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Stabilization and optimization of host-microbe-environment interactions as a potential reason for the behavior of natal philopatry

Animal Microbiome volume 3, Article number: 26 (2021) Cite this article

Abstract

Many animals engage in a behavior known as natal philopatry, where after sexual maturity they return to their own birthplaces for subsequent reproduction. There are many proposed ultimate factors that may underlie the evolution of natal philopatry, such as genetic optimization, suitable living conditions, and friendly neighbors, which can improve the survival rates of offspring. However, here we propose that a key factor that has been overlooked could be the colonization of gut microbiota during early life and the effects these microorganisms have on host performance and fitness. In addition to the bacteria transmitted from the mother to offspring, microbes from the surrounding environment also account for a large proportion of the developing gut microbiome. While it was long believed that microbial species all have global distributions, we now know that there are substantial geographic differences and dispersal limitations to environmental microbes. The establishment of gut microbiota during early life has enormous impacts on animal development, including energy metabolism, training of the immune system, and cognitive development. Moreover, these microbial effects scale to influence animal performance and fitness, raising the possibility for natural selection to act on the integrated combination of gut microbial communities and host genetics (i.e. the holobiont). Therefore, in this paper, we propose a hypothesis: that optimization of host-microbe-environment interactions represents a potentially important yet overlooked reason for natal philopatry. Microbiota obtained by natal philopatry could help animals adapt to the environment and improve the survival rates of their young. We propose future directions to test these ideas, and the implications that this hypothesis has for our understanding of host-microbe interactions.

Introduction

In nature, many species with long migration distances display some degree of natal philopatry, or returning to their birthplace to breed the next generation [1, 2]. By means of this activity, animals can meet the environmental conditions they need during a specific period of life, likely resulting in higher survival and fitness of individuals [3,4,5]. However, the ultimate mechanisms underlying the evolution of natal philopatry are still poorly understood. There has been a recently renewed appreciation for the role that host-associated microbes play in the performance and fitness of wild animals [6,7,8,9], including aspects of animal behaviors [10]. In this perspective article, we propose a potential role for these interactions to play in the evolution of natal philopatry. Specifically, we argue that by parents returning to natal habitats to breed, new offspring will acquire the optimal microbiome for their own physiological performance and fitness. We recognize that this idea is largely speculative but feel that it represents an exciting area for future research.

Natal philopatry is a life-history strategy where animals locate and return to reproduce at the same geographic location in which they were born [11]. An equivalent term, “natal homing”, was first used when describing the migratory and breeding habits of sea turtles [12]. In addition to sea turtles and well-known groups such as songbirds and salmon, many other animal groups engage in natal philopatry (Table 1). The prevalence and taxonomic distribution of natal philopatry has been reviewed elsewhere for mammals [30] and birds [31, 32].

Table 1 Examples of natal philopatry
Full size table

In recent decades, there has been a renewed appreciation for the fact that animals evolved in a world already dominated by microbes [33]. Therefore, many physiological processes in animals are intertwined with the action of microbial symbionts. Host-associated microbial communities have a number of impacts on their hosts, such as assisting with digestion or nutrient synthesis [34], providing protection against pathogens [35], aiding in the development of the immune system [36], and determining life history traits [37]. The hologenomic theory of evolution considers the collection of host and microbial genomes—known as ‘the holobiont’—a biological unit of organization upon which natural selection can act [38, 39]. There are numerous examples of connections between hologenomic evolution and aspects of animal behavior [10]. Here, we propose that microorganisms present in the natal habitat may be more suitable or beneficial for offspring, and thus returning to the natal habitat for reproduction may provide a fitness benefit to animals. We set up the rationale for this hypothesis by first reviewing the basics of natal philopatry, and then discussing how host-microbe interactions fit within these existing theories.

Mechanisms for Natal Philopatry

How do animals locate their birthplaces to reproduce and generate offspring? Several proximate mechanisms for natal philopatry have been proposed. Early work on homing in turtles hypothesized that this behavior was proximately driven through “social facilitation”, where first-time breeders follow experienced females to a nesting beach, and having had a “favorable” breeding experience, fix on that site for future nesting [2, 40]. Related, Nordeng et al. (1977) proposed a “pheromone hypothesis”, where anadromous salmon might produce population-specific odors which guide them in homing migration [41]. However, imprinting on the natal site itself is seems to be the most accepted mechanism underlying this behavior. Genetic analysis of natal philopatry in sea turtles is quite consistent with natal homing expectations and indicate that social facilitation to non-natal sites is uncommon [42]. There is some evidence sea turtles may imprint on the geomagnetic features of their natal beaches to return to these sites for reproduction [43]. Additionally, although definitive evidence is lacking, it is widely assumed that Pacific salmon imprint on key features of their nesting region, like the chemical profile of the beach or surrounding waters, during development, and then use this information to return as adults [44].

While these hypotheses explain the proximate mechanisms of how animals are able to locate their natal sites, the evolutionary reasons, or ultimate mechanisms, for natal philopatry are still poorly understood. Below we briefly outline the current theories of the ultimate mechanisms for natal philopatry. For example, the advantage of local knowledge may enable animals to optimally exploit the resources of the area and to successfully defend their territories against competitors [45, 46]. Thus, over many generations and through natural selection, populations would become adapted to the conditions prevailing in their natal habitat [45, 46]. Indeed, individual Collard Flycatchers that are more philopatric exhibit higher reproductive fitness than those that disperse over larger distances [47]. Similarly, philopatric individuals of the Great Reed Warbler exhibit higher lifetime fitness when compared to immigrant individuals [5].

Reasons for animal’s natal philopatry

Evolutionary and genetic optimization

The distance that young animals disperse from their place of origin before breeding has important implications for the extent of inbreeding and for the genetic structure of populations. Indeed, natal philopatry tends to result in high relatedness among individuals at a particular site [48, 49]. It has been proposed that natal philopatry may actually promote an optimal rate of inbreeding. While inbreeding is often viewed as detrimental due to the increased fixation of deleterious alleles, it can also offer benefits if alleles at various loci across the genome interact with each other in a beneficial manner. Thus, optimal inbreeding can reduce the costs of meiosis and recombination by preserving these interactions [50]. Such genetic optimization could be especially important for local adaptation associated with philopatry. For example, Coho salmon (Oncorhynchus kisutch) from more interior streams have greater swimming stamina as an adaptation to the longer migration distances [51]. It has previously been argued that gene flow between populations may erode these local adaptations [52]. Further, given that complex traits and adaptations are likely polygenic, maintenance of interacting alleles could also be important [53]. These genetic mechanisms could underlie the evolutionary benefits of natal homing behaviors.

Suitable environmental factors

Animals may also return to their birthplace for reproduction because these natal environments are most suitable for the growth and development of their young, including suitable temperature, abundant food resources, low abundances of predators, and nesting sites with superior geographical location. For example, female Pine snakes (Pituophis melanoleucus) show a high degree of nest site philopatry because it promotes location of sites that provide suitable temperature conditions [54]. Temperate zone bat species are believed to form summer maternity colonies to provide the appropriate thermal conditions for the growth and survival of their offspring [55]. Natal philopatry in bannertailed kangaroo rats (Dipodomys spectabilis) may be a means of providing juveniles with access to essential resources, such as food caches and large complex burrow systems, that are not readily available outside natal home ranges [56]. Overall, by returning to the same site for reproduction each year, individuals can be assured of the suitable environmental conditions to support growth, maturation, and survival of their young.

Maintaining social networks

Natal homing can help animals establish familiar community structure and reduce resource competition. In Antarctic fur seals (Arctocephalus gazella), adults of both sexes return to within a few meters of the breeding sites that were held in previous years [57]. Such behavior could potentially be adaptive in a crowded and highly competitive environment, perhaps by facilitating the re-occupation of previously held territories [58] or by creating stable neighborhood networks in which overall levels of conflict are minimized [59].

Beyond reducing competition, natal philopatry may help to maintain familiar social networks. For bottlenose dolphins (Tursiops truncatus), philopatry offers the benefits of familiar social networks and foraging habitats [60]. Additionally, it is thought that natal philopatry in Brown long-eared bats (Plecotus auritus) could be driven by the social benefits of associating with familiar individuals [28]. Thus, homing behavior may serve as a mechanism to sort and distribute animals, and in the process may maintain social benefits or decrease intraspecific competition for resources.

Another potential reason for natal philopatry: host-microbe-environment interactions

The fact that animals evolved in a world already dominated by microbes [33] opens the possibility for microbial involvement in the processes of natal philopatry. First, microbes could play a role in the proximate mechanisms of animals locating their natal sites. While many animals imprint on the geomagnetic features of their natal sites [43], we have a poor understanding of how animals sense and respond to magnetic fields, including the fact that bona fide animal magnetoreceptors have still not been identified [61]. It has recently been proposed that symbiotic magnetotactic bacteria could contribute to these capabilities [62]. For example, host-associated magnetotactic bacteria may aggregate based on the geomagnetic field and provide signals to their hosts [62]. Additionally, microbes may be involved in the location of natal sites using chemical cues given the large repertoire of volatile compounds they produce, which are also involved in inter-kingdom interactions [63]. For example, microbes create volatile compounds that may be used for inter-host communication, such as on the scent glands of hyenas [64] or the uropygial glands of birds [65]. Some soil bacteria also generate volatile compounds that attract small invertebrates (springtails), which then feed on the bacteria and mediate the dispersal of bacterial spores [66] . Therefore, it could be that local environmental microbes produce volatile compounds to act as proximate signals for the location of natal sites.

Beyond the location of natal sites, we propose that acquiring the optimal composition and structure of microorganisms may also be a reason why animals return to their birthplace for reproduction. Analogous to the ultimate factors previously proposed for the evolution of natal philopatry (Evolutionary and genetic optimization, Suitable environmental factors, and Maintaining social networks), we propose that host-microbe interactions during early life could be involved in (i) evolutionary and hologenomic optimization, (ii) acclimating to local environmental conditions and (iii) the social benefits of natal philopatry. While the connections between natal philopatry and microbial ecology have not been thoroughly investigated, we present a series of studies that provide interesting data supporting this hypothesis.

Evolutionary and hologenomic optimization

Our understanding of the evolutionary importance of host-microbe interactions is rapidly increasing. Host-microbe interactions have the capacity to affect many aspects of host performance and fitness [67]. Numerous studies across animal taxa have demonstrated that there are optimal combinations between host genetics and associated microbial communities, such that inoculating animals with the microbial communities from heterologous host species reduces performance and fitness [9, 68,69,70]. For example, individuals of Peromyscus polionotus inoculated with the microbes from other Peromyscus species exhibit decreased rates of food digestibility [9]. Additionally, both Drosophila flies, Nasonia wasps, and Caenorhabditis worms exhibit decreased fitness when inoculated with the microbiomes of congener hosts [9, 68,69,70]. Last, animals that are the hybrids of two species often suffer from incompatibilities between the host genome and the microbiome, leading to detrimental effects, such as gut inflammation or lethality [71, 72]. Thus, it is increasingly being recognized that we must expand our view of biological interactions to be a combination of GenomeHost x GenomeMicrobial x Environment interactions [38, 73]. For wild animals, ensuring that offspring associate with the proper microbial community in early life (described more in the sections below) could have large fitness consequences for reproducing animals.

These microbial associations can be especially important during early life [74]. Animals exhibit developmental windows during which microbial interactions are especially crucial [75]. For example, disruption of the microbiome in larval zebrafish can cause lasting changes to behavior and neurodevelopment [76]. Similarly, tadpoles reared under depleted microbial conditions exhibit increased susceptibility to later parasitic [77] and viral infections [78]. Moreover, early associations with particular microbes in early life can also influence the ability for subsequent microbes to take hold, a process known as priority effects or historical contingency [79]. Therefore, exposure to early environmental microbes could have life-long impacts on what other microbes are able to colonize animals. Given the effects that microbes can have on host digestion [34], protection against pathogens [35], the development of the immune system [36], associating with the proper microbial communities in early life has the potential to yield lifelong fitness effects.

Microbes as environmental factors

How then, do animals obtain their microbiome? Starting at birth or hatching, the microbiota develops from a simple, unstable community into a complex and climax community [74]. While a portion of the microbiome is vertically transmitted [80], a number of environmental microbes are also important early colonizers [81]. For example, some animal species predominantly acquire host-associated microbial communities from the environment each new generation, such as stinkbugs [82] and bioluminescent squid [83]. Studies in tadpoles [84] and several fish species [85, 86] demonstrate that the gut microbiota largely reflects those microbes present in their surrounding environments. In nest-building species, such as birds, the characteristics and environmental microbiome of nesting material can influence the composition of their offspring’s microbiome [87, 88]. Experimental research on laboratory mice [89] and wild Peromyscus mice [90] have also demonstrated that the gut microbiome of mammals can be determined by their juvenile environment. Thus, the microbiome of the surrounding environment could have important implications for the assembly of host-associated communities.

Additionally, environmental microbial populations exhibit substantial spatial heterogeneity across the landscape. While it had long been assumed that “everything is everywhere” [91], recent studies demonstrate that both terrestrial and aquatic microbial communities exhibit considerable biogeographic trends, resulting in heterogeneity of microbial diversity and community structure over geographic space [92, 93]. This spatial heterogeneity may contribute to the well-documented effects of geography on host-associated microbial communities [94]. For example, when comparing the gut microbial communities wild mice obtained from across France and Germany, results showed that patterns of microbiota diversity were principally explained by the geographical location of the mice, with weaker effects due to the genetic distance [95]. Other work has found that sympatric populations of gorillas and chimpanzees share more bacterial taxa than gorillas and chimps from disparate regions, suggesting a potential of limits to microbial dispersal [96]. The cloacal microbiota of fledgling greater flamingos (Phoenicopterus roseus) varied substantially across nine breeding sites, suggesting that local environments harbor distinct microbial communities [97].

The geographic variation in environmental microbes may carry “signatures” relating to characteristics of the local environment. For example, over large geographic scales the biogeographic distribution of soil microbes is driven by temperature [98, 99]. Host-microbe interactions have been implicated in thermal physiology of hosts [100] and their adaptations to local climate [101]. Thus, it could be that animals acquire environmental microbes that are adapted to certain aspects of the local environment (temperature, frequency of disturbance, etc.), and thereby convey related physiological benefits to their hosts. However, it should be noted that we still have a poor understanding of the spatial heterogeneity of environmental microbes on spatial scales that may be ecologically relevant to natal philopatry. For example, in a study of philopatric songbirds, a dispersal distance of roughly 1000 m from the natal habitat yielded lower fitness [47], while studies investigating site-specific avian microbial communities typically use greater spatial distances between sites [97, 102].

Microbes as a social benefit

Analogous to how natal philopatry may yield the social benefits through cooperation or reduced competition, there may be microbial benefits to living together [103]. The behavior of allo-coprophagy, where offspring consume the feces of adult individuals, including unrelated individuals, has been recorded in insects [104], reptiles [105, 106], birds [107], and mammals [108, 109]. This behavior can be important for juveniles to become inoculated with a microbial community. For example, cockroaches regularly consume feces of conspecifics, and doing so results in colonization of the gut and enhanced growth and tissue development [110] . Similarly, green iguanas regularly consume the feces of adult individuals [105], and doing so increases their ability to digest plant material and improves growth rates [111].

Even if not a principal source of microbial inoculation, group living has also been demonstrated to result in microbial sharing between individuals. Numerous social or gregarious insect species transmit some beneficial microbes between individuals [112,113,114]. In baboons, the degree of social interactions between individuals can explain a significant portion of microbial sharing [115]. Additionally, dispersal of individuals to join unrelated groups can result in acquisition of new microbial communities, and individuals that engage in more grooming behavior share similar microbial communities [116]. Similarly, affiliative behaviors between unrelated individuals of feral horses correlate with similarities in gut microbial community structure [117]. Thus, returning to the natal site for breeding may expose offspring to a social network and associated microbial symbionts that may be acquired through social transmission.

Caveats

It is important to acknowledge that our framework also has caveats. First, while natal philopatry is a relatively common behavior across animal taxa (Table 1), studies of this behavior may suffer from a reporting bias towards those that exhibit philopatry or are easier to study [32]. Second, natal philopatry is not always an adaptive behavior. In contrast to studies cited earlier, a study of Western gulls showed that philopatric individuals had lower survival and reproductive fitness, leading to a conclusion that the benefits of this life history strategy may vary temporally and spatially [118]. Similarly, the benefits of microbial interactions may also be variable across space and time. Related, our framework is largely rationalized by philopatry promoting the stabilization of environment-host-microbe interactions. However, novel microbial communities are thought to be a route by which animals may gain enhanced capabilities and adapt to novel environments [119]. Therefore, there may be some benefits to animals dispersing to new habitats for reproduction, which may lead to the acquisition of novel microbes in offspring. Such benefits could underlie the observed variability in the degree of site fidelity across individuals. Overall, more studies are needed to test ideas of our framework in a broad array of systems.

Future directions

With these research findings and caveats in mind, we propose a conceptual framework by which environmental acquisition of microbes and associated fitness benefits may contribute to the evolution of natal philopatry (Fig. 1). Here, individuals that exhibit philopatry return to their birthplace for reproduction, and thus their offspring acquire the optimal microbial communities during early life and exhibit improved performance and survival. Conversely, offspring of individuals that had dispersed for reproduction have a mismatch between host genetics and microbial genetics, and the environment. Such sub-optimal matching may result in decreased performance and fitness of offspring in these environments. Such fitness consequences may yield evolution in behavioral traits, such as natal homing, especially since natural selection is thought to act strongly on behavior [120], and behavioral traits are evolutionarily labile [121]. Through these processes, host-microbe interactions and the resulting fitness benefits could act as ultimate factors underlying the evolution of natal philopatry.

Fig. 1
figure 1

Diagrammatic representation of how host-microbe interactions may influence reproductive success of philopatric or dispersing individuals. Individuals that exhibit philopatry maintain optimal GenomeHost x GenomeMicrobial x Environment interactions. Conversely, individuals that disperse experience incompatibility in GenomeHost x GenomeMicrobial x Environment interactions, and suffer fitness consequences

Full size image

However, we again recognize that our framework is highly speculative. Future observational, comparative, and experimental work could help to address these ideas and large open questions that remain in this framework. First, a thorough understanding of the basic microbial ecology of animal systems that engage in natal philopatry is still lacking. Overall, microbiome research has been largely biased towards model systems and biomedical studies [122,123,124]. In many wild systems we still lack thorough knowledge on the routes of microbial acquisition, microbial sharing, and the effects of microbial communities on performance and fitness. Therefore, researchers should employ current techniques for inventorying the taxonomic composition and functions of microbial communities [125] and integrating these techniques with questions of integrative and comparative biology [125, 126]. Additionally, as mentioned above, we have poor understanding of the resolution of spatial heterogeneity in microbial communities, especially on scales relevant to animal ecology.

Another large question relates to the concept GenomeHost x GenomeMicrobial x Environment interactions, and which of these interactions are most important in determining performance and fitness. Classical work to test Genome x Environment interactions, such as common garden or transplant experiments, have largely conflated the aspects of GenomeHost and GenomeMicrobial. Additionally, existing work on GenomeHost x GenomeMicrobial interactions have largely ignored environmental variables, as they have been conducted in captivity under constant conditions [9, 68,69,70]. Thus, to our knowledge, full tests of GenomeHost x GenomeMicrobial x Environment interactions remain lacking. In the future, a combination of controlled microbial inoculations during early life followed by exposure to varying environments would benefit the framework presented in this article, as well as the greater field of host-microbe interactions.

We predict that manipulative experiments will provide powerful approaches to disentangle the effects of genetics, location, and the microbiome on breeding success. Some groups have used cross-fostering approaches in nestling birds to demonstrate that the local environment determines the membership of their gut microbiome [127]. Similar approaches could be taken in philopatric species. Additionally, controlled experimental studies in the laboratory could be useful. Several studies have manipulated environmental microbial communities in the lab to investigate their effects on animal performance [77, 128]. Similar approaches could be used with multiple environmental microbial sources. Following such microbial manipulations, researchers could release animals into experimental field sites and track performance and fitness. For example, researchers have used controlled environmental mesocosms to track the population dynamics of released lizards [129], voles [130], fish [131] and invertebrates [132]. Combining experimental microbial manipulations with mesocosm approaches will be a necessary next step in testing aspects of our conceptual framework.

Overall, it is becoming more and more clear that microbial partnerships influence many aspects of animal life-history and revealing a role for these partnerships in the enigmatic behavior of natal philopatry could have numerous implications. First, testing whether microbial interactions play a role in the evolution of natal philopatry will greatly enhance our understanding of hologenomic evolution [38], including the evolution of animal behavior [10] . Additionally, understanding the proximate and ultimate causes of natal philopatry has conservation implications to ensure successful breeding [13, 133]. Similarly, host-microbe interactions have the potential to influence conservation efforts [8], and thus understanding the role of microbes in early life success could help to shape and prioritize breeding sites and captive breeding efforts.

Conclusion

This article highlights the potential for host-microbe interactions to underly the evolution of natal philopatry. Numerous studies have demonstrated the importance of environmental microbes in colonizing animal hosts, and the effect of specific host-microbe associations on animal performance. Thus, we argue that the combination of these factors may lead animals to return to natal sites for breeding to ensure that their offspring acquire the optimal microbiome.

Availability of data and materials

Not applicable.

References

  1. Cava JA, Perlut NG, Travis SE. Why come back home? Investigating the proximate factors that influence natal philopatry in migratory passerines. Anim Behav. 2016;118:39–46. https://doi.org/10.1016/j.anbehav.2016.05.006.

    Article  Google Scholar 

  2. Hendrickson JR. The green sea turtle, Chelonia mydas (Linn.) in Malaya and Sarawak. Proc Zool Soc London. 1958;130:455–535.

    Article  Google Scholar 

  3. Forschler MI, Val ED, Bairlein F. Extraordinary high natal philopatry in a migratory passerine. J Ornithol. 2010;151(3):745–8. https://doi.org/10.1007/s10336-010-0495-y.

    Article  Google Scholar 

  4. Kristensen TN, Loeschcke V, Hoffmann AA. Linking inbreeding effects in captive populations with fitness in the wild: release of replicated Drosophila melanogaster lines under different temperatures. Conserv Biol. 2008;22(1):189–99. https://doi.org/10.1111/j.1523-1739.2007.00816.x.

    Article  PubMed  Google Scholar 

  5. Bensch S, Hasselquist D, Nielsen B, Hansson B. Higher fitness for philopatric than for immigrant males in a semi-isolated population of great reed warblers. Evolution. 1998;52(3):877–83. https://doi.org/10.1111/j.1558-5646.1998.tb03712.x.

    Article  PubMed  Google Scholar 

  6. Waite DW, Taylor MW. Characterizing the avian gut microbiota: membership, driving influences, and potential function. Front Microbiol. 2014;5:223.

    Article  PubMed  PubMed Central  Google Scholar 

  7. Kohl KD. Diversity and function of the avian gut microbiota. J Comp Physiol B. 2012;182(5):591–602. https://doi.org/10.1007/s00360-012-0645-z.

    Article  PubMed  Google Scholar 

  8. Trevelline BK, Fontaine SS, Hartup BK, Kohl KD. Conservation biology needs a microbial renaissance: a call for the consideration of host-associated microbiota in wildlife management practices. Proc R Soc B. 2019;286(1895):20182448. https://doi.org/10.1098/rspb.2018.2448.

    Article  PubMed  Google Scholar 

  9. Brooks AW, Kohl KD, Brucker RM, van Opstal EJ, Bordenstein SR. Phylosymbiosis: relationships and functional effects of microbial communities across host evolutionary history. PLoS Biol. 2016;14(11):e2000225. https://doi.org/10.1371/journal.pbio.2000225.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  10. Theis KR, Whittaker DJ, Rojas CA. In: Banzhaf W, BHC C, Deb K, Holekamp KE, Lenski RE, Ofria C, Pennock RT, Punch WF, Whittaker DJ, editors. A hologenomic approach to animal behavior. In: evolution in action: past, present and future: a festschrift in honor of Erik D Goodman. Cham: Springer International Publishing; 2020. p. 247–63.

    Google Scholar 

  11. Papi F. Navigation of marine, freshwater and coastal animals: concepts and current problems. Mar Freshw Behav Physiol. 2006;39(1):3–12. https://doi.org/10.1080/10236240600563057.

    Article  Google Scholar 

  12. Ehrenfeld DW, Carr A. The role of vision in the sea-finding orientation of the green turtle (Chelonia mydas). Anim Behav. 1967;15(1):25–36.

  13. Dolný A, Mižicova H, Harabis F. Natal philopatry in four European species of dragonflies (Odonata: Sympetrinae) and possible implications for conservation management. J Insect Conserv. 2013;17(4):821–9. https://doi.org/10.1007/s10841-013-9564-x.

    Article  Google Scholar 

  14. Weyer J, Schmitt T. Knowing the way home: strong philopatry of a highly mobile insect species. Brenthis ino J Insect Conserv. 2013;17(6):1197–208. https://doi.org/10.1007/s10841-013-9601-9.

    Article  Google Scholar 

  15. Keefer ML, Caudill CC. Homing and straying by anadromous salmonids: a review of mechanisms and rates. Rev Fish Biol Fish. 2014;24(1):333–68. https://doi.org/10.1007/s11160-013-9334-6.

    Article  Google Scholar 

  16. Thorrold SR, Latkoczy C, Swart PK, Jones CM. Natal homing in a marine fish metapopulation. Science. 2001;291(5502):297–9. https://doi.org/10.1126/science.291.5502.297.

    Article  CAS  PubMed  Google Scholar 

  17. Hueter RE, Heupel MR. Evidence of philopatry in sharks and implications for the management of shark fisheries. J Northwest Atl Fish Sci. 2004;35:239–47. https://doi.org/10.2960/J.v35.m493.

    Article  Google Scholar 

  18. Gamble LR, Mcgarigal K, Compton BW. Fidelity and dispersal in the pond-breeding amphibian, Ambystoma opacum: implications for spatio-temporal population dynamics and conservation. Biol Conserv. 2007;139(3):247–57. https://doi.org/10.1016/j.biocon.2007.07.001.

    Article  Google Scholar 

  19. Berven KA, Grudzien TA. Dispersal in the wood frog (Rana Sylvatica): implications for genetic population structure. Evolution. 1990;44(8):2047–56.

    PubMed  Google Scholar 

  20. Breden F. The effect of post-metamorphic dispersal on the population genetic structure of Fowler's toad, Bufo woodhousei fowleri. Copeia. 1987;1987(2):386–95. https://doi.org/10.2307/1445775.

    Article  Google Scholar 

  21. Reading CJ, Loman J, Madsen T. Breeding pond fidelity in the common toad, Bufo bufo. J Zool. 1991;225(2):201–11.

    Article  Google Scholar 

  22. Fitzsimmons NN, Limpus CJ, Norman JA, Goldizen AR, Miller JD, Moritz C. Philopatry of male marine turtles inferred from mitochondrial DNA markers. PNAS. 1997;94(16):8912–7. https://doi.org/10.1073/pnas.94.16.8912.

    Article  CAS  PubMed  Google Scholar 

  23. Lee PLM, Luschi P, Hays GC. Detecting female precise natal philopatry in green turtles using assignment methods. Mol Ecol. 2006;16(1):61–74. https://doi.org/10.1111/j.1365-294X.2006.03115.x.

    Article  CAS  Google Scholar 

  24. Burger J, Zappalorti R. Philopatry and nesting phenology of pine snakes Pituophis melanoleucus in the New Jersey pine barrens. Behav Ecol Sociobiol. 1992;30(5):331–6.

    Article  Google Scholar 

  25. Hansson B, Bensch S, Hasselquist D, Nielsen B. Restricted dispersal in a long-distance migrant bird with patchy distribution, the great reed warbler. Oecologia. 2002;130(4):536–42. https://doi.org/10.1007/s00442-001-0831-2.

    Article  PubMed  Google Scholar 

  26. Gauthier G, Milot E, Weimerskirch H. Small-scale dispersal and survival in a long-lived seabird, the wandering albatross. J Anim Ecol. 2010;79(4):879–87.

    PubMed  Google Scholar 

  27. Mchugh K, Allen J, Barleycorn AAA, Wells RS. Natal philopatry, ranging behavior, and habitat selection of juvenile bottlenose dolphins in Sarasota Bay. Florida J Mammal. 2011;92(6):1298–313. https://doi.org/10.1644/11-MAMM-A-026.1.

    Article  Google Scholar 

  28. Burland T, Barratt E, Nichols R, Racey PA. Mating patterns, relatedness and the basis of natal philopatry in the brown long-eared bat, Plecotus auritus. Mol Ecol. 2001;10(5):1309–21. https://doi.org/10.1046/j.1365-294X.2001.01273.x.

    Article  CAS  PubMed  Google Scholar 

  29. Hoffman JI, Forcada J. Extreme natal philopatry in female Antarctic fur seals (Arctocephalus gazella). Mamm Biol. 2012;77(1):71–3. https://doi.org/10.1016/j.mambio.2011.09.002.

    Article  Google Scholar 

  30. Waser PM, Jones WT. Natal philopatry among solitary mammals. Q Rev Biol. 1983;58(3):355–90. https://doi.org/10.1086/413385.

    Article  Google Scholar 

  31. Coulson JC. A review of philopatry in seabirds and comparisons with other waterbird species. Waterbirds. 1938;39(3):229–40.

    Article  Google Scholar 

  32. Weatherhead PJ, Forbes MRL. Natal philopatry in passerine birds: genetic or ecological influences? Behav Ecol. 1994;4:426–33.

    Article  Google Scholar 

  33. Mcfall-Ngai M, Hadfield MG, Bosch TCG, Carey HV, Domazet-loso T, Douglas AE, et al. Animals in a bacterial world, a new imperative for the life sciences. PNAS. 2013;110(9):3229–36. https://doi.org/10.1073/pnas.1218525110.

    Article  PubMed  Google Scholar 

  34. Cummings JH, Macfarlane GT. Role of intestinal bacteria in nutrient metabolism. Clin Nutr. 1997;16(1):3–11. https://doi.org/10.1016/S0261-5614(97)80252-X.

    Article  Google Scholar 

  35. Fukuda S, Toh H, Hase K, Oshima K, Nakanishi Y, Yoshimura K, et al. Bifidobacteria can protect from enteropathogenic infection through production of acetate. Nature. 2011;469(7331):543–7. https://doi.org/10.1038/nature09646.

    Article  CAS  PubMed  Google Scholar 

  36. Round JL, Mazmanian SK. The gut microbiota shapes intestinal immune responses during health and disease. Nat Rev Immunol. 2009;9(5):313–23. https://doi.org/10.1038/nri2515.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  37. Sisonmangus MP, Mushegian AA, Ebert D. Water fleas require microbiota for survival, growth and reproduction. ISME J. 2015;9(1):59–67. https://doi.org/10.1038/ismej.2014.116.

    Article  Google Scholar 

  38. Bordenstein SR, Theis KR. Host biology in light of the microbiome: ten principles of holobionts and hologenomes. PLoS Biol. 2015;13(8):e1002226.

  39. Zilber-Rosenberg I, Rosenberg E. Role of microorganisms in the evolution of animals and plants: the hologenome theory of evolution. FEMS Microbiol Rev. 2008;32(5):723–35. https://doi.org/10.1111/j.1574-6976.2008.00123.x.

    Article  CAS  PubMed  Google Scholar 

  40. Owens DW, Grassman MA, Hendrickson JR. The imprinting hypotheses and sea turtle reproduction. Herpetolog- ica. 1982;36:17–20.

    Google Scholar 

  41. Nordeng H. A pheromone hypothesis for homeward migration in anadromous salmonids. Oikos. 1977;28(2/3):155–9. https://doi.org/10.2307/3543965.

    Article  CAS  Google Scholar 

  42. Meylan AB, Bowen BW, Avise JC. A genetic test of the natal homing versus social facilitation models for green turtle migration. Science. 1990;248(4956):724–7. https://doi.org/10.1126/science.2333522.

    Article  CAS  PubMed  Google Scholar 

  43. Lohmann KJ. Evidence for geomagnetic imprinting and magnetic navigation in the natal homing of sea turtles. Curr Biol. 2015;25(3):392–6.

    Article  PubMed  Google Scholar 

  44. Dittman AH, Quinn TP. Homing in pacific salmon: mechanisms and ecological basis. J Exp Biol. 1996;199(1):83–91.

    CAS  PubMed  Google Scholar 

  45. Greenwood PJ, Harvey PH. The natal and breeding dispersal of birds. Annu Rev Ecol Syst. 1982;13(1):1–21. https://doi.org/10.1146/annurev.es.13.110182.000245.

    Article  Google Scholar 

  46. Newton I. The migration ecology of birds. London: Academic; 2008.

    Google Scholar 

  47. Part T. Philopatry pays: a comparison between collared flycatcher sisters. Am Nat. 1991;138(3):790–6. https://doi.org/10.1086/285252.

    Article  Google Scholar 

  48. Nichols HJ, Cant MA, Hoffman JI, Sanderson J. Evidence for frequent incest in a cooperatively breeding mammal. Biol Lett. 2014;10(12):20140898. https://doi.org/10.1098/rsbl.2014.0898.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  49. Rueger T, Harrison HB, Buston PM, Gardiner NM, Berumen ML, Jones GP. Natal philopatry increases relatedness within groups of coral reef cardinalfish. Proc R Soc B. 2020;287(1930):20201133.

  50. Shields WM. Philopatry, inbreeding, and the evolution of sex: Suny Press; 1982.

  51. Taylor JM, Mcphail JD. Burst swimming and size-related predation of newly emerged coho salmon Oncorhynchus kisutch trans. Am Fish Soc. 1985;114(4):546–51. https://doi.org/10.1577/1548-8659(1985)114<546:BSASPO>2.0.CO;2.

    Article  Google Scholar 

  52. Tigano A, Friesen VL. Genomics of local adaptation with gene flow. Mol Ecol. 2016;25(10):2144–64. https://doi.org/10.1111/mec.13606.

    Article  PubMed  Google Scholar 

  53. Akerman A, Bürger R. The consequences of gene flow for local adaptation and differentiation: a two-locus two-deme model. J Math Biol. 2014;68(5):1135–98. https://doi.org/10.1007/s00285-013-0660-z.

    Article  PubMed  Google Scholar 

  54. Burger J, Zappalorti RT. Philopatry and nesting phenology of pine snakes Pituophis melanoleucus in the New Jersey pine barrens. Behav Ecol Sociobiol. 1992;30(5):331–6.

    Article  Google Scholar 

  55. Mcnab BK. Ecology of bats. New York: Plenum Press; 1982.

    Google Scholar 

  56. Jones WT. Natal philopatry in bannertailed kangaroo rats. Behav Ecol Sociobiol. 1984;15(2):151–5. https://doi.org/10.1007/BF00299383.

    Article  Google Scholar 

  57. Forcada J, Trathan PN, Murphy EJ. Life history buffering in Antarctic mammals and birds against changing patterns of climate and environmental variation. Glob Chang Biol. 2008;14(11):2473–88. https://doi.org/10.1111/j.1365-2486.2008.01678.x.

    Article  Google Scholar 

  58. Forstmeier W. Benefits of early arrival at breeding grounds vary between males. J Anim Ecol. 2002;71(1):1–9. https://doi.org/10.1046/j.0021-8790.2001.00569.x.

    Article  Google Scholar 

  59. Beletsky LD, Orians GH. Familiar neighbours enhance breeding success in birds. Proc Natl Acad Sci. 1989;86(20):7933–6. https://doi.org/10.1073/pnas.86.20.7933.

    Article  CAS  PubMed  Google Scholar 

  60. Tsai YJ, Mann J. Dispersal, philopatry, and the role of fission-fusion dynamics in bottlenose dolphins. Mar Mamm Sci. 2013;29(2):261–79. https://doi.org/10.1111/j.1748-7692.2011.00559.x.

    Article  Google Scholar 

  61. Wiltschko R, Wiltschko W. Magnetoreception in birds. J R Soc Interface. 2019;16(158):20190295. https://doi.org/10.1098/rsif.2019.0295.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  62. Natan E, Fitak RR, Werber Y, Vortman Y. Symbiotic magnetic sensing: raising evidence and beyond. Philos T R Soc B. 2020;375(1808):20190595. https://doi.org/10.1098/rstb.2019.0595.

    Article  CAS  Google Scholar 

  63. Kristin SB, Martín-Sánchez L, Paolina G. Microbial volatiles: small molecules with an important role in intra- and inter-kingdom interactions. Front Microbiol. 2017;8:2484.

    Article  Google Scholar 

  64. Theis KR, Venkataraman A, Dycus JA, Koonter KD, Schmitt-Matzen EN, Wagner AP, Holekamp KE, Schmidt TM. Symbiotic bacteria appear to mediate hyena social odors. Proc Natl Acad Sci. 2013;110(49):19832–7.

  65. Whittaker DJ, Slowinski SP, Greenberg JM, Alian OM. Experimental evidence that symbiotic bacteria produce chemical cues in a songbird. J Exp Biol. 2019;222(20):jeb.202978.

    Article  Google Scholar 

  66. Becher PG, Verschut V, Bibb MJ, Bush MJ, Molnar BP, Barane E, et al. Developmentally regulated volatiles geosmin and 2-methylisoborneol attract a soil arthropod to Streptomyces bacteria promoting spore dispersal. Nat Microbiol. 2020;5(6):821–9. https://doi.org/10.1038/s41564-020-0697-x.

    Article  CAS  PubMed  Google Scholar 

  67. Gould AL, Zhang V, Lamberti L, Jones EW, Obadia B, Korasidis N, et al. Microbiome interactions shape host fitness. PNAS. 2018;115(51):11951–60.

    Article  Google Scholar 

  68. Adair KL, Bost A, Bueno E, Kaunisto S, Kortet R, Peters-Schulze G, et al. Host determinants of among-species variation in microbiome composition in drosophilid flies. ISME J. 2020;14(1):217–29. https://doi.org/10.1038/s41396-019-0532-7.

    Article  PubMed  Google Scholar 

  69. Berg M, Zhou XY, Shapira M. Host-specific functional significance of Caenorhabditis gut commensals. Front Microbiol. 2016;7:1622.

    Article  PubMed  PubMed Central  Google Scholar 

  70. van Opstal EJ, Bordenstein SR. Phylosymbiosis impacts adaptive traits in Nasonia wasps. mBio. 2019;10(4):e00887–19.

    PubMed  PubMed Central  Google Scholar 

  71. Brucker RM, Bordenstein SR. The hologenomic basis of speciation: gut bacteria cause hybrid lethality in the genus Nasonia. Science. 2013;341(6146):667–9. https://doi.org/10.1126/science.1240659.

    Article  CAS  PubMed  Google Scholar 

  72. Wang J, Kalyan S, Steck N, Turner LM, Harr B, Kunzel S, et al. Analysis of intestinal microbiota in hybrid house mice reveals evolutionary divergence in a vertebrate hologenome. Nat Commun. 2015;6(1):6440. https://doi.org/10.1038/ncomms7440.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  73. Carrier TJ, Reitzel AM. The hologenome across environments and the implications of a host-associated microbial repertoire. Front Microbiol. 2017;8:802.

  74. Tamburini S, Shen N, Wu HC, Clemente JC. The microbiome in early life: implications for health outcomes. Nat Med. 2016;22(7):713–22. https://doi.org/10.1038/nm.4142.

    Article  CAS  PubMed  Google Scholar 

  75. Cox LM, Yamanishi S, Sohn J, Alekseyenko AV, Leung JM, Cho I, et al. Altering the intestinal microbiota during a critical developmental window has lasting metabolic consequences. Cell. 2014;158(4):705–21. https://doi.org/10.1016/j.cell.2014.05.052.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  76. Phelps D, Brinkman NE, Keely SP, Anneken EM, Catron TR, Betancourt D, et al. Microbial colonization is required for normal neurobehavioral development in zebrafish. Sci Rep. 2017;7(1):1–13.

    Article  CAS  Google Scholar 

  77. Knutie SA, Wilkinson CL, Kohl KD, Rohr JR. Early-life disruption of amphibian microbiota decreases later-life resistance to parasites. Nat Commun. 2017;8(1):1–8.

    Article  CAS  Google Scholar 

  78. Warne RW, Kirschman LJ, Zeglin LH. Manipulation of gut microbiota during critical developmental windows affects host physiological performance and disease susceptibility across ontogeny. J Anim Ecol. 2019;88(6):845–56. https://doi.org/10.1111/1365-2656.12973.

    Article  PubMed  Google Scholar 

  79. Martinez I, Maldonadogomez MX, Gomesneto JC, Kittana H, Ding H, Schmaltz R, et al. Experimental evaluation of the importance of colonization history in early-life gut microbiota assembly. eLife. 2018;7. https://doi.org/10.7554/eLife.36521.

  80. Funkhouser LJ, Bordenstein SR. Mom knows best: the universality of maternal microbial transmission. PLoS Biol. 2013;11(8):e1001631.

  81. Dominguez-Bello MG, Costello EK, Contreras M, Magris M, Hidalgo G, Fierer N, et al. Delivery mode shapes the acquisition and structure of the initial microbiota across multiple body habitats in newborns. PNAS. 2010;107(26):11971–5. https://doi.org/10.1073/pnas.1002601107.

    Article  PubMed  Google Scholar 

  82. Kikuchi Y, Hosokawa T, Fukatsu T. Insect-microbe mutualism without vertical transmission: a stinkbug acquires a beneficial gut symbiont from the environment every generation. Appl Environ Microbiol. 2007;73(13):4308–16. https://doi.org/10.1128/AEM.00067-07.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  83. Nyholm SV, Mcfallngai MJ. The winnowing: establishing the squid– vibrio symbiosis. Nat Rev Microbiol. 2004;2(8):632–42. https://doi.org/10.1038/nrmicro957.

    Article  CAS  PubMed  Google Scholar 

  84. Correa DT, Rodriguez D, Emer C, Saenz D, Adams CK, Schiesari L, Matz M, Leibold MA. Multilevel community assembly of the tadpole gut. bioRxiv. 2020. https://doi.org/10.1101/2020.07.05.188698.

  85. Shangong W, Esther RA, Wang W, Li W, Zou H. Composition, diversity, and origin of the bacterial community in grass carp intestine. PLoS One. 2012;7(2):e30440.

    Article  Google Scholar 

  86. Wong S, Stephens WZ, Burns AR, Stagaman K, David LA, Bohannan BJM, et al. Ontogenetic differences in dietary fat influence microbiota assembly in the zebrafish gut. Mbio. 2015;6(5):e00687–15.

  87. Campos-Cerda F, Bohannan BJ. The Nidobiome: a framework for understanding microbiome assembly in neonates. Trends Ecol Evol. 2020;35(7):573–82. https://doi.org/10.1016/j.tree.2020.03.007.

    Article  PubMed  Google Scholar 

  88. Ruiz-Rodríguez M, Martín-Vivaldi M, Martínez-Bueno M, Soler JJ. Gut microbiota of great spotted cuckoo nestlings is a mixture of those of their foster magpie siblings and of cuckoo adults. Genes. 2018;9(8):381. https://doi.org/10.3390/genes9080381.

    Article  CAS  PubMed Central  Google Scholar 

  89. Snijders AM, Langley SA, Kim YM, Brislawn CJ, Noecker C, Zink EM, et al. Influence of early life exposure, host genetics and diet on the mouse gut microbiome and metabolome. Nat Microbiol. 2017;2(2):16221. https://doi.org/10.1038/nmicrobiol.2016.221.

    Article  CAS  Google Scholar 

  90. Schmidt E, Mykytczuk NCS, Schultehostedde AI. Effects of the captive and wild environment on diversity of the gut microbiome of deer mice (Peromyscus maniculatus). ISME J. 2019;13(5):1293–305. https://doi.org/10.1038/s41396-019-0345-8.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  91. Beijerinck MJM, Amsterdam. De infusies en de ontdekking der backteriën. Jaarboek van de Koninklijke Akademie voor Wetenschappen. 1913.

  92. Hellweger FL, van Sebille E, Fredrick ND. Biogeographic patterns in ocean microbes emerge in a neutral agent-based model. Science. 2014;345(6202):1346–9. https://doi.org/10.1126/science.1254421.

    Article  CAS  PubMed  Google Scholar 

  93. Fierer N, Jackson RB. The diversity and biogeography of soil bacterial communities. PNAS. 2006;103(3):626–31. https://doi.org/10.1073/pnas.0507535103.

    Article  CAS  PubMed  Google Scholar 

  94. Moeller AH, Suzuki TA, Lin D, Lacey EA, Wasser SK, Nachman MW. Dispersal limitation promotes the diversification of the mammalian gut microbiota. PNAS. 2017;114(52):13768–73. https://doi.org/10.1073/pnas.1700122114.

    Article  CAS  PubMed  Google Scholar 

  95. Weldon L, Abolins S, Lenzi L, Bourne C, Riley EM, Viney MJ. The gut microbiota of wild mice. PLoS One. 2015;10(8):e0134643.

  96. Moeller AH, Ndjango JB, Li Y, Hahn BH, Ochman H. Sympatric chimpanzees andgorillas harbor convergent gut microbial communities. Genome Res. 2013;23(10):1715–20. https://doi.org/10.1101/gr.154773.113.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  97. Gillingham MAF, Béchet A, Cézilly F, Wilhelm K, Rendón-Martos M, Borghesi F, et al. Offspring microbiomes differ across breeding sites in a panmictic species. Front Microbiol. 2019;10:35. https://doi.org/10.3389/fmicb.2019.00035.

    Article  PubMed  PubMed Central  Google Scholar 

  98. Garcia-Pichel F, Loza V, Marusenko Y, Mateo P, Potrafka RM. Temperature drives the continental-scale distribution of key microbes in topsoil communities. Science. 2013;340(6140):1574–157. https://doi.org/10.1126/science.1236404.

    Article  CAS  PubMed  Google Scholar 

  99. Nottingham AT, Noah F, Turner BL, Whitaker J, Ostle NJ, McNamara NP, et al. Microbes follow Humboldt: temperature drives plant and soil microbial diversity patterns from the Amazon to the Andes. Ecology. 2018;99(11):2455–66. https://doi.org/10.1002/ecy.2482.

    Article  PubMed  PubMed Central  Google Scholar 

  100. Moeller AH, Ivey K, Cornwall MB, Herr K, Rede J, Taylor EN, et al. Lizard gut microbiome changes with temperature and is associated with heat tolerance. Appl Environ Microbiol. 2020;86(17):e01181–20.

  101. Suzuki TA, Martins FM, Phiferixey M, Nachman MW. The gut microbiota and Bergmann's rule in wild house mice. Mol Ecol. 2020;29(12):2300–11.

  102. Kreisinger J, Kropackova L, Petrželkova A, Adamkova MK, Tomasek O, Martin J, et al. Temporal stability and the effect of transgenerational transfer on fecal microbiota structure in a long distance migratory bird. Front Microbiol. 2017;8. https://doi.org/10.3389/fmicb.2017.00050.

  103. Archie EA, Tung J. Social behavior and the microbiome. Curr Opin Behav Sci. 2015;6:28–34. https://doi.org/10.1016/j.cobeha.2015.07.008.

    Article  Google Scholar 

  104. Korner M, Diehl JMC, Meunier J. Growing up with feces: benefits of Allo-coprophagy in families of the European earwig. Behav Ecol. 2016;27(6):1775–81.

    Google Scholar 

  105. Troyer K. Behavioral acquisition of the hindgut fermentation system by hatchling Iguana iguana. Behav Ecol Sociobiol. 1984;14(3):189–93. https://doi.org/10.1007/BF00299618.

    Article  Google Scholar 

  106. Vicenzi N. Phymaturus palluma (high mountain lizard) coprophagy. Herpetol Rev. 2015;46:93.

    Google Scholar 

  107. Kobayashi A, Tsuchida S, Ueda A, Yamada T, Murata K, Nakamura H, et al. Role of coprophagy in the cecal microbiome development of an herbivorous bird Japanese rock ptarmigan. J Vet Med Sci. 2019;81(9):1389–99. https://doi.org/10.1292/jvms.19-0014.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  108. Crowelldavis SL, Houpt KA. Coprophagy by foals: effect of age and possible functions. Equine Vet J. 1985;17(1):17–9. https://doi.org/10.1111/j.2042-3306.1985.tb02030.x.

    Article  CAS  Google Scholar 

  109. Osawa R, Blanshard W, Ocallaghan P. Microbiological studies of the intestinal microflora of the koala, phascolarctos-cinereus. 2. Pap, a special maternal feces consumed by juvenile koalas. Aust J Zool. 1993;41(6):611–20. https://doi.org/10.1071/ZO9930611.

    Article  Google Scholar 

  110. Jahnes BC, Herrmann M, Sabree ZL. Conspecific coprophagy stimulates normal development in a germ-free model invertebrate. PeerJ. 2019;7:e6914. https://doi.org/10.7717/peerj.6914.

    Article  PubMed  PubMed Central  Google Scholar 

  111. Troyer K. Transfer of fermentative microbes between generations in a herbivorous lizard. Science. 1982;216(4545):540–2. https://doi.org/10.1126/science.216.4545.540.

    Article  CAS  PubMed  Google Scholar 

  112. Koch H, Schmidhempel P. Socially transmitted gut microbiota protect bumble bees against an intestinal parasite. PNAS. 2011;108(48):19288–92. https://doi.org/10.1073/pnas.1110474108.

    Article  PubMed  Google Scholar 

  113. Onchuru TO, Martinez AJ, Ingham CS, Kaltenpoth M. Transmission of mutualistic bacteria in social and gregarious insects. Curr Opin Insect Sci. 2018;28:50–8. https://doi.org/10.1016/j.cois.2018.05.002.

    Article  PubMed  Google Scholar 

  114. Salem H, Florez LV, Gerardo NM, Kaltenpoth M. An out-of-body experience: the extracellular dimension for the transmission of mutualistic bacteria in insects. Proc R Soc B. 2015;282(1804):29572957.

    Article  Google Scholar 

  115. Tung J, Barreiro LB, Burns MB, Grenier JC, Lynch J, Grieneisen LE, et al. Social networks predict gut microbiome composition in wild baboons. eLife. 2015;4(4):e05224.

  116. Grieneisen LE, Livermore J, Alberts SC, Tung J, Archie EA. Group living and male dispersal predict the core gut microbiome in wild baboons. Integr Comp Biol. 2017;57(4):770–85. https://doi.org/10.1093/icb/icx046.

    Article  PubMed  PubMed Central  Google Scholar 

  117. Antwis RE, Lea JMD, Unwin B, Shultz S. Gut microbiome composition is associated with spatial structuring and social interactions in semi-feral Welsh Mountain ponies. Microbiome. 2018;6(1):1–11.

    Article  Google Scholar 

  118. Spear LB, Pyle P, Nur N. Natal dispersal in the western gull: proximal factors and fitness consequences. J Anim Ecol. 1998;67(2):165–79. https://doi.org/10.1046/j.1365-2656.1998.00190.x.

    Article  Google Scholar 

  119. Alberdi A, Aizpurua O, Bohmann K, Zepeda-Mendoza ML, Gilbert M. Do vertebrate gut metagenomes confer rapid ecological adaptation? Trends Ecol Evol. 2016;31(9):689–99. https://doi.org/10.1016/j.tree.2016.06.008.

    Article  PubMed  Google Scholar 

  120. Boulding EG. Experimental evolution. Concepts, methods, and applications of selection experiments. Theodore Garland Jr and Michael R. rose, editors. Integr Comp Biol. 2010;50(5):909–10. https://doi.org/10.1093/icb/icq093.

    Article  Google Scholar 

  121. Blomberg SP, Garland JR, Ives AR. Testing for phylogenetic signal in comparative data: behavioral traits are more labile. Evolution. 2003;57(4):717–45. https://doi.org/10.1111/j.0014-3820.2003.tb00285.x.

    Article  PubMed  Google Scholar 

  122. Colston TJ, Jackson CR. Microbiome evolution along divergent branches of the vertebrate tree of life: what is known and unknown. Mol Ecol. 2016;25(16):3776–800. https://doi.org/10.1111/mec.13730.

    Article  PubMed  Google Scholar 

  123. Greysongaito CJ, Bartley TJ, Cottenie K, Jarvis WMC, Newman AEM, Stothart MR. Into the wild: microbiome transplant studies need broader ecological reality. Proc R Soc B. 2020;287(1921):2834.

    Google Scholar 

  124. Pascoe EL, Hauffe HC, Marchesi JR, Perkins SE. Network analysis of gut microbiota literature: an overview of the research landscape in non-human animal studies. ISME J. 2017;11(12):2644–51. https://doi.org/10.1038/ismej.2017.133.

    Article  PubMed  PubMed Central  Google Scholar 

  125. Liu YX, Qin Y, Chen T, Lu M, Qian X, Guo X, et al. A practical guide to amplicon and metagenomic analysis of microbiome data. Protein Cell. 2020:1–16. https://doi.org/10.1007/s13238-020-00724-8.

  126. Kohl KD. An introductory "how-to" guide for incorporating microbiome research into integrative and comparative biology. Integr Comp Biol. 2017;57(4):674–81. https://doi.org/10.1093/icb/icx013.

    Article  PubMed  Google Scholar 

  127. Teyssier A, Lens L, Matthysen E, White J. Dynamics of gut microbiota diversity during the early development of an avian host: evidence from a cross-foster experiment. Front Microbiol. 2018;9. https://doi.org/10.3389/fmicb.2018.01524.

  128. van Veelen HJ, Salles JF, Matson KD, van der Velde M, Tieleman BI. Microbial environment shapes immune function and cloacal microbiota dynamics in zebra finches Taeniopygia guttata. Anim Microbio. 2020;2(1):21. https://doi.org/10.1186/s42523-020-00039-3.

    Article  Google Scholar 

  129. Bestion E, Jacob S, Zinger L, Gesu LD, Richard M, White JL, et al. Climate warming reduces gut microbiota diversity in a vertebrate ectotherm. Nat Ecol Evol. 2017;1(6):0161. https://doi.org/10.1038/s41559-017-0161.

    Article  Google Scholar 

  130. Forbes KM, Henttonen H, Hirvelakoski V, Kipar A, Mappes T, Stuart P, et al. Food provisioning alters infection dynamics in populations of a wild rodent. Proc R Soc B. 2015;282(1816):1939.

    Article  Google Scholar 

  131. Keller AA, Kleinmacphee G. Impact of elevated temperature on the growth, survival, and trophic dynamics of winter flounder larvae: a mesocosm study. Can J Fish Aquat Sci. 2000;57(12):2382–92. https://doi.org/10.1139/f00-217.

    Article  Google Scholar 

  132. Wieczorek MV, Bakanov N, Bilancia D, Szocs E, Stehle S, Bundschuh M, et al. Structural and functional effects of a short-term pyrethroid pulse exposure on invertebrates in outdoor stream mesocosms. Sci Total Environ. 2018;610-611:810–9. https://doi.org/10.1016/j.scitotenv.2017.08.048.

    Article  CAS  PubMed  Google Scholar 

  133. Kruk M, Noordervliet MAW, Keurs WJT. Natal philopatry in the black-tailed godwit Limosa limosa L. and its possible implications for conservation. Ringing Migr. 1998;19(1):13–6. https://doi.org/10.1080/03078698.1998.9674156.

    Article  Google Scholar 

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Acknowledgements

We are grateful to Dr. Nick Barts and two anonymous reviewers for providing feedback that helped to improve this paper.

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This paper was supported by University of Pittsburgh Start-up funds to K.D.K.

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  1. State Key Laboratory of Integrated Management of Pest Insects and Rodents, Institute of Zoology, Chinese Academy of Sciences, Beijing, 100101, China

    Ting-bei Bo

  2. CAS Center for Excellence in Biotic Interactions, University of Chinese Academy of Sciences, Beijing, 100049, China

    Ting-bei Bo

  3. Department of Biological Sciences, University of Pittsburgh, Pittsburgh, PA, USA

    Ting-bei Bo & Kevin D. Kohl

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Bo, Tb., Kohl, K.D. Stabilization and optimization of host-microbe-environment interactions as a potential reason for the behavior of natal philopatry. anim microbiome 3, 26 (2021). https://doi.org/10.1186/s42523-021-00087-3

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Animal Microbiome

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