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

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.