Journal of Guangxi Normal University(Natural Science Edition) ›› 2025, Vol. 43 ›› Issue (3): 213-225.doi: 10.16088/j.issn.1001-6600.2024040306

• Molecular Biology and Biotechnology • Previous Articles    

Molecular Evolution of FOXP2 Gene in Birds and Reptiles

KAN Tuo1,2, LIANG Xinyue1,2, CHEN Minghui1,2, FENG Ping1,2*   

  1. 1. Key Laboratory of Ecology of Rare and Endangered Species and Environmental Protection (Guangxi Normal University), Ministry of Education, Guilin Guangxi 541006, China;
    2. College of Life Sciences, Guangxi Normal University, Guilin Guangxi 541006, China
  • Received:2024-04-03 Revised:2024-05-11 Online:2025-05-05 Published:2025-05-14

Abstract: FOXP2 gene of Fox family widely exists in the animal kingdom and is an important gene related to sound. Its mutation can cause human language disorder. FOXP2 gene is closely related to the language ability and learning behavior of birds and reptiles. In order to understand its evolutionary history, 66 species of birds and 30 species of reptiles were studied. Based on genomic data, the molecular evolution of FOXP2 gene in birds and reptiles was discussed by using selection pressure analysis and phylogenetic analysis. The results showed that: first, although both birds and reptiles had positive selection sites, FOXP2 gene was very conserved in reptiles and birds, and showed purifying selection on the whole; second, the FOXP2 gene of songbirds in birds did not undergo positive selection evolution, and there was no positive selection site, but the ω value was larger than that of other birds, indicating that the evolution rate of FOXP2 gene in songbirds is faster, which may be related to its outstanding singing ability; third, although FOXP2 of both birds and reptiles were under purifying selection, birds havd greater ω, indicating that birds were under relaxed selection and the FOXP2 gene of birds had a faster evolution rate than that of reptiles. The results of this study provide further theoretical basis for the study of the evolution and function of FOXP2 gene, and bring reference and enlightenment to the exploration of human language mechanism.

Key words: FOXP2, birds, reptiles, songbirds, select pressure analysis, phylogenetic analysis

CLC Number:  Q959.1
[1] HANNENHALLI S, KAESTNER K H. The evolution of Fox genes and their role in development and disease[J]. Nature Reviews Genetics, 2009, 10(4): 233-240. DOI: 10.1038/nrg2523.
[2]LAM E W F, BROSENS J J, GOMES A R, et al. Forkhead box proteins: tuning forks for transcriptional harmony[J]. Nature Reviews Cancer, 2013, 13(7): 482-495. DOI: 10.1038/nrc3539.
[3]VAGLIETTI S, VILLERI V, DELL’OCA M, et al.PolyQ length-based molecular encoding of vocalization frequency in FOXP2[J]. iScience, 2023, 26(10): 108036. DOI: 10.1016/j.isci.2023.108036.
[4]MOUSSAOUI B, ULMER K, ARAYA-SALAS M, et al. Persistent vocal learning in an aging open-ended learner reflected in neural FoxP2 expression[J]. BMC Neuroscience, 2024, 25(1): 31. DOI: 10.1186/s12868-024-00879-8.
[5]李东风. 人类语言起源之谜[J]. 生物学通报, 2021, 56(5): 6-9. DOI: 10.3969/j.issn.0006-3193.2021.05.002.
[6]CHE F Y, LI C H, ZHANG L Y, et al. Novel FOXP2 variant associated with speech and language dysfunction in a Chinese family and literature review[J]. Journal of Applied Genetics, 2024, 65(2): 367-373. DOI: 10.1007/s13353-024-00849-0.
[7]HAESLER S, WADA K, NSHDEJAN A, et al. FoxP2 expression in avian vocal learners and non-learners[J]. Journal of Neuro Science, 2004, 24(13): 3164-3175. DOI: 10.1523/JNEUROSCI.4369-03.2004.
[8]NUDEL R, NEWBURY D F. FOXP2[J]. Wiley Interdisciplinary Reviews-Cognitive Science, 2013, 4(5): 547-560. DOI: 10.1002/wcs.1247.
[9]FISHER S E. On genes, speech, and language[J]. New England Journal of Medicine, 2005, 353(16): 1655-1657. DOI: 10.1056/NEJMp058207.
[10]李慧. Foxp2小鼠模型中发育性言语障碍的分子遗传学研究[J]. 实验动物与比较医学, 2019,39(4): 331-336. DOI: 10.3969/j.issn.1674-5817.2019.04.015.
[11]VON MERTEN S, PFEIFLE C, KÜNZEL S. A humanized version of Foxp2 affects ultrasonic vocalization in adult female and male mice[J]. Genes, Brain and Behavior, 2021, 20(7): e12764. DOI: 10.1111/gbb.12764.
[12]VERNES S C, WILKINSON G S. Behaviour, biology and evolution of vocal learning in bats[J]. Philosophical Transactions of the Royal Society B: Biological Sciences, 2020, 375(1789): 20190061. DOI: 10.1098/rstb.2019.0061.
[13]MCGEE R M. Quantifying over expression of FoxP2 in the brain of budgerigars using immunohistochemistry[J]. The FASEB Journal, 2020, 34(S1): 1. DOI: 10.1096/fasebj.2020.34.s1.06062.
[14]杨利琼, 谢君, 刘昉昉, 等. 鸟类鸣叫及生物学意义的研究现状[J]. 实验动物与比较医学, 2019, 39(1): 77-82. DOI: 10.3969/j.issn.1674-5817.2019.01.015.
[15]BESSHO C, YAMADA S, TANIDA T, et al. FoxP2 protein decreases at a specific region in the chick midbrain after hatching[J]. Neuroscience Letters, 2023, 800: 137119. DOI: 10.1016/j.neulet.2023.137119.
[16]ROSSETTO F, LAIOLO P. Potential social facilitation through song in bird communities[J]. Behavioral Ecology and Sociobiology, 2024, 78(1): 10. DOI: 10.1007/s00265-023-03427-2.
[17] BALLENTINE B, HYMAN J, NOWICKI S. Vocal performance influences female response to male bird song: an experimental test[J]. Behavioral Ecology, 2004, 15(1): 163-168. DOI: 10.1093/beheco/arg090.
[18] SEARCY W A, ANDERSON R C, NOWICKI S. Bird song as a signal of aggressive intent[J].Behavioral Ecolology Sociobiolology, 2006, 60(2): 234-241. DOI: 10.1007/s00265-006-0161-9.
[19]ZHANG Y T, ZHOU L F, ZOU J G, et al. Analogies of human speech and bird song: from vocal learning behavior to its neural basis[J]. Frontiers in Psychology, 2023, 14:1100969. DOI: 10.3389/fpsyg.2023.1100969.
[20]SHI Z M, ZHANG Z Y, SCHAFFER L, et al. Dynamic transcriptome landscape in the song nucleus HVC between juvenile and adult zebra finches[J]. Advance in Genetics, 2021, 2(1): e10035. DOI: 10.1002/ggn2.10035.
[21] TEN DONKELAAR H J. Reptiles[M]//NIEUWENHUYS R, DONKELAAR H J, NICHOLSON C. THE Central Nervous System of Vertebrates. Berlin: Springer, 1998:1315-1524.
[22] GANS C, MADERSON P F A. Sound producing mechanisms in recent reptiles: review and comment[J]. American Zoologist, 1973, 13(4): 1195-1203. DOI: 10.1093/icb/13.4.1195.
[23] PINCHEIRA-DONOSO D, BAUER A M, MEIRI S, et al. Global taxonomic diversity of living reptiles[J]. PLoS One, 2013, 8(3): e59741. DOI: 10.1371/journal.pone.0059741.
[24] LI G, WANG J H, ROSSITER S J. Accelerated FoxP2 evolution in echolocating bats[J]. PLoS One, 2007, 2(9): e900. DOI: 10.1371/journal.pone.0000900.
[25] CLARK A G, GLANOWSKI S, NIELSEN R, et al. Inferring nonneutral evolution from human-chimp-mouse orthologous gene trios[J]. Science, 2003, 302(5652): 1960-1963. DOI: 10.1126/science.1088821.
[26] TIWARY B K. The cognitive and speech genes are jointly shaped by both positive and relaxed selection in the human lineage[J]. Genomics, 2020, 112(5): 2922-2927. DOI: 10.1016/j.ygeno.2020.05.006.
[27] FISHBEIN A R, IDSARDI W J, BALL G F, et al. Sound sequences in birdsong: how much do birds really care?[J]. Philosophical Transactions of the Royal Society B: Biological Sciences, 2020, 375(1789): 20190044. DOI: 10.1098/rstb.2019.0044.
[28]王青青, 陆文康, 王萍, 等. 5种鸟类FoxP2的分子进化分析[J]. 生物学杂志, 2017,34(5): 29-33. DOI: 10.3969/j.issn.2095-1736.2017.05.029.
[29] FERRARA C R, VOGT R C, SOUSA-LIMA R S. Turtle vocalizations as the first evidence of posthatching parental care in chelonians[J]. Journal of Comparative Psychology, 2013, 127(1): 24-32. DOI: 10.1037/a0029656.
[30] LACROIX C, DAVY C M, ROLLINSON N. Hatchling vocalizations and beneficial social interactions in subterranean nests of a widespread reptile[J]. Animal Behaviour, 2022, 187: 233-244. DOI: 10.1016/j.anbehav.2022.03.006.
[31] TANG Y Z, PIAO Y S, ZHUANG L Z, et al. Expression of androgen receptor mRNA in the brain of Gekko gecko: implications for understanding the role of androgens in controlling auditory and vocal processes[J]. The Journal of Comparative Neurology, 2001, 438(2): 136-147. DOI: 10.1002/cne.1305.
[32] SCHARFF C, HAESLER S. An evolutionary perspective on FoxP2: strictly for the birds?[J]. Current Opinion in Neurobiology, 2005, 15(6): 694-703. DOI: 10.1016/j.conb.2005.10.004.
[33]ABE K, MATSUI S, WATANABE D. Transgenic songbirds with suppressed or enhanced activity of CREB transcription factor[J]. Proceedings of the National Academy of Sciences of the United States of America, 2015, 112(24): 7599-7604. DOI: 10.1073/pnas.1413484112.
[34] MENDOZA E, TOKAREV K, DÜRING D N, et al. Differential coexpression of FoxP1, FoxP2, and FoxP4 in the zebra finch (Taeniopygia guttata) song system[J]. Journal of Comparative Neurology, 2015, 523(9): 1318-1340. DOI: 10.1002/cne.23731.
[35] PHILLMORE L S, MACGILLIVRAY H L, WILSON K R, et al. Effects of sex and seasonality on the song control system and FoxP2 protein expression in black-capped chickadees (Poecile atricapillus)[J]. Developmental Neurobiology, 2015, 75(2): 203-216. DOI: 10.1002/dneu.22220.
[36]XIAO L, MERULLO D P, KOCH T M I, et al. Expression of FoxP2 in the basal ganglia regulates vocal motor sequences in the adult songbird[J]. Nature Communications, 2021, 12(1): 2617. DOI: 10.1038/s41467-021-22918-2.
[37] CASTELLUCCI G A, CALBICK D, MCCORMICK D. The temporal organization of mouse ultrasonic vocalizations[J]. PLoS One, 2018, 13(10): e0199929. DOI: 10.1371/journal.pone.0199929.
[38] TERAMITSU I, WHITE S A. FoxP2 regulation during undirected singing in adult songbirds[J]. The Journal of Neuroscience, 2006, 26(28): 7390-7394. DOI: 10.1523/JNEUROSCI.1662-06.2006.
[39]MURUGAN M, HARWARD S, SCHARFF C, et al. Diminished FoxP2 levels affect dopaminergic modulation of corticostriatal signaling important to Song variability[J]. Neuron, 2013, 80(6): 1464-1476. DOI: 10.1016/j.neuron.2013.09.021.
[40] FISCH G S, FLINT J. Transgenic and knockout models of neuropsychiatric disorders[M]. Totowa NJ: Humana Press, 2006. DOI: 10.1007/978-1-59745-058-4.
[1] WU Ranxin, YU Tailin, FENG Changzhang, MA Yujun, ZHANG Gang. Diversity of Migratory Birds in Jiuwan Mountain, Guangxi, China [J]. Journal of Guangxi Normal University(Natural Science Edition), 2020, 38(1): 140-148.
Viewed
Full text


Abstract

Cited

  Shared   
  Discussed   
[1] YUAN Hong, WANG Xiaodong, WEI Xiuying, WANG Jiapin, CHEN Yifang, YAO Hongyan, CHEN Dunxue. Molecular Characterization of Circadian Clock Gene from Giant Spiny Frogs (Quasipaa spinosa) and Its Transcriptional Regulation During Different Developmental Stages[J]. Journal of Guangxi Normal University(Natural Science Edition), 2025, 43(3): 201 -212 .