Comparative genomic analysis of sifakas ( Propithecus ) reveals selection for folivory and high heterozygosity despite endangered status

Abstract

Sifakas (genus Propithecus) are critically endangered, large-bodied diurnal lemurs that eat leaf-based diets and show corresponding anatomical and microbial adaptations to folivory. We report on the genome assembly of Coquerel’s sifaka (P. coquereli) and the resequenced genomes of Verreaux’s (P. verreauxi), the golden-crowned (P. tattersalli), and the diademed (P. diadema) sifakas. We find high heterozygosity in all sifakas compared with other primates and endangered mammals. Demographic reconstructions nevertheless suggest declines in effective population size beginning before human arrival on Madagascar. Comparative genomic analyses indicate pervasive accelerated evolution in the ancestral sifaka lineage affecting genes in several complementary pathways relevant to folivory, including nutrient absorption and xenobiotic and fatty acid metabolism. Sifakas show convergent evolution at the level of the pathway, gene family, gene, and amino acid substitution with other folivores. Although sifakas have relatively generalized diets, the physiological challenges of habitual folivory likely led to strong selection.

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

“…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 (Estrada and Coates-Estrada, 1996;Bicca-Marques, 2003;Rimbach et al, 2013;Amato et al, 2020;Guevara et al, 2021).…”

“…As such, additional genetic analyses of various genes with roles in detoxification capacity and taste and odor perception could provide insights into differences in functional capacity that could inform conservation assessments. For example, members of the cytochrome P450 monooxygenase gene superfamily are hypothesized to evolve in response to plant secondary compound composition (Gonzalez and Nebert, 1990), and have shown rapid evolution in folivorous mammals, including lemurs (Hu et al, 2017;Johnson et al, 2018;Guevara et al, 2021). Sifakas and extinct koala lemurs (Megaladapis edwardsi), the latter based on a recent innovative analysis of recovered ancient DNA, show evidence of molecular adaptation in genes involved in detoxification and nutrient absorption (Guevara et al, 2021;Marciniak et al, 2021).…”

“…For example, members of the cytochrome P450 monooxygenase gene superfamily are hypothesized to evolve in response to plant secondary compound composition (Gonzalez and Nebert, 1990), and have shown rapid evolution in folivorous mammals, including lemurs (Hu et al, 2017;Johnson et al, 2018;Guevara et al, 2021). Sifakas and extinct koala lemurs (Megaladapis edwardsi), the latter based on a recent innovative analysis of recovered ancient DNA, show evidence of molecular adaptation in genes involved in detoxification and nutrient absorption (Guevara et al, 2021;Marciniak et al, 2021). Bitter taste receptor evolution may also play a key role in fine-tuning primate plant food selection (Soranzo et al, 2005;Purba et al, 2017;Dong et al, 2021).…”

“…Our previous work has uncovered positively selected sites in RNASE1 in sifaka lemurs (genus Propithecus) (Guevara et al, 2021). Sifakas, along with the indri (genus Indri) and woolly lemurs (genus Avahi), belong to the family Indriidae, all of whose members eat diets high in leafy material and show traits associated with obtaining nutrients from leaves.…”

Maternal stress effects on infant development in wild Verreaux's sifaka (Propithecus verreauxi)

“…Food availability, estimated as the relative abundance of leaves, flowers, and fruits (i.e., the main constituents of sifakas' diet, Guevara et al 2021), was assessed during biweekly phenology transects of 784 trees in the study area as detailed elsewhere (Koch et al 2017). Briefly, we applied a semi-quantitative method in which the availability for each food item was scored on an ordinal scale ranging from 0 to 4, where 0 reflects the complete absence of the item and 4 represents its maximum abundance.…”