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Chitinase Genes (Chias) Provide Genomic Footprints of a Post-Cretaceous Dietary Radiation in Placental Mammals

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Chitinase Genes (Chias) Provide Genomic Footprints of a Post-Cretaceous Dietary Radiation in Placental Mammals Whittier College Poet Commons Biology Faculty Publications & Research 2018 Chitinase genes (CHIAs) provide genomic footprints of a post- Cretaceous dietary radiation in placental mammals Christopher A. Emerling [email protected] Frédéric Delsuc Michael W. Nachman Follow this and additional works at: https://poetcommons.whittier.edu/bio Part of the Biology Commons Recommended Citation Emerling, C. A., Delsuc, F., & Nachman, M. W. (2018). Chitinase genes (CHIAs) provide genomic footprints of a post-Cretaceous dietary radiation in placental mammals. Science Advances, 4(5), 1-10. https://doi.org/10.1126/sciadv.aar6478 This Article is brought to you for free and open access by the Faculty Publications & Research at Poet Commons. It has been accepted for inclusion in Biology by an authorized administrator of Poet Commons. For more information, please contact [email protected]. SCIENCE ADVANCES | RESEARCH ARTICLE EVOLUTIONARY BIOLOGY Copyright © 2018 The Authors, some Chitinase genes (CHIAs) provide genomic footprints of a rights reserved; exclusive licensee post-Cretaceous dietary radiation in placental mammals American Association for the Advancement 1,2 2 1 of Science. No claim to Christopher A. Emerling, * Frédéric Delsuc, Michael W. Nachman original U.S. Government Works. Distributed The end-Cretaceous extinction led to a massive faunal turnover, with placental mammals radiating in the wake of under a Creative nonavian dinosaurs. Fossils indicate that Cretaceous stem placentals were generally insectivorous, whereas their Commons Attribution earliest Cenozoic descendants occupied a variety of dietary niches. It is hypothesized that this dietary radiation NonCommercial resulted from the opening of niche space, following the extinction of dinosaurian carnivores and herbivores. We License 4.0 (CC BY-NC). provide the first genomic evidence for the occurrence and timing of this dietary radiation in placental mammals. By comparing the genomes of 107 placental mammals, we robustly infer that chitinase genes (CHIAs), encoding en- zymes capable of digesting insect exoskeletal chitin, were present as five functional copies in the ancestor of all placental mammals, and the number of functional CHIAs in the genomes of extant species positively correlates with the percentage of invertebrates in their diets. The diverse repertoire of CHIAs in early placental mammals corrobo- rates fossil evidence of insectivory in Cretaceous eutherians, with descendant lineages repeatedly losing CHIAs beginning at the Cretaceous/Paleogene (K/Pg) boundary as they radiated into noninsectivorous niches. Further- Downloaded from more, the timing of gene loss suggests that interordinal diversification of placental mammals in the Cretaceous predates the dietary radiation in the early Cenozoic, helping to reconcile a long-standing debate between molecular timetrees and the fossil record. Our results demonstrate that placental mammal genomes, including humans, retain a molecular record of the post-K/Pg placental adaptive radiation in the form of numerous chitinase pseudogenes. http://advances.sciencemag.org/ INTRODUCTION in placental mammals relative to the K/Pg boundary. We provide ev- The traditional model of mammalian evolution posits that after origi- idence that CHIAs retain a genomic signal of the early Cenozoic radia- nating in the Triassic-Jurassic, Mesozoic mammals were typically small, tion of placental mammals, via the repeated, convergent decay of nocturnal, generalized terrestrial insectivores, limited in taxonomic and CHIAs in noninsectivorous mammals after the K/Pg boundary. ecological diversity due to predation by and/or competition with dino- saurs. After the extinction of nonavian dinosaurs at the Cretaceous/ Paleogene (K/Pg) boundary, Cenozoic mammals then radiated into RESULTS AND DISCUSSION an enormous range of ecologically distinct niches (1, 2). Recent re- Five CHIA paralogs in the last common ancestor of search suggests that this model is incomplete, with some fossil evi- placental mammals dence for Mesozoic diversification and niche expansion in mammals The original study describing CHIA reported only a single gene (13), (3–6). However, most Mesozoic eutherians (placental mammals + but we found numerous placental CHIA paralogs, similar to recent on October 1, 2020 stem taxa) were small, likely terrestrial-scansorial, and had jaw and analyses (16, 17). Phylogenetic analyses cluster these into five major dental morphologies consistent with insectivory (1, 4, 7). Further- clades(Fig.1;figs.S1toS3;andtableS1),whichwerefertoasCHIA1, more, although there is some evidence of eutherian niche diversifi- CHIA2, CHIA3, CHIA4,andCHIA5. All four superorders of placental cation in the Late Cretaceous (1, 8, 9), the fossil record unequivocally mammals (Xenarthra, Afrotheria, Euarchontoglires, and Laurasiatheria) points to an unprecedented adaptive radiation of placental mammals are represented by orthologs in all five CHIA clades, implying that the after the K/Pg boundary (1, 8–11). last common ancestor of placental mammals had five CHIAs. There is a Here, we test the hypothesis that this landmark evolutionary radia- consistent syntenic orientation of the paralogs, with multiple instances tion left a molecular signature in placental mammal genomes, specifi- of all five being localized to the same genomic contig/scaffold (fig. S4 cally in regard to diet. Jeuniaux (12) hypothesized that mammals and table S2). Each putatively functional CHIA paralog is of nearly inherited gastrointestinal (GI) chitinases from a vertebrate ancestor identical length, consists of 11 coding exons, and has canonical splice andsubsequentlylostthemastheyadapted to noninsectivorous diets. donor and acceptor sites, a catalytic domain in exon 5 (fig. S5) (18), Molecular studies have isolated an acidic mammalian chitinase (CHIA) and a chitin-binding domain in exon 11 (fig. S6) (19), suggesting that expressed in the mammalian GI tract (13, 14)thatisstableinthepres- all five CHIAs encode enzymes with chitinolytic function. Furthermore, ence of GI proteases (15),suggestingaroleinchitindigestion.Inthe transcriptome analyses indicate that all five CHIAs can be expressed absence of dietary chitin, selection on chitinase genes may have been in placental mammal GI tracts (table S3) and, therefore, each poten- relaxed, allowing for the accumulation of formerly deleterious mutations tially participates in the breakdown of ingested chitin. (for example, frameshift and nonsense mutations), resulting in unitary pseudogenes and gene deletions. We tested Jeuniaux’s(12) hypothesis CHIA and loss dietary shifts to carnivory and herbivory by analyzing patterns of acidic mammalian chitinase gene (CHIA)loss Although we inferred gene duplications early in mammalian history (fig. S1), the only duplications in crown Placentalia resulted in paralogs likely to be nonfunctional or lacking chitinolytic function (tables S1 and 1 Museum of Vertebrate Zoology, University of California, Berkeley, CA 94720, USA. S4 and figs. S2 and S3), with at least some of these duplicates appearing 2Institut des Sciences de l’Évolution de Montpellier (ISEM), Université de Montpel- lier, CNRS, IRD, EPHE, Montpellier, France. to have neofunctionalized into genes with immune-related functions *Corresponding author. Email: [email protected] (fig. S3) (20). By contrast, we found that CHIA loss, via pseudogenization Emerling, Delsuc, Nachman, Sci. Adv. 2018; 4 : eaar6478 16 May 2018 1of10 SCIENCE ADVANCES | RESEARCH ARTICLE CHIA2 CHIA3 Downloaded from CHIA1 CHIA4 http://advances.sciencemag.org/ CHIA5 Fig. 1. Placental mammal CHIA gene tree, simplified from fig. S3. Closed circles indicate functional CHIAs, and open circles indicate pseudogenic CHIAsand/orCHIAs lacking a chitinolytic and/or chitin-binding domain. Colored branches correspond to a subset of placental mammal clades: green, Cetartiodactyla; orange, Carnivora; on October 1, 2020 pink, Perissodactyla; red, Xenarthra; purple, Afrotheria; brown, Scandentia; cyan, Strepsirrhini; blue, Anthropoidea; yellow, Dermoptera. Silhouettes and licenses here and throughout are from phylopic.org. and whole-gene deletion, has occurred very frequently, particularly in Whereas the earliest placental mammals had five CHIAs, inactivat- carnivorous and herbivorous lineages (table S1). Strikingly, species with ing mutations and gene deletions shared between multiple species point five to three CHIA copies have, on average, a diet that consists almost to losses of functional CHIAs during the origins of modern placental entirely of invertebrates (five CHIAs, 88.3% diet invertebrates on aver- clades (Fig. 3 and table S4). Whereas some CHIAs were lost in indi- age; four CHIAs, 85%; three CHIAs, 80%), species with two copies on vidual species or families, other losses occurred before interordinal average consume a moderate amount of invertebrates (63.3%), and spe- (Paenungulata and Ostentoria) and intraordinal (Chiroptera, Carnivora, cies with one or no CHIAs average minimal invertebrate consumption Perissodactyla, Cetartiodactyla, and Lagomorpha) diversification. Sig- (one CHIA, 21.9%; no CHIAs, 7%). Phylogenetic generalized least- nificantly, all or nearly all CHIA genes were lost during the origin squares (PGLS) regression analyses using CHIAs derived from both and diversification of noninsectivorous lineages, including the herbivo- − gene models (n = 73, r2 = 0.3358, P =7.824×10 8) and genomic contigs rous sloths (Folivora), hyraxes, elephants, and sirenians (Paenungulata),
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