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

Abstract

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 RNASE1 in 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 > 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.

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Published Version (Please cite this version)

10.3389/fevo.2021.736741

Publication Info

Guevara, EE, LK Greene, MB Blanco, C Farmer, J Ranaivonasy, J Ratsirarson, KL Mahefarisoa, T Rajaonarivelo, et al. (2021). Molecular Adaptation to Folivory and the Conservation Implications for Madagascar’s Lemurs. Frontiers in Ecology and Evolution, 9. 10.3389/fevo.2021.736741 Retrieved from https://hdl.handle.net/10161/28432.

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Scholars@Duke

Greene

Lydia Greene

Dir, Acad Engagement for Acad Discipline

I am currently the Director of Academic Engagement for Natural & Quantitative Sciences in Duke's Academic Advising Center. My work involves mentoring and advising undergraduates pursuing opportunities and careers in the STEM fields, and working with campus partners to develop more inclusive STEM programming.

My own research is on the ecology of lemurs in Madagascar, with a central focus on mechanisms of local adaptation in sifakas. Prior to my role as NQS DAE, I was a postdoctoral associate at the Duke Lemur Center and graduate student in Duke's Ecology Program. My dissertation research was on the role of the gut microbiome in facilitating folivory as an ecological strategy in lemurs. 

Yoder

Anne Daphne Yoder

Braxton Craven Distinguished Professor of Evolutionary Biology

My work integrates field inventory activities with molecular phylogenetic techniques and geospatial analysis to investigate Madagascar, an area of the world that is biologically complex, poorly understood, and urgently threatened. Madagascar has been designated as one of the most critical geographic priorities for conservation action, retaining less than 10% of the natural habitats that existed before human colonization. It is critical that information be obtained as quickly as possible to document the biota that occurs in the remaining and highly threatened forested areas of western Madagascar, to gain an understanding of the evolutionary processes and associated distributional patterns that have shaped this diversity, and to use this information to help set conservation priorities. Phylogenetic and biogeographic analysis of Malagasy vertebrates, each with unique life-history and dispersal characteristics, are conducted to identify areas of high endemism potentially associated with underlying geological features, and also to test for the role that geographic features have played in generating patterns of vertebrate diversity and distribution. My lab also has a significant focus on capacity-building through the education and training of both American and Malagasy students. Research opportunities for American graduate students are enhanced by the formation of Malagasy/American partnerships.


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