The Ecology and Evolution of the Folivore Gut Microbiome in Madagascar’s Lemurs

Abstract

The gut microbiome (GMB) of folivores promotes host nutrition via metabolizing recalcitrant plant fibers into nutrients and degrading plant secondary compounds. A current aim within GMB research is to determine the evolutionary and ecological mechanisms that regulate the folivore GMB, which could be profitably addressed using comparative approaches and a broader representation of host systems. The lemurs of Madagascar, a phylogenetically and ecologically diverse primate group, include 45 folivorous species that vary in their evolutionary relationships, dietary niches, and habitat occupation. From 2013-2018, I and my collaborators collected 449 fecal samples from 325 wild and captive lemurs, representing four phylogenetic families, eight genera, and 21 species, various environmental and dietary conditions, and diverse feeding strategies ranging from folivory to frugivory. In each data chapter, I used subsets of samples and applied the comparative approach across analytical scales to probe GMB structure and function, determined via amplicon and metagenomic sequencing, and spectroscopy analysis. In my first data chapter, I compared GMBs across folivorous sifakas (Propithecus spp.) and frugivorous brown lemurs (Eulemur spp.). These lineages diverged over similar evolutionary time and live sympatrically in Madagascar’s rainforests and dry forests. Next, I compared GMBs across sympatric species of sifaka (P. diadema), indri (Indri indri), woolly lemur (Avahi laniger) and sportive lemur (Lepilemur mustelinus) that occupy different folivorous niches. I then focused on a captive population of sifakas (P. coquereli) and used manipulations of diet and housing condition to probe how foliage quality influences the folivore GMB across narrow timescales. In my final data chapter, I used three mini-studies to further underscore the importance of host phylogenetic and environmental scale in comparative microbiome research. My results reveal that the GMBs of folivorous lemurs are strikingly species and genus specific, are shaped by host evolutionary history over deeper timescales, but by habitat occupation over shallower timescales, and are finely tuned to available dietary resources. Ultimately, I suggest that within the constraints imposed by host phylogeny, feeding strategy can underlie the strength of host-microbiome coevolution. For folivores, a fundamental reliance on microbial metabolism to solve nutritional challenges has seemingly driven adaptation for hosts and microbiomes alike.