配偶行为相容性对动物繁殖的影响

doi:10.17520/biods.2022534

摘要/Abstract

摘要：

配对相容性(mate compatibility)常用于解释动物为何具有不同的配偶选择倾向及繁殖成功率, 涉及两性间基因、性状等的相互作用, 具体表现为配偶之间的基因、形态、行为相容性, 且直接或间接影响动物的繁殖。其中, 行为相容性受到越来越广泛的关注与研究, 主要原因是其对动物个性差异的维持与进化、物种适应环境变化的能力等均有深远影响, 但国内尚缺乏相关研究。本文主要基于以往的代表性研究结果, 对配对相容性的研究历史、定义、内容及其对动物繁殖的影响进行了简单总结和梳理, 并着重阐述了配偶行为相容性的研究进展、在进化与保护生物学等领域的研究潜力, 体现了其在动物濒危机制、种群数量恢复与维持等方面的重要意义, 有助于通过对旗舰种、伞护种的保护带动对区域内整个生态系统功能和生物多样性的保护。同时, 我们对动物配偶行为相容性未来的研究方向进行了展望, 提出工具技术革新、多学科融合以及更合理全面的实验设计可推动该领域研究在我国的发展和应用。

关键词: 行为相容性, 繁殖成功率, 动物个性, 配偶选择, 配对相容性

Abstract

Background & Aim: Mate compatibility is often used to explain why animals have different mate selection tendencies and reproductive success. It is related to the interaction of genes, traits and other aspects between the two sexes. Mate compatibility includes genetic, morphological, and behavioral compatibility, directly or indirectly affecting the reproduction of animals. In recent years, behavioral compatibility is receiving extensive attention since it is related to the maintenance and evolution of personality and the ability of species to adapt to environmental changes. However, further studies are needed on this topic in China.

Progress: Based on the representative studies over the years, we briefly review the research history and definition of mate compatibility and its impact on reproductive success. Specifically, we expound the research progress of behavioral compatibility and its development potential in evolution and conservation, so to reflect its great significance for the study of why some species become endangered and the recovery and maintenance of animal population. This could help to promote the protection of the entire ecosystem and biodiversity in the region through the protection of flagship species and umbrella species. Also, we put forward the prospect of the future research direction and improvement of techniques.

Conclusion: More attention should be paid to behavioral compatibility. The development of these fields will rely on innovations in research methods and tools, multidisciplinary integration, and rigorous experimental design.

Key words: behavioral compatibility, reproductive success, animal personality, mate choice, mate compatibility

何远思, 张轶宣, 王代平 (2023) 配偶行为相容性对动物繁殖的影响. 生物多样性, 31, 22534. DOI: 10.17520/biods.2022534.

Yuansi He, Yixuan Zhang, Daiping Wang (2023) Effects of mate behavioral compatibility on animal reproduction. Biodiversity Science, 31, 22534. DOI: 10.17520/biods.2022534.

导出引用管理器 EndNote|Ris|BibTeX

链接本文: https://www.biodiversity-science.net/CN/10.17520/biods.2022534

https://www.biodiversity-science.net/CN/Y2023/V31/I6/22534

图/表 2

参考文献 94

[1]	Anderson A (1984) Irreproducing ibis. Nature, 309, 741.
[2]	Baltz AP (1998) The assessment of reproductive potential in micronesian kingfisher pairs. Zoo Biology, 17, 425-432. DOI URL
[3]	Black JM, Choudhury S, Owen M (1996) Do barnacle geese benefit from lifelong monogamy? In: Partnerships in Birds: The Study of Monogamy (ed. Black JM), pp. 91-117. Oxford University Press, Oxford.
[4]	Both C, Dingemanse NJ, Drent PJ, Tinbergen JM (2005) Pairs of extreme avian personalities have highest reproductive success. Journal of Animal Ecology, 74, 667-674. DOI URL
[5]	Budaev SV, Zworykin DD, Mochek AD (1999) Individual differences in parental care and behaviour profile in the convict cichlid: A correlation study. Animal Behaviour, 58, 195-202. PMID
[6]	Burtka JL, Grindstaff JL (2015) Similar nest defence strategies within pairs increase reproductive success in the eastern bluebird, Sialia sialis. Animal Behaviour, 100, 174-182. DOI URL
[7]	Choudhury S (1995) Divorce in birds: A review of the hypotheses. Animal Behaviour, 50, 413-429. DOI URL
[8]	Choudhury S, Black JM, Owen M (1996) Body size, fitness and compatibility in barnacle geese Branta leucopsis. Ibis, 138, 700-709. DOI URL
[9]	Comizzoli P, Holt WV (2019) Breakthroughs and new horizons in reproductive biology of rare and endangered animal species. Biology of Reproduction, 101, 514-525. DOI PMID
[10]	Cooke F, Finney GH, Rockwell RF (1976) Assortative mating in lesser snow geese (Anser caerulescens). Behavior Genetics, 6, 127-140. PMID
[11]	Coulson JC (1966) The influence of the pair-bond and age on the breeding biology of the kittiwake gull Rissa tridactyla. The Journal of Animal Ecology, 35, 269-279. DOI URL
[12]	Coulson JC (1972) The significance of the pair-bond in the kittiwake. In: Proceedings of the 15th International Ornithological Congress (ed. Voous KH), pp. 423-433. EJ Brill, Leiden
[13]	Cunningham EJA, Birkhead TR (1998) Sex roles and sexual selection. Animal Behaviour, 56, 1311-1321. PMID
[14]	Curio E (1998) Behavior as a tool for management intervention in birds. In: Behavioral Ecology and Conservation Biology (ed. Caro TM), pp. 163-187. Oxford University Press, Oxford.
[15]	Dall SRX, Houston AI, McNamara JM (2004) The behavioural ecology of personality: Consistent individual differences from an adaptive perspective. Ecology Letters, 7, 734-739. DOI URL
[16]	Dingemanse NJ, Both C, Drent PJ, Tinbergen JM (2004) Fitness consequences of avian personalities in a fluctuating environment. Proceedings of the Royal Society B: Biological Sciences, 271, 847-852.
[17]	Dingemanse NJ, Réale D (2005) Natural selection and animal personality. Behaviour, 142, 1159-1184. DOI URL
[18]	E MJ (2017) Study on Mate Choice and Reproductive Fitness in the Yellow-rumped Flycatcher (Ficedula zanthopygia). PhD dissertation, Northeast Normal University, Changchun. (in Chinese with English abstract)
	[鄂明菊 (2017) 白眉姬鹟配偶选择与繁殖适合度研究. 博士学位论文, 东北师范大学, 长春.]
[19]	Ens BJ, Safriel UN, Harris MP (1993) Divorce in the long-lived and monogamous oystercatcher, Haematopus ostralegus: Incompatibility or choosing the better option? Animal Behaviour, 45, 1199-1217. DOI URL
[20]	Forstmeier W, Wang DP, Martin K, Kempenaers B (2021) Fitness costs of female choosiness are low in a socially monogamous songbird. PLoS Biology, 19, e3001257.
[21]	Fox RA, Millam JR (2014) Personality traits of pair members predict pair compatibility and reproductive success in a socially monogamous parrot breeding in captivity. Zoo Biology, 33, 166-172. DOI PMID
[22]	Freeman EW, Weiss E, Brown JL (2004) Examination of the interrelationships of behavior, dominance status, and ovarian activity in captive Asian and African elephants. Zoo Biology, 23, 431-448. DOI URL
[23]	Gabriel PO, Black JM (2012) Behavioural syndromes, partner compatibility and reproductive performance in Steller’s Jays. Ethology, 118, 76-86. DOI URL
[24]	Gold KC, Maple TL (1994) Personality assessment in the gorilla and its utility as a management tool. Zoo Biology, 13, 509-522. DOI URL
[25]	Gosling SD, John OP (1999) Personality dimensions in nonhuman animals: A cross-species review. Current Directions in Psychological Science, 8, 69-75. DOI URL
[26]	Grieves LA, Gloor GB, Bernards MA, MacDougall-Shackleton EA (2019) Songbirds show odour-based discrimination of similarity and diversity at the major histocompatibility complex. Animal Behaviour, 158, 131-138.
[27]	Han QH (2019) Breeding Ecology and Molecular Mechanism of Mate Choice in the Chinese Alligator. PhD dissertation, Zhejiang University, Hangzhou. (in Chinese with English abstract)
	[韩群花 (2019) 扬子鳄繁殖生态及配偶选择策略的分子机制. 博士学位论文, 浙江大学, 杭州.]
[28]	Harris MR, Siefferman L (2014) Interspecific competition influences fitness benefits of assortative mating for territorial aggression in eastern bluebirds (Sialia sialis). PLoS ONE, 9, e88668. DOI URL
[29]	Hartnett CM, Parrott ML, Mulder RA, Coulson G, Magrath MJL (2017) Opportunity for female mate choice improves reproductive outcomes in the conservation breeding program of the eastern barred bandicoot (Perameles gunnii). Applied Animal Behaviour Science, 199, 67-74. DOI URL
[30]	Harvey NC, Farabaugh SM, Woodward CD, Mccaffree K (2003) Parental care and aggression during incubation in captive California condors (Gymnogyps californianus). Bird Behavior, 15, 77-85.
[31]	Highfill L, Hanbury D, Kristiansen R, Kuczaj S, Watson S (2010) Rating vs. coding in animal personality research. Zoo Biology, 29, 509-516. DOI PMID
[32]	Ihle M (2015) Compatibility Benefits of Social and Extra-pair Mate Choice in the Zebra Finch. PhD dissertation, Ludwig-Maximilians-Universität München, Munich.
[33]	Ihle M, Kempenaers B, Forstmeier W (2015) Fitness benefits of mate choice for compatibility in a socially monogamous species. PLoS Biology, 13, e1002248.
[34]	Johnston VH, Ryder JP (1987) Divorce in larids: A review. Colonial Waterbirds, 10, 16-26. DOI URL
[35]	Johnstone RA, Manica A, Fayet AL, Stoddard MC, Rodriguez-Gironés MA, Hinde CA (2014) Reciprocity and conditional cooperation between great tit parents. Behavioral Ecology, 25, 216-222. DOI URL
[36]	Kamiya T, O’Dwyer K, Westerdahl H, Senior A, Nakagawa S (2014) A quantitative review of MHC-based mating preference: The role of diversity and dissimilarity. Molecular Ecology, 23, 5151-5163. DOI PMID
[37]	Kempenaers B (2007) Mate choice and genetic quality: A review of the heterozygosity theory. Advances in the Study of Behavior, 37, 189-278.
[38]	Kuduk K, Babik W, Bellemain E, Valentini A, Zedrosser A, Taberlet P, Kindberg J, Swenson JE, Radwan J (2014) No evidence for the effect of MHC on male mating success in the brown bear. PLoS ONE, 9, e113414. DOI URL
[39]	Laitinen T (1993) A set of MHC haplotypes found among Finnish couples suffering from recurrent spontaneous abortions. American Journal of Reproductive Immunology, 29, 148-154. PMID
[40]	Lambeck RJ (1997) Focal species: A multi-species umbrella for nature conservation. Conservation Biology, 11, 849-856. DOI URL
[41]	Landry C, Garant D, Duchesne P, Bernatchez L (2001) ‘Good genes as heterozygosity’:The major histocompatibility complex and mate choice in Atlantic salmon (Salmo salar). Proceedings of the Royal Society B: Biological Sciences, 268, 1279-1285.
[42]	Laubu C, Dechaume-Moncharmont FX, Motreuil S, Schweitzer C (2016) Mismatched partners that achieve postpairing behavioral similarity improve their reproductive success. Science Advances, 2, e1501013.
[43]	Lees CM, Wilcken J (2009) Sustaining the Ark: The challenges faced by zoos in maintaining viable populations. International Zoo Yearbook, 43, 6-18. DOI URL
[44]	Li TY, Liu YM, Wang DL, Zhong ZW (2022) Concepts, research progresses and prospects of animal personality. Acta Ecologica Sinica, 42, 37-44. (in Chinese with English abstract)
	[李天韵, 刘依明, 王德利, 钟志伟 (2022) 动物个性研究进展. 生态学报, 42, 37-44.]
[45]	Lloyd AS, Elizabeth Martin J, Bornett-Gauci HLI, Wilkinson RG (2007) Evaluation of a novel method of horse personality assessment: Rater-agreement and links to behaviour. Applied Animal Behaviour Science, 105, 205-222. DOI URL
[46]	Mariette MM, Griffith SC (2012) Nest visit synchrony is high and correlates with reproductive success in the wild zebra finch Taeniopygia guttata. Journal of Avian Biology, 43, 131-140. DOI URL
[47]	Martin MS, Shepherdson DJ (2012) Role of familiarity and preference in reproductive success in ex situ breeding programs. Conservation Biology, 26, 649-656. DOI URL
[48]	Martin-Wintle MS (2017) Do opposites attract? Effects of personality matching in breeding pairs of captive giant pandas on reproductive success. Biological Conservation, 207, 27-37. DOI URL
[49]	Martin-Wintle MS, Shepherdson D, Zhang GQ, Zhang HM, Li DS, Zhou XP, Li RG, Swaisgood RR (2015) Free mate choice enhances conservation breeding in the endangered giant panda. Nature Communications, 6, 10125. DOI PMID
[50]	Martin-Wintle MS, Wintle NJP, Díez-León M, Swaisgood RR, Asa CS (2019) Improving the sustainability of ex situ populations with mate choice. Zoo Biology, 38, 119-132. DOI PMID
[51]	Marzluff JM, Balda RP (1988) The advantages of, and constraints forcing, mate fidelity in Pinyon Jays. The Auk, 105, 286-295. DOI URL
[52]	Mays HL, Hill GE (2004) Choosing mates: Good genes versus genes that are a good fit. Trends in Ecology & Evolution, 19, 554-559. DOI URL
[53]	Neff BD, Pitcher TE (2005) Genetic quality and sexual selection: An integrated framework for good genes and compatible genes. Molecular Ecology, 14, 19-38. PMID
[54]	Ober C, Weitkamp LR, Cox N, Dytch H, Kostyu D, Elias S (1997) HLA and mate choice in humans. The American Journal of Human Genetics, 61, 497-504. DOI URL
[55]	Olsson M, Madsen T, Nordby J, Wapstra E, Ujvari B, Wittsell H (2003) Major histocompatibility complex and mate choice in sand lizards. Proceedings of the Royal Society B: Biological Sciences, 270, S254-S256.
[56]	Potts WK, Manning CJ, Wakeland EK (1991) Mating patterns in seminatural populations of mice influenced by MHC genotype. Nature, 352, 619-621. DOI
[57]	Potts WK, Wakeland EK (1990) Evolution of diversity at the major histocompatibility complex. Trends in Ecology & Evolution, 5, 181-187. DOI URL
[58]	Pryke SR, Griffith SC (2009) Postzygotic genetic incompatibility between sympatric color morphs. Evolution, 63, 793-798. DOI PMID
[59]	Pryke SR, Rollins LA, Griffith SC (2010) Females use multiple mating and genetically loaded sperm competition to target compatible genes. Science, 329, 964-967. DOI PMID
[60]	Qian J, Zhuang HF, Yang WK, Chen YF, Chen SL, Qu YH, Zhang YM, Yang YP, Wang YH (2020) Selecting flagship species to solve a biodiversity conservation conundrum. Plant Diversity, 42, 488-491. DOI
[61]	Qiao JL, Sun TF, Qi LP, Cai YH, Zheng CL, Cheng JG, Fu WL, Meng XX (2018) Studies on the personality and relationships of musk secretion and reproduction success in captive forest musk deer. Acta Ecologica Sinica, 38, 8306-8313. (in Chinese with English abstract)
	[乔佳伦, 孙太福, 齐利平, 蔡永华, 郑程莉, 程建国, 付文龙, 孟秀祥 (2018) 圈养林麝(Moschus berezovskii)个性及与麝香分泌和繁殖成效的关系. 生态学报, 38, 8306-8313.]
[62]	Rabdeau J, Badenhausser I, Gaffard A, Mangelinck C, Moreau J, Bretagnolle V, Monceau K (2021) Assortative pairing for boldness and consequences for reproductive success in Montagu’s harrier. Biological Journal of the Linnean Society, 132, 759-773. DOI URL
[63]	Radwan J, Tkacz A, Kloch A (2008) MHC and preferences for male odour in the bank vole. Ethology, 114, 827-833. DOI URL
[64]	Roberts SC, Little AC, Gosling LM, Perrett DI, Carter V, Jones BC, Penton-Voak I, Petrie M (2005) MHC-heterozygosity and human facial attractiveness. Evolution and Human Behavior, 26, 213-226. DOI URL
[65]	Royle NJ, Hartley IR, Parker GA (2006) Consequences of biparental care for begging and growth in zebra finches, Taeniopygia guttata. Animal Behaviour, 72, 123-130. DOI URL
[66]	Royle NJ, Schuett W, Dall SRX (2010) Behavioral consistency and the resolution of sexual conflict over parental investment. Behavioral Ecology, 21, 1125-1130. DOI URL
[67]	Ryan KK, Altmann J (2001) Selection for male choice based primarily on mate compatibility in the oldfield mouse, Peromyscus polionotus rhoadsi. Behavioral Ecology and Sociobiology, 50, 436-440. DOI URL
[68]	Santema P, Schlicht E, Kempenaers B (2019) Testing the conditional cooperation model: What can we learn from parents taking turns when feeding offspring? Frontiers in Ecology and Evolution, 7, 94. DOI URL
[69]	Schlicht E, Santema P, Schlicht R, Kempenaers B (2016) Evidence for conditional cooperation in biparental care systems? A comment on Johnstone et al. Behavioral Ecology, 27, e2-e5. DOI URL
[70]	Schuett W, Dall SRX, Royle NJ (2011) Pairs of zebra finches with similar ‘personalities’ make better parents. Animal Behaviour, 81, 609-618. DOI URL
[71]	Schuett W, Tregenza T, Dall SRX (2010) Sexual selection and animal personality. Biological Reviews, 85, 217-246. DOI URL
[72]	Shuster SM, Wade MJ (2003) Mating Systems and Strategies. Princeton University Press, Princeton.
[73]	Sih A, Bell A, Johnson JC (2004) Behavioral syndromes: An ecological and evolutionary overview. Trends in Ecology & Evolution, 19, 372-378. DOI URL
[74]	Sinn DL, Apiolaza LA, Moltschaniwskyj NA (2006) Heritability and fitness-related consequences of squid personality traits. Journal of Evolutionary Biology, 19, 1437-1447. PMID
[75]	Smith BR, Blumstein DT (2008) Fitness consequences of personality: A meta-analysis. Behavioral Ecology, 19, 448-455. DOI URL
[76]	Spoon TR, Millam JR, Owings DH (2004) Variation in the stability of cockatiel (Nymphicus hollandicus) pair relationships: The roles of males, females, and mate compatibility. Behaviour, 141, 1211-1234. DOI URL
[77]	Spoon TR, Millam JR, Owings DH (2006) The importance of mate behavioural compatibility in parenting and reproductive success by cockatiels, Nymphicus hollandicus. Animal Behaviour, 71, 315-326. DOI URL
[78]	Spoon TR, Millam JR, Owings DH (2007) Behavioural compatibility, extrapair copulation and mate switching in a socially monogamous parrot. Animal Behaviour, 73, 815-824. DOI URL
[79]	Stervander M, Dierickx EG, Thorley J, de L Brooke M, Westerdahl H (2020) High MHC gene copy number maintains diversity despite homozygosity in a critically endangered single-island endemic bird, but no evidence of MHC-based mate choice. Molecular Ecology, 29, 3578-3592. DOI URL
[80]	Tregenza T, Wedell N (2000) Genetic compatibility, mate choice and patterns of parentage: Invited Review. Molecular Ecology, 9, 1013-1027. PMID
[81]	Triver RL (1972) Parental investment and sexual selection. In: Sexual Selection and the Descent of Man (ed. Campbell B), pp. 136-179. Aldine Publishing Company, Chicago.
[82]	Wang DP, Forstmeier W, DʼAmelio PB, Martin K, Kempenaers B (2021) Is female mate choice repeatable across males with nearly identical songs? Animal Behaviour, 181, 137-149. DOI URL
[83]	Wang DP, Forstmeier W, Farine DR, Maldonado-Chaparro AA, Martin K, Pei YF, Alarcón-Nieto G, Klarevas-Irby JA, Ma SW, Aplin LM, Kempenaers B (2022) Machine learning reveals cryptic dialects that explain mate choice in a songbird. Nature Communications, 13, 1630. DOI PMID
[84]	Wang DP, Forstmeier W, Martin K, Wilson A, Kempenaers B (2020) The role of genetic constraints and social environment in explaining female extra-pair mating. Evolution, 74, 544-558. DOI PMID
[85]	Watters JV, Powell DM (2011) Measuring animal personality for use in population management in zoos: Suggested methods and rationale. Zoo Biology, 31, 1-12. DOI URL
[86]	Wedekind C, Seebeck T, Bettens F, Paepke AJ (1995) MHC-dependent mate preferences in humans. Proceedings of the Royal Society B: Biological Sciences, 260, 245-249.
[87]	Weiss A, King JE, Perkins L (2006) Personality and subjective well-being in orangutans (Pongo pygmaeus and Pongo abelii). Journal of Personality and Social Psychology, 90, 501-511. DOI URL
[88]	Westerdahl H (2004) No evidence of an MHC-based female mating preference in great reed warblers. Molecular Ecology, 13, 2465-2470. PMID
[89]	Wilcox BA (1984) In situ conservation of genetic resources: Determinants of minimum area requirements. In: National Parks: Conservation and Development (eds McNeely JA, Miller KR), pp. 639-657. Smithsonian Institution Press, Washington DC.
[90]	Wiley RH (1973) Territoriality and non-random mating in sage grouse, Centrocercus urophasianus. Animal Behaviour Monographs, 6, 85-169. DOI URL
[91]	Winternitz J, Abbate JL, Huchard E, Havlíček J, Garamszegi LZ (2017) Patterns of MHC-dependent mate selection in humans and nonhuman primates: A meta-analysis. Molecular Ecology, 26, 668-688. DOI PMID
[92]	Yamazaki K, Boyse EA, Miké V, Thaler HT, Mathieson BJ, Abbott J, Boyse J, Zayas ZA, Thomas L (1976) Control of mating preferences in mice by genes in the major histocompatibility complex. Journal of Experimental Medicine, 144, 1324-1335. DOI PMID
[93]	Yu LJ, Nie YG, Yan L, Hu YB, Wei FW (2018) No evidence for MHC-based mate choice in wild giant pandas. Ecology and Evolution, 8, 8642-8651. DOI PMID
[94]	Zacharias MA, Roff JC (2001) Use of focal species in marine conservation and management: A review and critique. Aquatic Conservation: Marine and Freshwater Ecosystems, 11, 59-76. DOI URL