簡易檢索 / 詳目顯示

研究生: 范桂慈
Fan, Kuei-Tzu
論文名稱: 以形態學以及多體學方法探究尼羅河鼠(Arvicanthis niloticus)費洛蒙感知系統的演化
Evolution of Pheromone Sensing System of the Nile rat (Arvicanthis niloticus): A Morphological and Multi-omic Study
指導教授: 廖本揚
Liao, Ben-Yang
焦傳金
Chiao, Chuan-Chin
口試委員: 陳豐奇
Chen, Feng-Chi
陳俊宏
Chen, Chun-Hong
學位類別: 碩士
Master
系所名稱: 生命科學暨醫學院 - 分子醫學研究所
Institute of Molecular Medicine
論文出版年: 2024
畢業學年度: 112
語文別: 中文
論文頁數: 110
中文關鍵詞: 感官系統生理生態學日行性夜行性囓齒目
外文關鍵詞: Sensory System, Physiological Ecology, Diurnal, Nocturnal, Rodents
相關次數: 點閱:1下載:0
分享至:
查詢本校圖書館目錄 查詢臺灣博碩士論文知識加值系統 勘誤回報
  • 為因應環境變化,動物發展出不同類型的感官系統來接受環境中的訊息。哺乳動物的嗅覺包括氣味感知和費洛蒙感知兩個系統;這兩個系統都會影響個體的行為,並且其相關的基因群也各不相同。尼羅河鼠(Arvicanthis niloticus)與小家鼠(Mus musculus)近緣,而褐家鼠(Rattus norvegicus)為其兩者的外群;然而,不同於夜行性的小家鼠和褐家鼠,尼羅河鼠為日行性。我們過去的研究發現,尼羅河鼠在演化過程中為節省感知所需的能量消耗,在獲得日光視覺和增強視力敏銳度的同時,其氣味感知能力發生退化。於是我們探討尼羅河鼠的費洛蒙感知系統是否與氣味感知系統在演化上連動,同時發生退化的情形。首先,我們透過微電腦斷層(Micro-CT)量測並比較小家鼠、尼羅河鼠和褐家鼠頭骨的犁鼻器(VNO, vomeronasal organ)的形態。結果顯示,尼羅河鼠犁鼻器並非三者中最小。透過基因體以及轉錄體分析,我們比較三個物種與犁鼻器功能相關的基因群數量以及mRNA表達量,這些基因包含第一型犁鼻器受體(V1R)和第二型犁鼻器受體(V2R)。結果發現儘管尼羅河鼠擁有三者中最少的V2R基因,其V1R基因數量和所佔比例皆高於褐家鼠。更重要的是,尼羅河鼠具備高mRNA表達的犁鼻器基因數量,在三個物種中最多。顯然,尼羅河鼠的費洛蒙感知系統並沒有退化。我們針對尼羅河鼠的研究顯示,哺乳動物兩種嗅覺系統在演化的過程中,呈現獨立而不連動的關係。


    Animal species have evolved sensory systems that work as modules to perceive environmental cues. Mammalian olfaction comprises two major systems: the odorant detection system and the pheromone sensing system, each influencing individual behavior through distinct gene families. The Nile rat (Arvicanthis niloticus), which is phylogenetically closer to the mouse (Mus musculus) than the rat (Rattus norvegicus), has recently transitioned from a nocturnal to a diurnal diel pattern. Our previous study on the Nile rat showed that the odorant detection system of this species has been traded off evolutionarily following the acquisition of daylight vision and enhanced visual acuity. In this thesis, we investigate whether the pheromone sensing system of the Nile rat has been evolutionarily coupled with the odorant detection system and has also degenerated. To explore this, we compared the morphological data of the vomeronasal organ (VNO) based on 3D models derived from micro-CT images of the mouse, the Nile rat, and the rat skulls. The results indicate that the Nile rat doesn't have the smallest VNO size in terms of relative sizes of both length and surface area. Additionally, we conducted comparative genomics and transcriptome of the three species, focusing on two vomeronasal receptors gene families: type 1 vomeronasal receptors (V1Rs) and type 2 vomeronasal receptors (V2Rs). The Nile rat has the fewest V2R genes, but it has a greater number of V1R genes and a higher ratio of intact V1R genes compared to the rat. More importantly, the mRNA abundance data showed that the number of VNO-expressed V1R genes in the Nile rat is the largest among the three species studied. Our findings suggest that the pheromone sensing system of the Nile rat has not degenerated, indicating that the two olfaction systems of the Nile rat have evolved independently.

    中文摘要 i ABSTRACT ii 致謝 iii 目錄 iv 圖目錄 viii 表目錄 ix 圖附錄 x 表附錄 x 縮寫 xi 第一章、研究背景 1 1-1.感官系統的演化 1 1-2.日行性尼羅河鼠擁有進化的視覺系統 3 1-3.動物的兩個嗅覺系統 6 1-3-1.檢測氣味的主要嗅覺 6 1-3-2.感知費洛蒙的犁鼻器 9 1-4.日行性尼羅河鼠擁有退化的主要嗅覺 13 1-5.研究目的與假說 14 第二章、材料與方法 17 2-1.動物來源 17 2-2.組織學分析與Micro-CT實驗 17 2-3. 3D模型、形態測量與統計分析 18 2-4.基因組組裝與註釋 18 2-5.定義V1R、V2R和FPR基因 19 2-6.犁鼻器相關基因的獲得和丟失 21 2-7.犁鼻器解剖 23 2-8.RNA-seq實驗與分析 24 第三章、結果 27 3-1.形態數據 27 3-1-1.犁鼻器解剖位置與結構 27 3-1-2.以長度為基礎定義犁鼻器尺寸 28 3-1-3.以表面積為基礎定義犁鼻器尺寸 29 3-2.犁鼻器功能相關的基因庫大小與演化動態(evolutionary dynamics) 31 3-2-1.犁鼻器相關基因數量 31 3-2-2.犁鼻器相關基因的獲得與丟失 33 3-2-3.比較結果:尼羅河鼠的犁鼻器基因家族沒有發生收縮 36 3-3.犁鼻器轉錄體 37 3-3-1.犁鼻器相關基因在犁鼻器的表達量 37 3-3-2.犁鼻器相關基因在主要嗅覺上皮的表達量 39 3-3-3.比較結果:尼羅河鼠的犁鼻器基因轉錄沒有發生減少 40 第四章、討論與結論 42 4-1.犁鼻系統與生態區間的關聯性 42 4-1-1.日夜生態區間 42 4-1-2.明亮和黑暗生態區間 43 4-2.犁鼻系統與社會型態 45 4-3.犁鼻器相關基因數量和表達量 47 4-3-1.非嗅覺和犁鼻器相關基因的GPCRs數量 47 4-3-2.犁鼻器轉錄體表達量的差異 47 4-4.結論 48 圖 50 表 72 參考文獻 84 附圖 96 附表 98

    [1] Niven JE, Laughlin SB. Energy limitation as a selective pressure on the evolution of sensory systems. J Exp Biol. 2008;211(Pt 11):1792-804.
    [2] Avarguès-Weber A, Mota T, Giurfa M. New vistas on honey bee vision. Apidologie. 2012;43(3):244-268.
    [3] Kaveh A, Farhoudi N. A new optimization method: Dolphin echolocation. Adv Eng Softw. 2013;59:53-70.
    [4] Oteiza P, Baldwin MW. Evolution of sensory systems. Curr Opin Neurobiol. 2021;71:52-59.
    [5] Nummela S, Pihlström H, Puolamäki K, et al. Exploring the mammalian sensory space: co-operations and trade-offs among senses. J Comp Physiol A. 2013;199(12):1077-1092.
    [6] Olsson L, Nehaniv C, Polani D. Information trade-offs and the evolution of sensory layouts. In: Artificial Life IX: Proceedings of the ninth international conference on the simulation and synthesis of living systems. MIT Press. 2004:119-124.
    [7] Catania KC. Evolution of sensory specializations in insectivores. Anat Rec A Discov Mol Cell Evol Biol. 2005;287(1):1038-50.
    [8] Shi P, Zhang J. Contrasting modes of evolution between vertebrate sweet/umami receptor genes and bitter receptor genes. Mol Biol Evol. 2006;23(2):292-300.
    [9] Skalnikova P, Frynta D, Abramjan A, et al. Spontaneous color preferences in rhesus monkeys: What is the advantage of primate trichromacy? Behav Processes. 2020;174:104084.
    [10] Surridge AK, Osorio D, Mundy NI. Evolution and selection of trichromatic vision in primates. Trends Ecol Evol. 2003;18(4):198-205.
    [11] Hunt DM, Dulai KS, Cowing JA, et al. Molecular evolution of trichromacy in primates. Vision Res. 1998;38(21):3299-306.
    [12] Hiramatsu C, Melin AD, Allen WL, et al. Experimental evidence that primate trichromacy is well suited for detecting primate social colour signals. P Roy Soc B-Biol Sci. 2017;284(1856).
    [13] Bringmann A, Syrbe S, Gorner K, et al. The primate fovea: Structure, function and development. Prog Retin Eye Res. 2018;66:49-84.
    [14] Provis JM, Diaz CM, Dreher B. Ontogeny of the primate fovea: a central issue in retinal development. Prog Neurobiol. 1998;54(5):549-80.
    [15] Kawamura S, Melin AD. Evolution of genes for color vision and the Chemical Senses in Primates. In: Evolution of the Human Genome I: The genome and genes. Springer Japan. 2017;181-216.
    [16] Carandini M, Churchland AK. Probing perceptual decisions in rodents. Nat Neurosci. 2013;16(7):824-31.
    [17] Gerkema MP, Davies WI, Foster RG, et al. The nocturnal bottleneck and the evolution of activity patterns in mammals. Proc Biol Sci. 2013;280:20130508.
    [18] Verra DM, Sajdak BS, Merriman DK, Hicks D. Diurnal rodents as pertinent animal models of human retinal physiology and pathology. Prog Retin Eye Res. 2020;74:100776.
    [19] Ache BW, Young JM. Olfaction: diverse species, conserved principles. Neuron. 2005;48(3):417-30.
    [20] Balcombe JP. Laboratory environments and rodents' behavioural needs: a review. Lab Anim-Uk. 2006;40(3):217-235.
    [21] Foster RG, Hughes S, Peirson SN. Circadian photoentrainment in mice and humans. Biology (Basel). 2020;9(7).
    [22] Mrosovsky N, Edelstein K, Hastings MH, Maywood ES. Cycle of period gene expression in a diurnal mammal (Spermophilus tridecemlineatus): implications for nonphotic phase shifting. J Biol Rhythms. 2001;16(5):471-8.
    [23] Lee TM. Octodon degus: a diurnal, social, and long-lived rodent. ILAR J. 2004;45(1):14-24.
    [24] Dellaa A, Polosa A, Mbarek S, et al. Characterizing the retinal function of Psammomys obesus: A diurnal rodent model to study human retinal function. Curr Eye Res. 2017;42(1):79-87.
    [25] Refinetti R. The Nile grass rat as a laboratory animal. Lab Anim (NY). 2004;33(9):54-7.
    [26] Blanchong JA, McElhinny TL, Mahoney MM, Smale L. Nocturnal and diurnal rhythms in the unstriped Nile rat, Arvicanthis niloticus. J Biol Rhythm. 1999;14(5):364-377.
    [27] Aghova T, Kimura Y, Bryja J, et al. Fossils know it best: Using a new set of fossil calibrations to improve the temporal phylogenetic framework of murid rodents (Rodentia: Muridae). Mol Phylogenet Evol. 2018;128:98-111.
    [28] Kumar S, Stecher G, Suleski M, Hedges SB. TimeTree: A resource for timelines, Timetrees, and Divergence Times. Mol Biol Evol. 2017;34(7):1812-1819.
    [29] McElhinny TL, Smale L, Holekamp KE. Patterns of body temperature, activity, and reproductive behavior in a tropical murid rodent, Arvicanthis niloticus. Physiol Behav. 1997;62(1):91-6.
    [30] Gaillard F, Bonfield S, Gilmour GS, et al. Retinal anatomy and visual performance in a diurnal cone-rich laboratory rodent, the Nile grass rat (Arvicanthis niloticus). J Comp Neurol. 2008;510(5):525-38.
    [31] Gaillard F, Karten HJ, Sauve Y. Retinorecipient areas in the diurnal murine rodent Arvicanthis niloticus: A disproportionally large superior colliculus. J Comp Neurol. 2013;521(8):Spc1.
    [32] Hecht S. The relation between visual acuity and illumination. J Gen Physiol. 1928;11(3):255-81.
    [33] Gaillard F, Kuny S, Sauve Y. Topographic arrangement of S-cone photoreceptors in the retina of the diurnal Nile grass rat (Arvicanthis niloticus). Invest Ophthalmol Vis Sci. 2009;50(11):5426-34.
    [34] Gilmour GS, Gaillard F, Watson J, et al. The electroretinogram (ERG) of a diurnal cone-rich laboratory rodent, the Nile grass rat (Arvicanthis niloticus). Vision Res. 2008;48(27):2723-31.
    [35] Yan L, Smale L, Nunez AA. Circadian and photic modulation of daily rhythms in diurnal mammals. Eur J Neurosci. 2020;51(1):551-566.
    [36] Zufall F, Munger SD. Chemosensory transduction: The detection of odors, tastes, and other chemostimuli. Elsevier Academic Press. 2016.
    [37] Touhara K, Vosshall LB. Sensing odorants and pheromones with chemosensory receptors. Annu Rev Physiol. 2009;71:307-32.
    [38] Kelliher KR. The combined role of the main olfactory and vomeronasal systems in social communication in mammals. Horm Behav. 2007;52(5):561-70.
    [39] Buck L, Axel R. A novel multigene family may encode odorant receptors: a molecular basis for odor recognition. Cell. 1991;65(1):175-87.
    [40] Niimura Y. Olfactory receptor genes: Evolution. eLS John Wiley & Sons. 2014.
    [41] Niimura Y, Matsui A, Touhara K. Extreme expansion of the olfactory receptor gene repertoire in African elephants and evolutionary dynamics of orthologous gene groups in 13 placental mammals. Genome Res. 2014;24(9):1485-96.
    [42] Touhara K, Sengoku S, Inaki K, et al. Functional identification and reconstitution of an odorant receptor in single olfactory neurons. Proc Natl Acad Sci U S A. 1999;96(7):4040-5.
    [43] Nei M, Niimura Y, Nozawa M. The evolution of animal chemosensory receptor gene repertoires: roles of chance and necessity. Nat Rev Genet. 2008;9(12):951-63.
    [44] Liao BY, Weng MP, Chang TY, et al. Degeneration of the Olfactory System in a Murid Rodent that Evolved Diurnalism. Mol Biol Evol. 2024;41(3).
    [45] Young JM, Kambere M, Trask BJ, Lane RP. Divergent V1R repertoires in five species: Amplification in rodents, decimation in primates, and a surprisingly small repertoire in dogs. Genome Res. 2005;15(2):231-40.
    [46] Young JM, Trask BJ. V2R gene families degenerated in primates, dog and cow, but expanded in opossum. Trends Genet. 2007;23(5):212-5.
    [47] Riviere S, Challet L, Fluegge D, et al. Formyl peptide receptor-like proteins are a novel family of vomeronasal chemosensors. Nature. 2009;459(7246):574-7.
    [48] Silva L, Antunes A. Vomeronasal receptors in vertebrates and the evolution of pheromone detection. Annu Rev Anim Biosci. 2017;5:353-370.
    [49] Dietschi Q, Tuberosa J, Rosingh L, et al. Evolution of immune chemoreceptors into sensors of the outside world. Proc Natl Acad Sci U S A. 2017;114(28):7397-7402.
    [50] Del Punta K, Puche A, Adams NC, et al. A divergent pattern of sensory axonal projections is rendered convergent by second-order neurons in the accessory olfactory bulb. Neuron. 2002;35(6):1057-66.
    [51] Francia S, Silvotti L, Ghirardi F, et al. Evolution of spatially coexpressed families of type-2 vomeronasal receptors in rodents. Genome Biol Evol. 2014;7(1):272-85.
    [52] Meredith M, Westberry JM. Distinctive responses in the medial amygdala to same-species and different-species pheromones. J Neurosci. 2004;24(25):5719-25.
    [53] Ferguson JN, Aldag JM, Insel TR, Young LJ. Oxytocin in the medial amygdala is essential for social recognition in the mouse. J Neurosci. 2001;21(20):8278-85.
    [54] Touhara K. Molecular biology of peptide pheromone production and reception in mice. Adv Genet. 2007;59:147-71.
    [55] Mombaerts P. Genes and ligands for odorant, vomeronasal and taste receptors. Nat Rev Neurosci. 2004;5(4):263-278.
    [56] Niimura Y, Biswa BB, Kishida T, et al. Synchronized expansion and contraction of olfactory, vomeronasal, and taste receptor gene families in Hystricomorph rodents. Mol Biol Evol. 2024;41(4).
    [57] Dulac C, Axel R. A novel family of genes encoding putative pheromone receptors in mammals. Cell. 1995;83(2):195-206.
    [58] Grus WE, Shi P, Zhang J. Largest vertebrate vomeronasal type 1 receptor gene repertoire in the semiaquatic platypus. Mol Biol Evol. 2007;24(10):2153-7.
    [59] Policarpo M, Baldwin MW, Casane D, Salzburger W. Diversity and evolution of the vertebrate chemoreceptor gene repertoire. Nat Commun. 2024;15(1):1421.
    [60] Francia S, Pifferi S, Menini A, Tirindelli R. Vomeronasal receptors and signal transduction in the vomeronasal organ of mammals. In: Mucignat-Caretta C, editor. Neurobiology of Chemical Communication. Frontiers in Neuroscience. Boca Raton (FL)2014.
    [61] Matsunami H, Buck LB. A multigene family encoding a diverse array of putative pheromone receptors in mammals. Cell. 1997;90(4):775-84.
    [62] Herrada G, Dulac C. A novel family of putative pheromone receptors in mammals with a topographically organized and sexually dimorphic distribution. Cell. 1997;90(4):763-73.
    [63] Zhang ZC, Sakuma A, Kuraku S, Nikaido M. Remarkable diversity of vomeronasal type 2 receptor (OlfC) genes of basal ray-finned fish and its evolutionary trajectory in jawed vertebrates. Sci Rep-Uk. 2022;12(1).
    [64] Brykczynska U, Tzika AC, Rodriguez I, Milinkovitch MC. Contrasted evolution of the vomeronasal receptor repertoires in mammals and squamate reptiles. Genome Biol Evol. 2013;5(2):389-401.
    [65] Shi P, Zhang J. Comparative genomic analysis identifies an evolutionary shift of vomeronasal receptor gene repertoires in the vertebrate transition from water to land. Genome Res. 2007;17(2):166-74.
    [66] Young JM, Massa HF, Hsu L, Trask BJ. Extreme variability among mammalian V1R gene families. Genome Res. 2010;20(1):10-8.
    [67] Torres MV, Ortiz-Leal I, Sanchez-Quinteiro P. Pheromone sensing in mammals: A review of thevomeronasal system. Anatomia. 2023;2(4):346-413.
    [68] Swaney WT, Keverne EB. The evolution of pheromonal communication. Behav Brain Res. 2009;200(2):239-47.
    [69] Hatanaka T, Matsuzaki O. Odor responses of the vomeronasal system in Reeve's turtle, Geoclemys reevesii. Brain Behav Evol. 1993;41(3-5):183-6.
    [70] Bufe B, Schumann T, Zufall F. Formyl peptide receptors from immune and vomeronasal system exhibit distinct agonist properties. J Biol Chem. 2012;287(40):33644-55.
    [71] Dietschi Q, Tuberosa J, Fodoulian L, et al. Clustering of vomeronasal receptor genes is required for transcriptional stability but not for choice. Sci Adv. 2022;8(46):eabn7450.
    [72] Green PA, Van Valkenburgh B, Pang B, et al. Respiratory and olfactory turbinal size in canid and arctoid carnivorans. J Anat. 2012;221(6):609-21.
    [73] Bird DJ, Murphy WJ, Fox-Rosales L, et al. Olfaction written in bone: cribriform plate size parallels olfactory receptor gene repertoires in Mammalia. Proc Biol Sci. 2018;285(1874).
    [74] Ribeiro PF, Manger PR, Catania KC, et al. Greater addition of neurons to the olfactory bulb than to the cerebral cortex of eulipotyphlans but not rodents, afrotherians or primates. Front Neuroanat. 2014;8:23.
    [75] Liao BY, Weng MP. Unraveling the association between mRNA expressions and mutant phenotypes in a genome-wide assessment of mice. Proc Natl Acad Sci U S A. 2015;112(15):4707-12.
    [76] Grus WE, Zhang J. Distinct evolutionary patterns between chemoreceptors of 2 vertebrate olfactory systems and the differential tuning hypothesis. Mol Biol Evol. 2008;25(8):1593-601.
    [77] Scalia F, Winans SS. The differential projections of the olfactory bulb and accessory olfactory bulb in mammals. J Comp Neurol. 1975;161(1):31-55.
    [78] Garrett EC, Steiper ME. Strong links between genomic and anatomical diversity in both mammalian olfactory chemosensory systems. P Roy Soc B-Biol Sci. 2014;281(1783).
    [79] Oelschläger HA. Development of the olfactory and terminalis systems in whales and dolphins. In: Doty RL, Müller-Schwarze D, editors. Chemical Signals in Vertebrates 6. Boston, MA: Springer US; 1992. p. 141-147.
    [80] Dorries KM, Adkins-Regan E, Halpern BP. Olfactory sensitivity to the pheromone, androstenone, is sexually dimorphic in the pig. Physiol Behav. 1995;57(2):255-9.
    [81] Belluscio L, Gold GH, Nemes A, Axel R. Mice deficient in G(olf) are anosmic. Neuron. 199;20(1):69-81.
    [82] Spehr M, Spehr J, Ukhanov K, et al. Parallel processing of social signals by the mammalian main and accessory olfactory systems. Cell Mol Life Sci. 2006;63(13):1476-84.
    [83] Fedorov A, Beichel R, Kalpathy-Cramer J, et al. 3D Slicer as an image computing platform for the Quantitative Imaging Network. Magn Reson Imaging. 2012;30(9):1323-1341.
    [84] R Core Team R. R: A language and environment for statistical computing. 2013.
    [85] Cunningham F, Allen JE, Allen J, et al. Ensembl 2022. Nucleic Acids Res. 2022;50(D1):D988-D995.
    [86] Mudunuri U, Che A, Yi M, Stephens RM. bioDBnet: the biological database network. Bioinformatics. 2009;25(4):555-556.
    [87] Mistry J, Chuguransky S, Williams L, et al. Pfam: The protein families database in 2021. Nucleic Acids Research. 2021;49(D1):D412-D419.
    [88] Eddy SR. Accelerated Profile HMM Searches. PLoS Comput Biol. 2011;7(10):e1002195.
    [89] Niimura Y, Nei M. Extensive gains and losses of olfactory receptor genes in mammalian evolution. PLoS One. 2007;2(8):e708.
    [90] Ji YP, Zhang Z, Hu YH. The repertoire of G-protein-coupled receptors in. Bmc Genomics. 2009;10.
    [91] Villamayor PR, Robledo D, Fernández C, et al. Analysis of the vomeronasal organ transcriptome reveals variable gene expression depending on age and function in rabbits. Genomics. 2021;113(4):2240-2252.
    [92] Camacho C, Coulouris G, Avagyan V, et al. BLAST+: architecture and applications. BMC Bioinformatics. 2009;10:421.
    [93] Emms DM, Kelly S. OrthoFinder: solving fundamental biases in whole genome comparisons dramatically improves orthogroup inference accuracy. Genome Biol. 2015;16(1):157.
    [94] Krogh A, Larsson B, von Heijne G, Sonnhammer EL. Predicting transmembrane protein topology with a hidden Markov model: application to complete genomes. J Mol Biol. 2001;305(3):567-80.
    [95] Rodriguez I, Del Punta K, Rothman A, et al. Multiple new and isolated families within the mouse superfamily of V1r vomeronasal receptors. Nat Neurosci. 2002;5(2):134-40.
    [96] Paysan-Lafosse T, Blum M, Chuguransky S, et al. InterPro in 2022. Nucleic Acids Res. 2023;51(D1):D418-D427.
    [97] Zhang Z, Carriero N, Zheng D, et al. PseudoPipe: an automated pseudogene identification pipeline. Bioinformatics. 2006;22(12):1437-9.
    [98] Huerta-Cepas J, Serra F, Bork P. ETE 3: Reconstruction, analysis, and visualization of phylogenomic data. Mol Biol Evol. 2016;33(6):1635-8.
    [99] Bansal MS, Kellis M, Kordi M, Kundu S. RANGER-DTL 2.0: rigorous reconstruction of gene-family evolution by duplication, transfer and loss. Bioinformatics. 2018;34(18):3214-3216.
    [100] Tamura K, Stecher G, Kumar S. MEGA11: Molecular evolutionary genetics analysis version 11. Molecular Biology and Evolution. 2021;38(7):3022-3027.
    [101] Chen K, Durand D, Farach-Colton M. NOTUNG: a program for dating gene duplications and optimizing gene family trees. J Comput Biol. 2000;7(3-4):429-47.
    [102] Duchemin W, Gence G, Chifolleau AMA, et al. RecPhyloXML: a format for reconciled gene trees. Bioinformatics. 2018;34(21):3646-3652.
    [103] Ackels T, Drose DR, Spehr M. In-depth physiological analysis of defined cell populations in acute tissue slices of the mouse vomeronasal organ. J Vis Exp. 2016;115.
    [104] Chen S, Zhou Y, Chen Y, Gu J. fastp: an ultra-fast all-in-one FASTQ preprocessor. Bioinformatics. 2018;34(17):i884-i890.
    [105] Kim D, Paggi JM, Park C, et al. Graph-based genome alignment and genotyping with HISAT2 and HISAT-genotype. Nat Biotechnol. 2019;37(8):907-915.
    [106] Danecek P, Bonfield JK, Liddle J, et al. Twelve years of SAMtools and BCFtools. Gigascience. 2021;10(2).
    [107] Pertea M, Pertea GM, Antonescu CM, et al. StringTie enables improved reconstruction of a transcriptome from RNA-seq reads. Nat Biotechnol. 2015;33(3):290-5.
    [108] Dawley EM. Species, sex, and seasonal differences in VNO size. Microsc Res Tech. 1998;41(6):506-18.
    [109] Garrett EC. Was there a sensory trade-off in primate evolution? The vomeronasal groove as a means of understanding the vomeronasal system in the fossil record. CUNY Academic. 2015.
    [110] Weiler E. Postnatal development of the rat vomeronasal organ. Chem Senses. 2005;30 Suppl 1:i127-8.
    [111] Rodriguez I, Mombaerts P. Novel human vomeronasal receptor-like genes reveal species-specific families. Curr Biol. 2002;12(12):R409-11.
    [112] Yang H, Shi P, Zhang YP, Zhang J. Composition and evolution of the V2r vomeronasal receptor gene repertoire in mice and rats. Genomics. 2005;86(3):306-15.
    [113] Grus WE, Zhang J. Origin of the genetic components of the vomeronasal system in the common ancestor of all extant vertebrates. Mol Biol Evol. 2009 ;26(2):407-19.
    [114] Park SH, Podlaha O, Grus WE, Zhang J. The microevolution of V1r vomeronasal receptor genes in mice. Genome Biol Evol. 2011;3:401-12.
    [115] Miller CH, Campbell P, Sheehan MJ. Distinct evolutionary trajectories of V1R clades across mouse species. BMC Evol Biol. 2020;20(1):99.
    [116] Kowatschew D, Korsching SI. Lamprey possess both V1R and V2R olfactory receptors, but only V1Rs are expressed in olfactory sensory neurons. Chem Senses. 2022;47.
    [117] Henningsson S, Hovey D, Vass K, et al. A missense polymorphism in the putative pheromone receptor gene VN1R1 is associated with sociosexual behavior. Transl Psychiatry. 2017;7(4):e1102.
    [118] Ibarra-Soria X, Levitin MO, Saraiva LR, Logan DW. The olfactory transcriptomes of mice. PLoS Genet. 2014;10(9):e1004593.
    [119] Hohenbrink P, Radespiel U, Mundy NI. Pervasive and ongoing positive selection in the vomeronasal-1 receptor (V1R) repertoire of mouse lemurs. Mol Biol Evol. 2012 Dec;29(12):3807-16.
    [120] Zhang J, Webb DM. Evolutionary deterioration of the vomeronasal pheromone transduction pathway in catarrhine primates. Proc Natl Acad Sci U S A. 2003;100(14):8337-41.
    [121] Wang G, Zhu Z, Shi P, Zhang Y. Comparative genomic analysis reveals more functional nasal chemoreceptors in nocturnal mammals than in diurnal mammals. Chinese Science Bulletin.2010;55(34):3901-3910.
    [122] Webb DM, Cortes-Ortiz L, Zhang J. Genetic evidence for the coexistence of pheromone perception and full trichromatic vision in howler monkeys. Mol Biol Evol. 2004;21(4):697-704.
    [123] Lacey EA. Life underground: the biology of subterranean rodents. University of Chicago Press; 2000.
    [124] Wang G, Shi P, Zhu Z, Zhang YP. More functional V1R genes occur in nest-living and nocturnal terricolous mammals. Genome Biol Evol. 2010;2:277-83.
    [125] Jiao H, Hong W, Nevo E, et al. Convergent reduction of V1R genes in subterranean rodents. BMC Evolutionary Biology. 2019;19(1):176.
    [126] Blanchong JA, Smale L. Temporal Patterns of Activity of the Unstriped Nile Rat, Arvicanthis niloticus. Journal of Mammalogy. 2000;81(2):595-599.
    [127] Arvicanthis niloticus (Desmarest, 1822) in GBIF Secretariat (2023). GBIF Backbone Taxonomy; Checklist dataset https://doi.org/10.15468/39omei accessed via GBIF.org on 2024.
    [128] Mus musculus Linnaeus, 1758 in GBIF Secretariat (2023). GBIF Backbone Taxonomy; Checklist dataset https://doi.org/10.15468/39omei accessed via GBIF.org on 2024
    [129] St. John, J. 2005. "Arvicanthis niloticus" (On-line). Animal Diversity Web; Accessed 2024 at https://animaldiversity.org/accounts/Arvicanthis_niloticus/.
    [130] Castillo-Ruiz A, Indic P, Schwartz WJ. Time management in a co-housed social rodent species (Arvicanthis niloticus). Sci Rep. 2018;8(1):1202.
    [131] Ueno H, Takahashi Y, Mori S, et al. Mice recognise mice in neighbouring rearing cages and change their social behaviour. Behav Neurol. 2024:9215607.
    [132] Schweinfurth MK. The social life of Norway rats (Rattus norvegicus). Elife. 2020;9.
    [133] Zhang JX, Liu YJ, Zhang JH, Sun L. Dual role of preputial gland secretion and its major components in sex recognition of mice. Physiol Behav. 2008;95(3):388-94.
    [134] Hudson R, Distel H. Pheromonal release of suckling in rabbits does not depend on the vomeronasal organ. Physiol Behav. 1986;37(1):123-8.
    [135] Dorries KM, Adkins-Regan E, Halpern BP. Sensitivity and behavioral responses to the pheromone androstenone are not mediated by the vomeronasal organ in domestic pigs. Brain Behav Evol. 1997;49(1):53-62.

    QR CODE