016). Therefore, AVP may not necessarily stimulate paternal care, but may maintain it following its onset. In support, pup-related stimuli increased activation of AVP-IR cells in the PVN of male prairie voles (Kenkel et al., 2012). Prolactin acts on the brain, although its role in the onset of paternal care in biparental species is questionable (Wynne- Edwards & Timonin, 2007). Prolactin might be critical for organizing neural substrates (Schradin & Anzenberger, 1999), explaining why decreasing prolactin does not compromise paternal care in some species (e.g. Djungarian hamsters, Brooks, Vella & Wynne-Edwards, 2005). Offspring cues also influence prolactin secretion in non-paternal species (e.g. laboratory mice, Mak & Weiss, 2010), suggesting that prolactin may maintain paternal care. Genetic and environmental factors Paternal care is not solely an innate property of endocrine-specific events in response to offspring stimuli (Champagne et al., 2003), given natural individual variation, genetic make-up and experience. Several candidate genes in non-paternal (e.g. Sry gene in laboratory mice, Reisert et al., 2002) and paternal (e.g. genes coding for progesterone, OT and AVP receptor gene expression in California mice, Perea-Rodriguez et al., 2015) species apparently influence paternal care (Champagne & Curley, 2012). Likewise, quantitative genetic studies have revealed heritability for paternal care in some biparental rodents (e.g. striped mice Rhabdomys pumilio, Rymer & Pillay, 2011a), although studies are rare. In California mice, parental care increases neuronal plasticity in numerous brain regions, including the MPOA and BNST (de Jong et al., 2009) and dentate gyrus of the hippocampus (Glasper et al., 2011). Direct paternal care varies between fathers (e.g. striped mice, Rymer & Pillay, 2011b), and could be epigenetically transmitted to offspring (e.g. mandarin voles, Jia et al., 2011), possibly driven by changes in AVP-IR in the PVN and/or BNST (e.g. California mice, Frazier et al., 2006). Furthermore, paternal care influences synaptic development in several brain regions (e.g. orbitofrontal cortex, Helmeke et al., 2009; amygdala and hippocampus, Seidel et al., 2011) of male offspring (e.g. trumpet-tailed rats Octodon degus). Alterations to these brain regions could influence supportive paternal care behaviours (e.g. resource acquisition, territory maintenance) via their impact on problem-solving, learning and decision-making (e.g. California mice, Bredy et al., 2004). Indirect genetic effects (IGEs) occur when variation in the quality of the environment (e.g. nest/burrow) provided by parents reflects genetic differences among them (Wolf et al., 1998). Environmental effects derived from this parental variation are considered inherited environments because the parental phenotypes producing these environmental effects in offspring could be heritable (Wolf et al., 1998). Paternal effects are specific IGEs derived from the environment provided by fathers. They occur when fathers are influenced by environmental factors (e.g. changes in resource availability), which impact offspring (or grandoffspring, Curley, Mashoodh & Champagne, 2011). Paternal effects also occur when fathers influence maternal care of their mates. The father s absence can lead to reduced (e.g. trumpet-tailed rats, Helmeke et al., 2009) or increased (e.g. striped mice, Rymer & Pillay, 2011b) maternal care. In striped mice, females compensate for a lack of paternal help when raising offspring alone, resulting in adult sons providing more care to their own offspring (Rymer & Pillay, 2011b). Environmental effects induce lasting physiological, neural and behavioural changes (e.g. prolactin can be regulated by environmental stimuli; Schradin & Pillay, 2004), and changes in experience can also impact neuromodulator (e.g. oestrogens) expression, causing adjustments in behaviour in response to changes in social organization. For example, mating, paternal experience and offspring exposure alter ERa and OT receptor levels in mandarin voles, leading to elevated paternal care (Song et al., 2010). Evolution and adaptive significance of paternal care While paternal care evolved independently across mammalian lineages, and succeeded the evolution of social monogamy (Lukas & Clutton-Brock, 2013), its evolution within lineages is debated. Arguments arise over benefits versus costs of paternal care (Woodroffe & Vincent, 1994) because lifetime reproductive success of male mammals is mainly determined by numbers of matings than numbers of offspring raised, since males are unable to provide direct care prenatally (Queller, 1997). Few rodent taxa have been studied intensively, so many proposed hypotheses are not generalizable across taxa. Generally, two broad groups of hypotheses are proposed for mammals, which could explain the evolution of paternal care in rodents. (1) Fitness-enhancing hypotheses assume that paternal care evolved because there was an initial direct benefit to offspring, fathers and/or mothers. (2) Constraints hypotheses assume that paternal care evolved in the absence of fitness-related benefits, but males were constrained to remain with females and/or offspring due to extrinsic (ecological) or intrinsic (physiological) constraints. Fitness-enhancing hypotheses A male s fitness can increase through providing care if (1) his offspring survive and reproduce (paternity certainty hypothesis, Trivers, 1972), and/or (2) he gains additional mating opportunities (mating effort hypothesis, Smuts, 1985). Certainty of paternity, achieved through offspring recognition, is presumably a contributor to the evolution of paternal care. Yet, certainty of paternity is not always correlated with paternal care in muroid rodents (Hartung & Dewsbury, 1979). Furthermore, a male s fitness could be increased if females prefer better fathers (Stiver & Alonzo, 2009), yet not all females show such a preference (e.g. striped mice, Rymer & Pillay, 2010). Journal of Zoology (2018) ª 2018 The Zoological Society of London 3

4 Paternal care in rodents T. L. Rymer and N. Pillay Therefore, male fitness benefits do not adequately explain the evolution of paternal care in rodents. Paternal care can contribute to offspring survival, growth and/or development (Maynard Smith, 1977), particularly when resources are limited (male care hypothesis, Gubernick & Teferi, 2000), or there is a risk of infanticide (anti-infanticide hypothesis, Sommer, 1997), such as in California mice (Gubernick et al., 1994) and Mongolian gerbils Meriones unguiculatus (Elwood, 1980). However, while offspring fitness benefits might promote the evolution of paternal care in some taxa, the lack of paternal care in some socially monogamous species (Lukas & Clutton-Brock, 2013), and a lack of studies demonstrating the adaptive significance of paternal care (specifically offspring fitness benefits, Gubernick & Teferi, 2000), suggests that paternal care is not necessarily crucial for infant survival. Finally, paternal care could evolve directly through alleviating reproductive costs (i.e. lactation and daily energy expenditure, Gittleman & Thompson, 1988) of females (loadlightening hypothesis, West & Capellini, 2016). Males making energetic contributions (e.g. provisioning food or huddling offspring) enable females to redirect resources into reproduction (Woodroffe & Vincent, 1994) or foraging (e.g. trumpet-tailed rats, Helmeke et al., 2009), although such a reduction in maternal workload is not generalizable across rodent families (West & Capellini, 2016). Consequently, female fitness benefits are not the sole explanation for the evolution of paternal care in rodents. Constraints hypotheses While number of matings achieved determines a male s lifetime reproductive success (Queller, 1997), multiple matings can incur significant costs (e.g. testosterone production, Wingfield et al., 2001; increased predation risk during dispersal/ mate searching, Emlen, 1994). Therefore, the benefits associated with greater competitive ability are traded off against other fitness-related traits (physiological constraints hypothesis), including paternal care (but see Trainor & Marler, 2002). Resource limitation, due to spatiotemporal environmental variation and unpredictability, influences dispersal strategies (Maher & Burger, 2016) and the evolution of cooperative behaviours (Emlen, 1994). Limiting resources favour males defending exclusive territories into which females disperse (social constraints hypothesis, Payne & Payne, 1993), leaving little opportunity for additional matings. Amicability, social tolerance (Carr & MacDonald, 1986) and/or paternal care could emerge consequently. Under limiting resources, clumping of individuals due to costs associated with dispersal into potentially resource-poor environments (Emlen, 1994) could lead to mate guarding (or harem defence) and paternal care (ecological constraints hypothesis, Maher & Burger, 2016). The extent of paternal care, and its subsequent cost to males, likely varies among individuals and species across ecological conditions due to historical and physiological processes (Requena & Alonzo, 2017). Therefore, constraints hypotheses in isolation do not adequately explain why paternal care has not evolved in rodents species generally. Integrating proximate and ultimate questions to understand paternal care in rodents Unlike maternal care, mammalian paternal care is less studied. Although rodent studies have focused on the ontogeny and mechanism of paternal care (Champagne & Curley, 2012), and the adaptive significance and evolution of paternal care (Gubernick & Teferi, 2000), few studies have explored both proximate and ultimate explanations in the same species, with ultimate explanations outstripping proximate research. Given the considerable scientific attention already given to California mice, prairie voles and striped mice, these provide worthy candidates for future considerations integrating proximate ultimate explanations. Nonetheless, other candidate species may be identified among mammals in general. Proximate and ultimate questions can be integrated to understand paternal care in rodents, and mammals generally (Fig. 1). The interactions suggest complicated, complex and inter-connected relationships, our understanding of which is limited due to severe gaps in our knowledge. Environmental factors (biophysical and social) drive constraints directly (ecological constraints, a in Fig. 1), or indirectly (social and/or physiological constraints, b). The interactions between the biophysical and social environments are mostly unidirectional (c), although the social environment can influence resource availability. Critically, environmental factors directly influence all aspects of the male s phenotype (d). The onset, activation and maintenance of paternal care is governed by complex interactions in neuroendocrine systems that change during ontogeny (e). The behavioural machinery underlying paternal care is hormonally organized (f), and the activation and maintenance of paternal care is hormonally regulated. These physiological changes influence the interactions of males with conspecifics, including offspring (g). Direct interactions with offspring, and experience of providing care (h), feedback to the neuroendocrine systems, generating neuronal plasticity, and causing a cascade of physiological effects, further altering behaviour (e.g. through epigenetic effects, i). The interactions between these systems ultimately drive physiological constraints directly (j) or indirectly (k). A male s underlying neuroendocrine systems could influence his perception and response to environmental and social stimuli, including females (mating effort, l) and offspring (certainty of paternity, m), which change with ontogeny (Schradin & Yuen, 2011). Consequently, the benefits offspring accrue from receiving paternal care are also influenced by neuroendocrine and ontogenetic mechanisms in the father (n). Finally, male female interactions are also influenced by male endocrine factors directly influencing his neural circuity. Ontogenetic changes (e.g. development and maturation of the reproductive organs), coupled with associated behavioural changes driving female male interactions, potentially lead to females accruing benefits (load-lightening; n). While the relationships between the proximate mechanisms and the ultimate causes for the antiinfanticide hypothesis are not clear, a reduction in infanticide could arise as a by-product of behaviours performed for other reasons (o). 4 Journal of Zoology (2018) ª 2018 The Zoological Society of London

5 T. L. Rymer and N. Pillay Paternal care in rodents Figure 1 An integrated understanding of paternal care demonstrating complex, inter-connected relationships. Solid lines indicate direct effects. Dashed lines indicate indirect effects. Environmental factors drive constraints (a, b), and the biophysical environment impacts the social environment (c). Environmental factors influence all aspects of the male s phenotype (d). Paternal care is governed by complex interactions in neuroendocrine systems that change during ontogeny (e), and the behavioural machinery underlying paternal care is organized by hormones (f). Furthermore, physiological changes influence conspecific interactions (g) which, together with experience (h), feedback to neuroendocrine systems, further altering behaviour (i). The interactions between these systems drive physiological constraints (j, k). The neuroendocrine systems also influence male perception and response to females and offspring, which change with ontogeny (l). Consequently, potential benefits to males, females and offspring (m, n) are also influenced by neuroendocrine and ontogenetic mechanisms in the father. A reduction in infanticide could also arise as a by-product of behaviours performed for other reasons (o). Conclusions Our review of the ontogeny, mechanisms, adaptive significance and evolution of paternal care in rodents can be applied to a general understanding of mammalian paternal care. However, unlike maternal care, which is phylogenetically constrained in mammals (Dall & Boyd, 2004), paternal care can be initiated de novo (e.g. appearance of pups; Champagne et al., 2003) and by receiving stimuli that activate previously organized neural pathways to elicit neuroendocrine changes. While the evolution of paternal care involves complex gene-phenotypedevelopment patterns that resemble maternal care, and some of the behavioural machinery underpinning paternal care is homologous with maternal care, our understanding is currently limited to a few naturally biparental species that have been intensively studied. Furthermore, the fitness benefits of providing paternal care are not clearly understood. While the evolution of different strategies of lactation in females have been debated (Dall & Boyd, 2004), the benefits of suckling for offspring are obvious. However, unlike females, males can desert their mates and offspring. Therefore, males that provide care do so under a particular set of circumstances that could incur fitness benefits to them, their mates and/or offspring. This might explain the existence of various functional hypotheses that are not generalizable, although a lack of information in most taxonomic groups of mammals also makes generalisations difficult. Therefore, unlike maternal care, expecting a one size fits all hypothesis for paternal care across multiple species is unreasonable. There is a desperate need for broader studies using a multi-faceted proximate/ultimate approach involving within and between species comparisons in freeliving species. Acknowledgements TLR was supported by James Cook University and the Centre for Tropical Environmental and Sustainability Sciences. NP is funded by grants through the National Research Foundation and the University of the Witwatersrand. We thank Nigel Bennett for presenting us with the opportunity to write this review. Journal of Zoology (2018) ª 2018 The Zoological Society of London 5

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