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Dietary Specialization Drives Multiple Independent Losses and Gains in the Bitter Taste Gene Repertoire of Laurasiatherian Mammals

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Dietary Specialization Drives Multiple Independent Losses and Gains in the Bitter Taste Gene Repertoire of Laurasiatherian Mammals Dietary specialization drives multiple independent losses and gains in the bitter taste gene repertoire of Laurasiatherian Mammals Liu et al. Frontiers in Zoology (2016) 13:28 DOI 10.1186/s12983-016-0161-1 Liu et al. Frontiers in Zoology (2016) 13:28 DOI 10.1186/s12983-016-0161-1 RESEARCH Open Access Dietary specialization drives multiple independent losses and gains in the bitter taste gene repertoire of Laurasiatherian Mammals Zhijin Liu1,2*†, Guangjian Liu1†, Frank Hailer2†, Pablo Orozco-terWengel2†, Xinxin Tan1,3†, Jundong Tian4, Zhongze Yan1,3, Baowei Zhang5 and Ming Li1* Abstract Background: Bitter taste perception is essential for species with selective food intake, enabling them to avoid unpalatable or toxic items. Previous studies noted a marked variation in the number of TAS2R genes among various vertebrate species, but the underlying causes are not well understood. Laurasiatherian mammals have highly diversified dietary niche, showing repeated evolution of specialized feeding preferences in multiple lineages and offering a unique chance to investigate how various feeding niches are associated with copy number variation for bitter taste receptor genes. Results: Here we investigated the evolutionary trajectories of TAS2Rs and their implications on bitter taste perception in whole-genome assemblies of 41 Laurasiatherian species. The number of intact TAS2Rs copies varied considerably, ranging from 0 to 52. As an extreme example of a narrow dietary niche, the Chinese pangolin possessed the lowest number of intact TAS2Rs(n = 2) among studied terrestrial vertebrates. Marine mammals (cetacea and pinnipedia), which swallow prey whole, presented a reduced copy number of TAS2Rs(n = 0-5). In contrast, independent insectivorous lineages, such as the shrew and insectivorous bats possessed a higher TAS2R diversity (n =52andn = 20-32, respectively), exceeding that in herbivores (n = 9-22) and omnivores (n = 18-22). Conclusions: Besides herbivores, insectivores in Laurasiatheria tend to have more functional TAS2Rsincomparisonto carnivores and omnivores. Furthermore, animals swallowing food whole (cetacean, pinnipedia and pangolin) have lost most functional TAS2Rs. These findings provide the most comprehensive view of the bitter taste gene repertoire in Laurasiatherian mammals to date, casting new light on the relationship between losses and gains of TAS2Rs and dietary specialization in mammals. Keywords: Laurasiatheria, Mammal, Bitter taste receptor, TAS2R, Gene gain and loss, Dietary specialization Background noted a marked variation in the number of TAS2R genes The ability to perceive taste provides animals with import- among various vertebrate species, but the underlying cause ant dietary information that can be crucial for their sur- is not well understood [2, 3]. A study surveying bitter taste vival. Bitter taste perception is mediated by a group of G receptor genes in 52 vertebrate species (fish, birds, amphib- protein-coupled receptors, which are encoded by the type ians, reptiles and mammals) [4] reported that the number 2 taste receptor gene family (TAS2Rs) [1]. Previous studies of TAS2R genesperspeciescorrelateswiththeproportion of plants in their diet. Furthermore, carnivores were found * Correspondence: [email protected]; [email protected] to have fewer TAS2R genes compared to herbivores and † Equal contributors omnivores [5]. Because plant tissues contain more toxic 1Key laboratory of Animal Ecology and Conservation Biology, Institute of Zoology, Chinese Academy of Sciences, 1-5 Beichen West Road, Chaoyang, compounds than animal tissues, these findings suggest that Beijing 100101, China dietary toxins are a major selective force influencing the Full list of author information is available at the end of the article © 2016 The Author(s). Open Access This article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated. Liu et al. Frontiers in Zoology (2016) 13:28 Page 2 of 9 diversity of the TAS2R repertoire. Given this finding, it is partial and 473 disrupted TAS2Rs) in these genome assem- reasonable to speculate that animals whose diet contains blies were annotated (Fig. 1), with the number of intact more toxins, besides herbivores, tend to have more func- (both complete and partial copies) TAS2Rs varying in the tional TAS2Rs, while animals with less dependence on bit- range from 0 to 52 (Figs. 1 and 2). The sequences and ter taste are likely to lose a certain number of functional genomic locations of these TAS2Rs are listed in the elec- TAS2Rs. To test this hypothesis it is necessary to rely on a tronic supplementary dataset. Among all studied terrestrial taxon with highly diversified and specialized dietary niches. Laurasiatherian mammals the average number of TASR2s Over an estimated ~80 million years of diversification [6], was 18.7 (standard deviation, sd: 8.6), with the Chinese Laurasiatherian mammals have evolved multiple lineage- pangolin presenting the lowest number of intact TAR2Rs specific feeding characteristics, such as the obligate ant- (n = 2). Marine cetaceans (whale and dolphin) and pinni- ingesting pangolins, the insectivorous shrews, carnivores pedia (walrus and seal) also showed few intact TAS2Rs (cats, dogs and allies), ungulate herbivores, herbivorous or (range: 0–5). The insectivorous shrew (Sorex araneus) insectivorous bats, and marine mammals that adopted a showed the largest number of intact TAS2Rs(n = 52). purely marine diet [7]. During the process of diet differenti- Similarly, insect-eating bats also had significantly higher ation in Laurasiatheria, bitter taste preferences presumably numbers of intact TAS2Rs(n = 20-32) compared to evolved adaptively to avoid ingestion of indigestible or fruit-eating flying foxes (n = 14-18; Fishers Exact Test, harmful compounds. In particular, there are several inde- P = 0.008). The numbers of intact TAS2Rsinherbivorous pendent insectivorous lineages (shrews, insectivorous bats ruminants, tylopods and perissodactyls ranged from 15 to and so on). Eating insects is similar to herbivory, where de- 20, 9–13 and 21–27, respectively. The terrestrial Carnivora tecting toxins is important. Many insects release defensive (excluding walrus and seal) had 12–17 functional TAS2Rs secretions that are toxic to their predators [8–10]. It could (Fig. 2). therefore be hypothesized thatinsectivoresmaybeexposed The phylogeny of all alignable TAS2Rs in the 41 stud- to a similar amount of toxins as herbivores. Furthermore, ied Laurasiatherian mammals was constructed, including there are also several independent lineages (cetaceans, pinni- representative orthologs from all 28 clades of Euarchon- peds and pangolins), which have evolved specialised foraging toglires TAS2Rs reported in Hayakawa et al. [12]. The behaviour, ingesting prey whole. These species are likely to gene tree recovered the same 28 main clades of TAS2Rs lose a certain number of functional TAS2Rsduetoless in Laurasiatheria as in Euarchontoglires (hence for all dependence on the taste perception. In summary, Laura- Boreoeutheria), thus we maintained the nomenclature of siatheria offers a unique chance to investigate how various the TAS2Rs clades established by Hayakawa et al. [12]. feeding niches are associated with copy number variation TAS2R6 and TAS2R13 were not found in the studied for bitter taste receptor genes. Since the publication of Li Laurasiatherian mammals (Fig. 3a). Additionally, ortho- and Zhang [4] additional vertebrate genomes have become logs of the clade TAS2R301 in Laurasiatheria were pseu- available for study. Wang and Zhao [11] have reported a dogenized. Conservatively, we conclude that the most small repertoire of TAS2Rsinbirdsbasedonagenomicsur- recent common ancestor (MRCA) of Laurasiatheria had vey including 48 birds. Furthermore, Hayakawa et al. [12] at least 25 intact TAS2Rs. The orthologous and paralo- have described the frequent expansions of the TAS2Rsin gous relationships among the annotated Laurasiatherian the Euarchontoglires clade, which is the sister clade of Laura- TAS2Rs are provided in Additional file 1: Table S2. sitherian mammals. However, less research has been carried out concerning the evolutionary history of the repertoire of Lineage-specific gene degeneration and expansion in TAS2Rs in Laurasitheria. Here we use a comprehensive set Laurasiatherian TAS2Rs of 41 Laurasitherian genomes encompassing all dietary Chinese pangolin (Manis pentadactyla)onlycontainedtwo niches across mammals and test the potential impact of all intact bitter taste genes (TAS2R1 and TAS2R7;Fig.1).In dietary types (herbivory, insectivory, carnivory and omnivory) Cetartiodactylaonlytheminkewhale(Balaenoptera acutor- and foraging behaviours (swallowing the prey whole or not) ostrata) and the Antarctic minke whale (Balaenoptera on the evolutionary scenarios of TAS2Rs in Laurasiatherian bonaerensis)retainasingleTAS2R gene, although each mammals. The results showed that the diverse dietary species retains a different one, i.e. TAS2R16 and TAS2R67, characteristics in Laurasiatheria have had a larger impact
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