群体基因组分析揭示短耳犬蝠适应城市化的遗传学基础

doi:10.16829/j.slxb.150824

摘要/Abstract

摘要： 短耳犬蝠(Cynopterus brachyotis)是栖息在城市的典型蝙蝠物种。已发表的研究表明，短耳犬蝠的遗传多样性显著降低与快速城市化紧密相关，但该物种适应城市环境的遗传学基础仍缺乏研究。本研究基于已发表的短耳犬蝠历史样本(1931年)和当代样本(2011—2012年)的群体基因组重测序数据，通过位点突变频率、基于群体遗传分化的选择信号检测方法、基于单倍型的选择信号检测方法和受选择基因座检测方法，探究了快速城市化对短耳犬蝠的影响及其适应城市化的遗传学基础。研究结果表明：短耳犬蝠历史群体中鉴定到669个受选择基因，基因功能富集主要集中在视觉和嗅觉等通路；在当代群体中鉴定到2 013个受选择基因，这些基因除了参与视觉和嗅觉相关通路外，还在免疫、味觉和听觉等通路中发挥作用。该结果提示，快速城市化可能影响短耳犬蝠的感官系统和免疫系统；为了适应快速城市化，短耳犬蝠可能在免疫、味觉和听觉等功能方面发生了适应性演化。

关键词: 短耳犬蝠, 城市化, 群体基因组, 选择信号

Abstract: The lesser short-nosed fruit bat (Cynopterus brachyotis) is a bat species commonly found in urban areas. A published study showed that rapid urbanization has led to a significant decrease in genetic diversity in this fruit bat. However, the genetic mechanisms underlying this species’ adaptations to urban environments have not been investigated. Based on the published population genome resequencing data from historical samples collected in 1931 and contemporary samples from 2011 - 2012, this study investigated the effects of rapid urbanization on the lesser shortnosed fruit bat and the genetic basis of adaptations to urbanization, using four methods (allele frequency analysis, selection signal detection based on population genetic differentiation, selection signal detection based on haplotypes, and detection of selected loci). Our results show that 669 selected genes were identified in the historical population and these genes were functionally enriched in visual and olfactory pathways. In contrast, 2 013 selected genes were identified in the contemporary population and these genes were enriched in immune, gustatory, and auditory pathways in addition to visual and olfactory-related pathways. These results suggest that rapid urbanization may have affected multiple sensory systems and immune systems in this species. Therefore, adaptive molecular evolution of immune, gustatory, and auditory genes may have occurred in C. brachyotis in response to rapid urbanization.

Key words: Cynopterus brachyotis, Urbanization, Population genomics, Selection signals

中图分类号:

Q346.4

王菲, 赵华斌. 群体基因组分析揭示短耳犬蝠适应城市化的遗传学基础[J]. 兽类学报, 2023, 43(6): 644-651.

WANG Fei, ZHAO Huabin. Population genomic analysis revealed the genetic basis of adaptations to urbanization in the lesser short-nosed fruit bat (Cynopterus brachyotis)[J]. ACTA THERIOLOGICA SINICA, 2023, 43(6): 644-651.

参考文献

Ashburner M, Ball C A, Blake J A, Botstein D, Butler H, Cherry J M, Davis A P, Dolinski K, Dwight S S, Eppig J T, Harris M A, Hill D P, Issel-Tarver L, Kasarskis A. 2000. Gene ontology: tool for the unification of biology. Nature Genetics, 25 (1): 25-29.
Bachmano A, Beauchamp G. 2007. Taste receptor genes. Annual Review of Nutrition, 27 (1): 389-414.
Bayat S, Geiser F, Kristiansen P, Wilson S C. 2014. Organic contaminants in bats: trends and new issues. Environment International, 63 (37): 40-52.
Chan A A Q, Aziz S A, Clare E L, Coleman J L. 2021. Diet, ecological role and potential ecosystem services of the fruit bat, Cynopterus brachyotis, in a tropical city. Urban Ecosystems, 24 (2):251-263.
Chattopadhyay B, Garg K M, Mendenhall I H, Rheindt F E. 2019. Historic reveals Anthropocene threat to a tropical urban fruit bat. Current Biology, 29 (24): R1299-R1300.
Chen C, Liu Z G, Pan Q, Chen X, Wang H H, Guo H K, Liu S D, Lu H F, Tian S L, Li R Q, Shi W. 2016. Genomic analyses reveal demographic history and temperate adaptation of the newly discovered honey bee subspecies Apis mellifera sinisxinyuan n. ssp. Molecular Biology and Evolution, 33 (5): 1337-1348.
Chen S F, Zhou Y Q, Chen Y R, Gu J. 2018. fastp: an ultra-fast all-in-one FASTQ preprocessor. Bioinformatics, 34 (17): i884-i890.
Corlett R T. 2015. The anthropocene concept in ecology and conservation. Trends in Ecology & Evolution, 30 (1): 36-41.
Crutzen P J. 2002. Geology of mankind. Nature, 415 (6867): 23.
Danecek P, Auton A, Abecasis G, Albers C A, Banks E, DePristo M A, Handsaker R E, Lunter G, Marth G T, Sherry S T, McVean G, Durbin R. 2011. The variant call format and VCFtools. Bioinformatics, 27 (15): 2156-2158.
Daniel C, Salvekar A, Schindler U. 2000. A gain-of-function mutation in STAT6. Journal of Biological Chemistry, 275 (19): 14255-14259.
DeSimone J A, Lyall V, Heck G L, Feldman G M. 2001. Acid detection by taste receptor cells. Respiration Physiology, 129 (1-2):231-245.
Dirzo R, Young H S, Galetti M, Ceballos G, Isaac N J B, Collen B. 2014. Defaunation in the anthropocene. Science, 345 (6195):401-406.
Excoffier L, Lischer H E L. 2010. Arlequin suite ver 3. 5: a new series of programs to perform population genetics analyses under Linux and Windows. Molecular Ecology Resources, 10 (3):564-567.
Fabregat A, Sidiropoulos K, Viteri G, Forner O, Marin-Garcia P, Arnau V, D’ Eustachio P, Stein L, Hermjakob H. 2017. Reactome pathway analysis: a high-performance in-memory approach. Bioinformatics, 18 (1): 142.
Fahrig L. 2003. Effects of habitat fragmentation on biodiversity. Annual Review of Ecology, Evolution, and Systematics, 34 (7):487-515.
Frick W F, Kingston T, Flanders J. 2020. A review of the major threats and challenges to global bat conservation. Annals of the New York Academy of Sciences, 1469 (1): 5-25.
Gaisler J, Zukal J, Rehak Z, Homolka M. 1998. Habitat preference and flight activity of bats in a city. Journal of Zoology, 244 (3):439-445.
Glikson A. 2016. Cenozoic mean greenhouse gases and temperature changes with reference to the Anthropocene. Global Change Biology, 22 (12): 3843-3858.
Harris S E, Munshi-South J. 2017. Signatures of positive selection and local adaptation to urbanization in white-footed mice (Peromyscus leucopus). Molecular Ecology, 26 (22): 6336-6350.
Hem S, Gherardini P F, Fortéa J O Y, Hourdel V, Morales M A, Watanabe R, Pescher P, Kuzyk M A, Smith D, Borchers C H, Zilberstein D, Helmer-Citterich M, Namane A, Späth G F. 2011. Identification of Leishmania-specific protein phosphorylation sites by LC-ESI-MS/MS and comparative genomics analyses. Proteomics, 10 (21): 3868-3883.
Jung K, Kalko E K V. 2011. Adaptability and vulnerability of high flying Neotropical aerial insectivorous bats to urbanization. Diversity and Distributions, 17 (2): 262-274.
Kanehisa M, Goto S. 2000. KEGG: Kyoto Encyclopedia of Genes and Genomes. Nucleic Acids Research, 28 (1): 27-30.
Korine C, Kalko E K V. 2005. Fruit detection and discrimination by small fruit-eating bats (Phyllostomidae): echolocation call design and olfaction. Behavioral Ecology and Sociobiology, 59 (1):12-23.
Li H, Handsaker B, Wysoker A, Fennell T, Ruan J, Homer N, Marth G, Abecasis G, Durbin R. 2009. The sequence alignment/map format and SAMtools. Bioinformatics, 25 (16): 2078-2079.
Lilley T M, Stauffer J, Kanerva M, Eeva T. 2014. Interspecific variation in redox status regulation and immune defence in five bat species: the role of ectoparasites. Oecologia, 175 (3): 811-823.
Meyerhof W, Batram C, Kuhn C, Brockhoff A, Chudoba E, Bufe B, Appendino G, Behrens M. 2010. The molecular receptive ranges of human TAS2R bitter taste receptors. Chemical Senses, 35 (2):157-170.
Munshi-South J, Zolnik C P, Harris S E. 2016. Population genomics of the Anthropocene: Urbanization is negatively associated with genome-wide variation in white-footed mouse populations. Evolutionary Applications, 9 (4): 546-564.
Page R A, ter Hofstede H M. 2021. Sensory and cognitive ecology of bats. Annual Review of Ecology, Evolution, and Systematics, 52(1): 541.
Patterson B D, Dick C W, Dittmar K. 2007. Roosting habits of bats affect their parasitism by bat flies (Diptera: Streblidae). Journal of Tropical Ecology, 23 (2): 177-189.
Qiu Q, Wang L Z, Wang K, Yang Y Z, Ma T, Wang Z F, Zhang X, Ni Z Q, Hou F F, Long R J, Abbott R, Lenstra J, Liu J Q. 2015. Yak whole-genome resequencing reveals domestication signatures and prehistoric population expansions. Nature Communications, 6 (1): 10283.
Sabeti P C, Varilly P, Fry B, Lohmueller J, Hostetter E, Cotsapas C, Xie X, Byrne E H, McCarroll S A, Gaudet R, Schaffner S F, Lander E S, Frazer K A. 2007. Genome-wide detection and characterization of positive selection in human populations. Nature, 449 (7164): 913-918.
Schneeberger K, Czirják G Á, Voigt C C. 2013. Inflammatory challenge increases measures of oxidative stress in a free-ranging, long-lived mammal. Journal of Experimental Biology, 216 (24):4514-4519.
Sengupta S, Mondal M, Basu P. 2014. Bird species assemblages across a rural urban gradient around Kolkata, India. Urban Ecosystems, 17 (2): 585-596.
She R, Chu J S C, Uyar B, Wang J, Wang K, Chen N S. 2011. GenBlastG: using BLAST searches to build homologous gene models. Bioinformatics, 27 (15): 2141-2143.
Siemers B M, Schaub A. 2011. Hunting at the highway: traffic noise reduces foraging efficiency in acoustic predators. Proceedings of the Royal Society of London Series B-Biological Sciences, 278(1712): 1646-1652.
Spann M F, Blondell J M, Hunting K L. 2000. Acute hazards to young children from residential pesticide exposures. American Journal of Public Health, 90 (6): 971-973.
Stone E L, Jones G, Harris S. 2009. Street lighting disturbs commuting bats. Current Biology, 19 (13): 1123-1127.
Suzuki T, Hidaka T, Kumagai Y, Yamamoto M. 2020. Environmental pollutants and the immune response. Nature Immunology, 21(12): 1486-1495.
Szpiech Z A, Hernandez R D. 2014. selscan: An efficient multithreaded program to perform EHH-based scans for positive selection. Molecular Biology and Evolution, 31 (10): 2824-2827.
Vidler A. 2021. Exterranean: extraction in the humanist Anthropocene. Journal of the Society of Architectural Historians, 80 (2):221-222.
Vitousek P M, Mooney H A, Lubchenco J, Melillo J M. 1997. Human domination of earth’s ecosystems. Science, 277 (5325):494-499.
Weir B S, Cockerham C C. 1984. Estimating F-statistics for the analysis of population structure. Evolution, 38 (6): 1358-1370.
Xu H B, Luo X, Qian J, Pang X H, Song J Y, Qian G R, Chen J H, Chen S L. 2012. FastUniq: A fast de novo duplicates removal tool forpaired short reads. PLoS ONE, 7 (12): e52249.
Zhang H, Liang Q Q, Wang N, Wang Q G, Leng L, Mao J, Wang Y X, Wang S Z, Zhang J Y, Liang H, Zhou X, Li Y M, Cao Z P, Luan P, Wang Z P, Yuan H, Wang Z Q, Zhou X M, Lamont S J, Da Y, Li R Q, Tian S L, Du Z Q, Li H. 2020. Microevolutionary dynamics of chicken genomes under divergent selection for adiposity. iScience, 23 (6): 101193.
Zhao H B, Rossiter S J, Teeling E C, Li C J, Cotton J A, Zhang S Y. 2009. The evolution of color vision in nocturnal mammals. Proceedings of the National Academy of Sciences of the United States of America, 106 (22): 8980-8985.
Zhou Y Y, Zhou B, Pache L, Chang M, Khodabakhshi A H, Tanaseichuk O, Benner C, Chanda S K. 2019. Metascape provides a biologist-oriented resource for the analysis of systems-level datasets. Nature Communications, 10 (1): 1523.