Molecular Adaptation to Folivory and the Conservation Implications for Madagascar’s Lemurs

The lemurs of Madagascar include numerous species characterized by folivory across several families. Many extant lemuriform folivores exist in sympatry in Madagascar’s remaining forests. These species avoid feeding competition by adopting different dietary strategies within folivory, reflected in behavioral, morphological, and microbiota diversity across species. These conditions make lemurs an ideal study system for understanding adaptation to leaf-eating. Most folivorous lemurs are also highly endangered. The significance of folivory for conservation outlook is complex. Though generalist folivores may be relatively well equipped to survive habitat disturbance, specialist folivores occupying narrow dietary niches may be less resilient. Characterizing the genetic bases of adaptation to folivory across species and lineages can provide insights into their differential physiology and potential to resist habitat change. We recently reported accelerated genetic change in RNASE1, a gene encoding an enzyme (RNase 1) involved in molecular adaptation in mammalian folivores, including various monkeys and sifakas (genus Propithecus; family Indriidae). Here, we sought to assess whether other lemurs, including phylogenetically and ecologically diverse folivores, might show parallel adaptive change in RNASE1 that could underlie a capacity for efficient folivory. We characterized RNASE1in 21 lemur species representing all five families and members of the three extant folivorous lineages: (1) bamboo lemurs (family Lemuridae), (2) sportive lemurs (family Lepilemuridae), and (3) indriids (family Indriidae). We found pervasive sequence change in RNASE1 across all indriids, a dN/dS value \u3e 3 in this clade, and evidence for shared change in isoelectric point, indicating altered enzymatic function. Sportive and bamboo lemurs, in contrast, showed more modest sequence change. The greater change in indriids may reflect a shared strategy emphasizing complex gut morphology and microbiota to facilitate folivory. This case study illustrates how genetic analysis may reveal differences in functional traits that could influence species’ ecology and, in turn, their resilience to habitat change. Moreover, our results support the body of work demonstrating that not all primate folivores are built the same and reiterate the need to avoid generalizations about dietary guild in considering conservation outlook, particularly in lemurs where such diversity in folivory has probably led to extensive specialization via niche partitioning

A role for gut microbiota in host niche differentiation

If gut microbes influence host behavioral ecology in the short term, over evolutionary time, they could drive host niche differentiation. We explored this possibility by comparing the gut microbiota of Madagascar's folivorous lemurs from Indriidae and Lepilemuridae. Occurring sympatrically in the eastern rainforest, our four, target species have different dietary specializations, including frugo-folivory (sifakas), young-leaf folivory (indri and woolly lemurs), and mature-leaf folivory (sportive lemurs). We collected fecal samples, from 2013 to 2017, and used amplicon sequencing, metagenomic sequencing, and nuclear magnetic resonance spectroscopy, respectively, to integrate analyses of gut microbiome structure and function with analysis of the colonic metabolome. The lemurs harbored species-specific microbiomes, metagenomes, and metabolomes that were tuned to their dietary specializations: Frugo-folivores had greater microbial and metagenomic diversity, and harbored generalist taxa. Mature-leaf folivores had greater individual microbiome variation, and taxa and metabolites putatively involved in cellulolysis. The consortia even differed between related, young-leaf specialists, with indri prioritizing metabolism of fiber and plant secondary compounds, and woolly lemurs prioritizing amino-acid cycling. Specialized gut microbiota and associated gastrointestinal morphologies enable folivores to variably tolerate resource fluctuation and support nutrient extraction from challenging resources (e.g., by metabolizing plant secondary compounds or recalcitrant fibers), perhaps ultimately facilitating host species' diversity and specialized feeding ecologies