Gut microbiome, diet, and conservation of endangered langurs in Sri Lanka

Amato, Katherine R.; Kuthyar, Sahana; Ekanayake‐Weber, Marcy; Salmi, Roberta; Snyder‐Mackler, Noah; Wijayathunga, Lasanthi; Vandercone, Rajnish P. G.; Lu, Amy

doi:10.1111/btp.12805

Cited by 19 publications

(15 citation statements)

References 58 publications

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“…Similarly, a study of the GSM microbiome found high relative abundances of ber-degrading Prevotella and Ruminocaccaceae [43]. The fecal microbiomes of gray (Semnopithecus priam) and purple-faced langurs (S. vetulus) contain many of the same microbial taxa that we detected in the GSM [44]. Finally, proboscis monkey (Nasalis larvatus) foreguts have high abundances of Prevotella, which likely function in structural carbohydrate degradation [45].…”

Section: Discussionsupporting

confidence: 56%

Digestive Adaptations of Both the Fore- and Hind-gut in a Temperate Colobine Monkey

Liu¹,

Amato²,

Hou³

et al. 2021

Preprint

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Background: In mammal herbivores, the digestion of fiber usually occurs predominantly in either the foregut or in the hindgut. However, how both gut regions function synergistically in the digestion of fiber and other nutrients has rarely been reported in wild mammals. This requires an integrative study of host anatomy, physiology and gut microbiome. Colobine monkeys (Colobinae) are folivorous, with fiber fermentation primarily occurring in the foregut, with residual fermentation in the hindgut. For the few colobine species that live in temperate regions obtaining energy from fiber during winter is critical but the mechanisms enabling this remain unclear. Results: We studied microbial and morphological digestive adaptations of golden snub-nosed monkeys (GSMs), Rhinopithecus roxellana, a temperate forest colobine from central China. We tested for synergistic foregut and hindgut fiber digestion in a species that experiences high thermal energy demands while restricted to a fibrous, low-energy winter diet. We found that the GSM’s colon has a significantly greater volume than that of other foregut fermenting colobines, and both gut regions of GSMs are dominated by microbial taxa producing enzymes to enable active digestion of complex carbohydrates. The microbiomes of the fore- and hindgut differed significantly in composition and abundance. Although the expression of microbial gene functions for fiber digestion were higher in the foregut than in the hindgut, our microbiome analysis in conjunction with that for morphology, enzyme activity and fiber-protein digestion, suggests complementary fiber and protein metabolism in both gut regions. Conclusions: Our results support that both the GSM fore- and hindgut facilitate fiber digestion, with an enlarged colon consistent as an adaptation to accommodate high throughput of fiber-rich food during winter.

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Section: Discussionsupporting

confidence: 56%

Digestive Adaptations of Both the Fore- and Hind-gut in a Temperate Colobine Monkey

Liu¹,

Amato²,

Hou³

et al. 2021

Preprint

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“…Molecular adaptation of RNASE1 may thus be part of a folivory strategy involving large body size, at least in the case of indriids and howlers, caeco-colonic fermentation, and relatively generalist feeding strategies. There is some evidence that sifakas, howler monkeys, and some colobines may be somewhat resilient to habitat disturbance due to their dietary flexibility and ability to rely on foliage as fallback foods (7,(69)(70)(71)(72).…”

Section: Discussionmentioning

confidence: 99%

Molecular adaptation to folivory and the conservation implications for Madagascar’s lemurs

Guevara

Greene

Blanco

et al. 2021

Preprint

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Folivory evolved independently at least three times over the last 40 million years among Madagascar's lemurs. 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 contention that not all primate folivores are built the same and highlight 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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Section: Discussionmentioning

confidence: 99%

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

et al. 2021

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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.

show abstract

Gut microbiome, diet, and conservation of endangered langurs in Sri Lanka

Cited by 19 publications

References 58 publications

Digestive Adaptations of Both the Fore- and Hind-gut in a Temperate Colobine Monkey

Digestive Adaptations of Both the Fore- and Hind-gut in a Temperate Colobine Monkey

Molecular adaptation to folivory and the conservation implications for Madagascar’s lemurs

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

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