The evolution of paternal care: a role for microbes?

Abstract

10Paternal care is an evolutionary mystery. Despite extensive research, both theoretical and 11 experimental, the reasons for its ubiquity remain unclear. Common explanations include kin 12 selection and limited accuracy in parentage assessment. However, these explanations do not 13 cover the breadth of circumstances in which paternal care has been observed, particularly in 14 cases of uncertain paternity. Here we propose that microbes may play a key role in the 15 evolution of paternal care among their hosts. Using computational models, we demonstrate 16 that microbes associated with increased paternal care could be favoured by natural selection. 17 We find that microbe-induced paternal care could evolve under wider conditions than 18 suggested by genetic models. Moreover, we show that microbe-induced paternal care is more 19 likely to evolve when considering paternal care interactions that increase microbial 20 transmission, such as feeding and grooming. Our results imply that factors affecting the 21 composition of host microbiome may also alter paternal behaviour. 22 Keywords 23 Microbiome, paternal care, mathematical model, extra-pair mating, sexual conflict, 24 nongenetic inheritance 25 26When would a father benefit more from caring for its offspring, rather than looking for 27 additional mating opportunities? This question has been broadly addressed both theoretically 28 and experimentally. Paternal care was frequently observed among avian species 1 (~85%), and 29 was also found in mammalian species 2 (~5%), amphibians 3 , and many species of fish 4 . 30Paternal care is most commonly observed alongside maternal care, while exclusive paternal 31 care is rare 4,5 . A male may demonstrate care for its offspring with several types of 32 interactions 4,5 , such as feeding, grooming, or guarding against predators. It can also provide 33 spousal care for the female while she cares for the young 6,7 . 34A commonly proposed explanation for the prevalence of paternal care is kin selection 8,9 . This 35 explanation suggests that paternal care would be favoured whenever the paternal contribution 36 to offspring survival increases paternal fitness more than pursuing additional mating 37 opportunities 10,11 . In some settings, such as caring for unrelated young, this explanation is 38 insufficient, and alternative explanations are suggested 12,13 . Interestingly, studies relating 39 paternal effort to certainty of paternity obtained mixed results 14-20 , and paternal care has been 40 observed even in cases of very high probability of extra-pair paternity (e.g. in avian species 21 41where extra-pair parenthood can range up to 95% in fairywrens 22 ). 42Here we consider the potential role of the microbes in host paternal care. The microbiome is a 43 significant agent affecting host health and behaviour [23][24][25][26][27] , through pathways such as the 'gut-44 brain axis' 28 . Numerous studies have demonstrated a possible association between microbes 45 and social behaviour [29][30][31][32][33][34] , and certain species o...

Social complexity as a driving force of gut microbiota exchange among conspecific hosts in non-human primates

“…The evolution of cooperative behaviors should consider the strength of selection, the heritability of the group and individual level traits, and the genetic correlation between them ( Goodnight, 2005 ). However, given different examples of adaptability provided by studies of symbiotic relationships with microorganisms ( Li et al, 2008 ; Ezenwa et al, 2012 ; Cani et al, 2019 ; Gurevich et al, 2020 ), it is highly unlikely that natural selection could be applying any selective mechanisms only to genotypes or phenotypes of individuals.…”

“…This implies, on the one hand, the understanding of the role that the microbiome could play in the evolution of social behavior. For now, mathematical models suggest that the microbiome is key to explain the evolution of complex social behaviors, such as altruism, cooperation, and parental care ( Lewin-Epstein et al, 2017 ; Gurevich et al, 2020 ; Lewin-Epstein and Hadany, 2020 ). On the other hand, several hosts forming a social group can modify their social microbiome, as well as microbial transmission routes ( Miller et al, 2018 ), by making shared or unshared decisions for accessing to resources (e.g., beneficial endosymbionts).…”

“…In addition to the possibility of microbial transmission involved in group living, Stilling et al (2014) proposed considering the non-protein-coding regions, transcribed into RNA and with promising roles in neurodevelopmental processes, as part of an integrated model to understand the evolution of -human- social behavior. More recently, results of computational simulations driven by mathematical models in which natural selection acts on microbes harbored by interacting individuals show that microbes may affect the tendency of their hosts to cooperate or display paternal care behaviors ( Lewin-Epstein et al, 2017 ; Gurevich et al, 2020 ; Lewin-Epstein and Hadany, 2020 ). Lastly, to fully capture the dynamics of host-microbial systems, ecological metacommunity theory has been expanded to include the feedback between the host-as-patch and its microbial communities as well as between the hosts and the species pool ( Miller et al, 2018 ).…”

Addictions may be driven by competition-induced microbiome dysbiosis

“…Previous models studied interactions between microbial strains within the microbiome [26][27][28] and also host-microbe interactions [29][30][31][32] . Here we combine these two approaches into a framework that models the eco-system of a host, whose wellbeing and behavior alters the microbiome composition, and the microbiome, which affects the host state.…”

Microbiome-related aspects of locust density-dependent phase transition

“…Recent studies have revealed mechanisms by which the microbiome can affect its host behavior [15,16], including insects [17,18]. Other studies have explored the evolutionary perspective of microbiome-induced social interactions [19][20][21]. In the current controlled laboratory study we used the desert locust (Schistocerca gregaria) as a model with which we directly explore the association between solitary-togregarious phase transition and the individual locust's microbiome.…”