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

Abstract

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.

Diet drove brain and dental morphological coevolution in strepsirrhine primates

“…Finally, topographic complexity of the molar crown did not reveal a clear pattern discriminating dietary specialisations, although mean OPCR was higher in folivores and lower in frugivores. Ambiguous differentiation of dietary guilds based on OPCR has previously been reported in prosimians, especially after controlling for phylogenetic relatedness [ 23 , 47 ] Unexpectedly, the highest variation in OPCR was found in folivorous species, which could reflect the importance of specialisations to different folivore niches during the diversification of Malagasy lemurs [ 49 ]. Significant integration between dental morphology and brain size and shape suggests that, despite their assumed independence, dietary specialisations represented a major factor canalising their variation to act as a functional unit.…”

“…Moreover, our results of higher evolutionary rates in folivores indicate unexpected phenotypic changes to adapt to folivorous niches. Malagasy colonisation by strepsirrhine primates has been associated with a diversification of folivore niches, linked to significant molecular adaptations to occupy non-overlapping niches and avoid competition [ 49 ]. Our results showing accelerated phenotypic changes in folivores can be linked to the folivorous diversification of malagasy lemurs.…”

“…Evolutionary model fitting revealed that the two most-integrated traits (brain shape and dental morphology) followed the same trajectory, but that trajectory differed across guilds. Brain shape and dental morphology evolved under stabilising selection in folivores and following a BM process in frugivores, signalling the selective pressures acting during the phenotypic evolution of folivorous strepsirrhines and the ancestral frugivorous state in Strepsirrhini [ 25 , 28 , 49 ]. Our results suggest that adapting to insectivory correlated with directional selection in brain shape, the only guild with such a pattern.…”