Evolutionary and phylogenetic insights from a nuclear genome sequence of the extinct, giant ‘subfossil’ koala lemurMegaladapis edwardsi

Abstract

No endemic Madagascar animal with body mass >10 kg survived a relatively recent wave of extinction on the island. From morphological and isotopic analyses of skeletal "subfossil" remains we can reconstruct some of the biology and behavioral ecology of giant lemurs (primates; up to ~160 kg), elephant birds (up to ~860 kg), and other extraordinary Malagasy megafauna that survived well into the past millennium. Yet much about the evolutionary biology of these now extinct species remains unknown, along with persistent phylogenetic uncertainty in some cases. Thankfully, despite the challenges of DNA preservation in tropical and sub-tropical environments, technical advances have enabled the recovery of ancient DNA from some Malagasy subfossil specimens. Here we present a nuclear genome sequence (~2X coverage) for one of the largest extinct lemurs, the koala lemur Megaladapis edwardsi (~85kg). To support the testing of key phylogenetic and evolutionary hypotheses we also generated new high-coverage complete nuclear genomes for two extant lemur species, Eulemur rufifrons and Lepilemur mustelinus, and we aligned these sequences with previously published genomes for three other extant lemur species and 47 non-lemur vertebrates. Our phylogenetic results confirm that Megaladapis is most closely related to the extant Lemuridae (typified in our analysis by E. rufifrons) to the exclusion of L. mustelinus, which contradicts morphology-based phylogenies. Our evolutionary analyses identified significant convergent evolution between M. edwardsi and extant folivorous primates (colobine monkeys) and ungulate herbivores (horses) in genes encoding protein products that function in the biodegradation of plant toxins and nutrient absorption. These results suggest that koala lemurs were highly adapted to a leaf-based diet, which may also explain their convergent craniodental morphology with the small-bodied folivore Lepilemur.

Examining Natural History through the Lens of Palaeogenomics

“…specimen excavated in the Southern Caucasus [16] and >120 000 year old specimens of the straight-tusked elephant (Palaeoloxodon antiquus) from Germany [17] (Figure 1). Palaeogenomic data have already provided insight into the process of domestication [18,19], the phylogenetic relationships and evolutionary adaptations of extinct species [20,21,93,94], the mechanisms underlying the loss of flight in palaeognathous birds [22], the convergence between carnivorous marsupials and placental mammals [23,24], and the origin of some of humanity's deadliest diseases [25]. However, in this review, we will examine how the palaeogenomic revolution can contribute new insights into past ecological communities and provide a new dimension to Quaternary science that can inform our interpretation of fossil data more broadly.…”

Iterative deletion of gene trees detects extreme biases in distance-based phylogenomic coalescent analyses

“…One of the most surprising conflicts in the distance-based coalescent trees involved placement of the aye-aye, Daubentonia (Chiromyiformes), a highly specialized strepsirrhine primate that is well established as the sister group to lemurs (Lemuriformes). This sister-group relationship is supported by mitochondrial genomes (Finstermeier et al, 2013), supermatrices (Fabre et al, 2009; Perelman et al, 2011; Springer et al, 2012), nuclear genomes (Marciniak et al 2021), and low-homoplasy retroelement insertions (McLain et al, 2012). By contrast, STAR and NJst (Fig.…”

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

“…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).…”

“…Madagascar was also home to several larger bodied, extinct, "subfossil" lineages that were also likely characterized by folivory, including the "sloth lemurs" (family: Paleopropithecidae) and the koala lemurs (genus: Megaladapis) (Yoder, 1999;Fleagle, 2013;Kistler et al, 2015;Marciniak et al, 2021). It is difficult to estimate the number of times that folivory evolved independently in lemurs with confidence, especially given challenges to reconstructing the phylogenetic relationships among lemur families (Horvath et al, 2008;Perelman et al, 2011;McLain et al, 2012;Springer et al, 2012;Herrera and Dávalos, 2016), likely due to a series of ancient rapid divergences resulting in incomplete lineage sorting (Horvath et al, 2008;Marciniak et al, 2021). However, the ancestral lemurid is thought to be a generalist, with folivory in bamboo lemurs representing convergence with other lemur lineages (Ballhorn et al, 2016;Fulwood et al, 2021).…”