生物多样性, 2023, 31(6): 22534 doi: 10.17520/biods.2022534

综述

配偶行为相容性对动物繁殖的影响

何远思1,2, 张轶宣1,2, 王代平,,1,2,*

1.中国科学院动物研究所动物生态与保护生物学院重点实验室, 北京 100101

2.中国科学院大学, 北京 100049

Effects of mate behavioral compatibility on animal reproduction

Yuansi He1,2, Yixuan Zhang1,2, Daiping Wang,,1,2,*

1. Key Laboratory of Animal Ecology and Conservation Biology, Institute of Zoology, Chinese Academy of Sciences, Beijing 100101

2. University of Chinese Academy of Sciences, Beijing 100049

通讯作者: * E-mail:wangdaiping@ioz.ac.cn

编委: 王彦平

责任编辑: 李会丽

收稿日期: 2022-09-18   接受日期: 2023-01-5  

基金资助: “中国科学院百人计划”资助项目、广东车八岭国家级自然保护区鸟类声音自动监测与收集(E290B711)
科技部基地与人才专项-第三次新疆综合科学考察“阿尔泰山跨境保护地资源环境考察”项目(2022xjkk0801)

Corresponding authors: * E-mail:wangdaiping@ioz.ac.cn

Received: 2022-09-18   Accepted: 2023-01-5  

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.

Keywords: behavioral compatibility; reproductive success; animal personality; mate choice; mate compatibility

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本文引用格式

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.

动物对配偶的选择通常不是随机的, 个体往往需要选择合适的配偶以保证后代质量、提高自身适合度。因此, 何谓“合适的配偶”一直是研究者关注的问题。配对相容性这一概念最早见于配偶之间不相容的假说, 该假说提出配偶间的不相容可能导致繁殖失败, 个体因此选择“离婚”并寻找新配偶(Coulson, 1966)。在配偶选择研究当中, 个体性状本身在进化上也许不具有积极或消极意义, 即对动物的生存繁衍既无益处也无害处, 但双方性状组合的“不和谐”可能导致双方“离婚”后得到的好处超过需要为此付出的代价(Marzluff & Balda, 1988; Ens et al, 1993)。

配对相容性受两性基因、性状、所在环境等相互作用影响(Ryan & Altmann, 2001), 囊括因两个个体相互作用而产生、但在个体水平上无法关注到的因素(Spoon et al, 2004)。在不同水平具体表现为配偶双方基因、形态和行为相容的程度, 不同层次的相容性对动物繁殖有着直接或间接影响, 包括后代质量、亲代繁殖活动协调等(Harvey et al, 2003; Pryke et al, 2010; Winternitz et al, 2017), 并可能影响动物个性差异的维持与进化(Dingemanse & Réale, 2005)、物种对环境变化的适应能力(Harris & Siefferman, 2014)、笼养动物的繁殖成功率(Fox & Millam, 2014)等。

经过数十年发展, 配对相容性相关理论逐渐完备, 尤其在起步较早的基因相容性领域, 现阶段已有海量资料总结了其在不同物种繁殖配对过程中的作用情况(Mays & Hill, 2004; Neff & Pitcher, 2005; Kamiya et al, 2014; Winternitz et al, 2017)。与此相比, 形态相容性研究相对较少, 已有结论显示其本质可能为基因或行为层面的相容。近年来, 研究者们对配偶之间行为相容性的关注日益增加, 研究表明其在进化、保护等领域具有重要研究意义与潜在应用前景。由于与物种对环境压力的抵抗力和适应性有关(Harris & Siefferman, 2014; Burtka & Grindstaff, 2015; Laubu et al, 2016), 完善对物种配偶行为相容性的研究将有利于进一步理解物种濒危的原因、适应性差异的来源等, 并采取针对性保护措施。此外, 个性特征的组合以及是否与偏好对象配对会影响圈养动物的繁殖性能及成功率(Schuett et al, 2011; Martin & Shepherdson, 2012; Ihle, 2015; Martin- Wintle et al, 2015; Martin-Wintle, 2017; Hartnett et al, 2017), 行为间的不相容可能导致繁殖合作不佳或者频繁的配对内攻击行为, 使配对双方因难以和谐相处而无法完成交配, 甚至造成个体死亡, 给物种保护工作带来损失(Anderson, 1984; Fox & Millam, 2014)。故在繁育中考虑配对双方的相容性, 允许动物选择自己偏好的配偶, 可能是提高繁育工作效率的关键所在。

当前世界生物多样性显著下降, 急需开展有效的保护工作。由于物力、时间、技术的限制, 为提高保护效率, 常需要选择具有代表性的珍稀濒危物种优先进行研究(Wilcox, 1984), 以带动对物种分布区内整个生态系统的功能和多样性保护, 具体如旗舰种(flagship species)、伞护种(umbrella species)等。旗舰种通常为特殊栖息地或精神文化、审美的代表物种, 能有效吸引公众力量参与保护(Zacharias & Roff, 2001; Qian et al, 2020); 伞护种则由于生境需求覆盖面广而对要求较低的共存物种具有辐射保护作用(Lambeck, 1997)。相关工作需要解决的问题包括厘清物种濒危原因、机制以制定有针对性的保护措施, 有效恢复并维持其种群数量与繁殖力, 从而实现长期可持续发展。故加强对配偶行为相容性的研究, 尤其以珍稀濒危动物为研究对象展开探索, 对完善生物多样性保护工作具有重要意义。

目前国内关于动物基因、个性、行为模式及其对繁殖策略、配偶选择等的影响已有报道(鄂明菊, 2017; 乔佳伦等, 2018; 韩群花, 2019; 罗娟娟, 2019(①罗娟娟 (2019) 灰喜鹊个性对繁殖策略的影响. 硕士学位论文, 兰州大学, 兰州.); 张娟, 2020(②张娟 (2020) 社会环境中灰文鸟个性表达以及与雌性配偶选择的关系. 硕士学位论文, 辽宁大学, 沈阳.)), 但主要限于个体层面及基因相容性的研究, 行为相容性方面尚待进一步补充探索。故开展相关工作, 尤其是针对我国珍稀濒危动物进行研究, 对解答与进化、物种濒危机制等有关的问题以及实施有效保护措施十分必要。

本文基于数十年来较有代表性的研究结果, 综述了配对相容性的研究历史、定义、不同表现, 并着重介绍了配偶行为相容性概念的产生、对动物繁殖影响的研究进展等, 同时对未来研究方向和方法改进提出设想, 以期进一步推动我国在该领域的探索。

1 配对相容性的研究发展

1.1 研究历史

配对相容性概念的提出源于对鸟类“离婚”现象的研究。所谓“离婚”是指一年中的任何时候, 配对一方在旧配偶仍存活的情况下, 在后续繁殖中与新配偶配对的行为(Choudhury, 1995)。通过“离婚”来改变配偶, 尤其对“一夫一妻”制的物种而言往往存在代价(例如导致个体错失繁殖机会)。为理解“离婚”行为的适应性, 研究者们提出了许多假说, 其中Coulson (1966)的不相容假说认为, 配偶间可能存在一定程度的不相容进而导致繁殖失败, 因此个体解除当前配对关系去寻找新的配偶将拥有更高适合度。Johnston和Ryder (1987)在综述中指出, 配偶之间的相容性可能是影响生育成功的潜在根本因素, 相容的配对将拥有更高的繁殖成功率, 配对关系也更稳固。但此时尚缺少对配对相容性的具体定义。

随后研究者们开始着眼于从配对水平对伴侣质量进行评估与研究。1988年, Marzluff和Balda提出, 个体在形成配对后会产生涌现特性(emergent properties), 即形成的这个配对产生了新的、存在于配对层面的特性, 而不仅仅是雌雄个体的简单加和, 这意味着不仅个体本身, 而且个体的组合情况也会对繁殖造成影响(Marzluff & Balda, 1988)。Ens等(1993)基于前人结论对不相容假说进行了更完善的表述, 强调: (1)配对双方的相关性状从进化角度看趋于中性, 可能对动物的生存和繁殖既无益处也无害处, (2)但它们可以组合并相互作用, 因而有时导致配对双方分开的好处大于代价。Ryan和Altmann (2001)也指出, 配对相容性与两性表型或基因型间的动态相互作用有关。2004年, Spoon等通过对鸡尾鹦鹉(Nymphicus hollandicus)的研究确定配对与非配对个体, 以及不同配对间存在一系列行为差异, 包括不同的从属关系、合作行为、相互整饰、性行为频率以及对内攻击性、配对双方的距离等, 这些差异可以通过相容性来归纳解释, 因而相容性用于概括由于两个个体相互作用而产生、但在仅考虑个体时无法被考虑到的因素(Spoon et al, 2004)。

综上, 配对相容性是在配对层面描述双方各自性状、特征的组合与相互作用情况; 或者说其关注的是配对双方各自性状、特征通过组合发生相互作用形成协调整体的能力。它强调从配对水平出发度量该配对的质量, 而非仅从个体水平对配对双方进行单独的观察与研究。

1.2 配对相容性研究内涵

配对相容性主要包括基因相容性、形态相容性与行为相容性, 从不同方面对动物的繁殖产生直接或间接影响。直接影响指亲代行为、生殖投资等对后代质量或数量的影响, 而间接影响指亲代遗传贡献对后代的影响(Ihle et al, 2015)。衡量繁殖结果的指标由于研究目的、对象及研究条件的不同而存在一定差异, 具体包括筑巢起始日期(Gabriel & Black, 2012)、受精率(Sinn et al, 2006; Spoon et al, 2006)、产卵数(Spoon et al, 2006)、孵化率(Spoon et al, 2006)、出飞率(Gabriel & Black, 2012)、存活的后代数(Choudhury et al, 1996; Spoon et al, 2006; Laubu et al, 2016)、后代质量(Schuett et al, 2011; Harris & Siefferman, 2014)等, 涉及配对相容性对繁殖活动不同时期的影响(图1)。

图1

图1   配对相容性的不同表现及其对繁殖的影响(虚线代表未有确切证据的潜在关联)

Fig. 1   Different aspects of mate compatibility and their effects on reproduction. The dashed line represents potential associations for which there is no definitive evidence.


1.2.1 配偶基因相容性

基因相容性假说认为, 个体可以基于自身基因型来选择与其相适应的配偶, 从而增加后代遗传多样性、提高适合度(Kempenaers, 2007)。关于基因相容性的工作以“主要组织相容性复合体” (major histocompatibility complex, MHC)基因型的研究为代表, 对于动物如何识别出不同个体间MHC基因型的差异(如嗅觉、面容吸引力)、在何种层次上选择(如配偶选择)、适合度差异的表现(如免疫效应、流产率)等方面目前已有相当数量的研究结果(Laitinen, 1993; Tregenza & Wedell, 2000; Roberts et al, 2005; Radwan et al, 2008; Winternitz et al, 2017)。除此之外, 也有研究人员聚焦于微卫星标记等其他序列(Landry et al, 2001; 鄂明菊, 2017)。

MHC基因几乎存在于所有脊椎动物中, 具有高度多态性, 负责编码能识别结合非自身抗原的蛋白质以引导恰当的免疫反应(Potts & Wakeland, 1990)。不同动物包括鱼类(Landry et al, 2001)、爬行类(Olsson et al, 2003)、啮齿类(Yamazaki et al, 1976; Potts et al, 1991)、人(Wedekind et al, 1995; Ober et al, 1997)以及鸟类(Grieves et al, 2019)等均有选择MHC基因型不同的同类作为配偶的倾向, 这可能有利于减少雌性流产概率(Laitinen, 1993)、增强后代的免疫能力和避免近亲繁殖(Winternitz et al, 2017)等, 能通过遗传因素对个体繁殖造成间接影响, 进而改变个体适合度。但同时, 也有研究显示动物并不根据MHC基因型相容性来选择与其适合的配偶(Westerdahl, 2004; Kuduk et al, 2014; Yu et al, 2018; Stervander et al, 2020), 有荟萃分析研究也表明该领域文献结论异质性较高(Kamiya et al, 2014; Winternitz et al, 2017), 因而相关理论有待通过更严谨全面的实验设计进行检验。

1.2.2 配偶形态相容性

形态相容性主要指配对双方个体形态特征的组合情况, 包括体型、羽色等。已有研究表明, 野外环境中极少存在不同色型雪雁(Anser caerulescens)杂交配对的情况(Cooke et al, 1976); 在蓝头鸦(Gymnorhinus cyanocephalu)中, 体型相似的伴侣配对关系比体型不相似的伴侣更长久(Marzluff & Balda, 1988); 在黑雁(Branta leucopsis)中, 体型相似的配对比不相似的繁殖更好(Black et al, 1996); 七彩文鸟(Chloebia gouldiae)偏好选择头色与自己相同的个体(Pryke et al, 2010)。

形态相容性对繁殖的影响可能通过两个方面产生。一方面, 某些形态可能指示了特定基因, 本质上是通过基因相容性对繁殖结果产生影响, 即形态的相容性实际反映了基因的相容性。如七彩文鸟中红、黑两种头色变种(即不同基因型)存在遗传不相容, 两者杂交会导致后代有较高的死亡率(Pryke & Griffith, 2009), 个体能通过对色型的选择减少或规避对后代的负面影响(Pryke et al, 2010); 另一方面, 在某些类群比如雪雁中, 个体与其所选择的配偶形态之所以相似, 是因为印记行为使它偏好选择与自己亲本一致的表型(Cooke et al, 1976), 即印记行为可能使个体倾向于选择与同种群或较亲近的、与自身相似的同类配对(Wang et al, 2022)。其意义除了防止与其他物种交配之外, 或许还在于同种群的成员彼此可能更熟悉、更容易配合, 所以能更快形成配对从而为繁殖争取时间, 或者配对双方能在繁殖合作中表现更好, 即形态相容性通过改变行为相容性对繁殖结果造成影响, 但有关理论尚待进一步验证。

1.2.3 配偶行为相容性

在配对相容性领域中, 行为相容性日益成为研究者们重点关注的方向。关于配偶行为相容的概念, Spoon等(2006)认为, 行为相容性高的关系会呈现出高的一致性和低的不一致性, 相比相容性低的配对, 相容性高的配对双方会有更多的协调性行为以及更少的攻击性行为, 实际观察中所见的行为互补与协调可能是相容性的具体表现, 其中互补指配对双方在繁殖活动中各司其职、完成不同的工作, 协调指双方在同类型任务中实现权衡。该领域研究内容主要涉及配对双方个性(personality)的组合方式、配对内互动情况如配对内攻击性(intrapair aggression)以及两者在繁殖活动中的合作情况等。行为相容性可通过影响亲本对后代的照顾情况对繁殖产生直接影响。

动物个性, 或称行为综合特征(behavioral syndrome)、性格(temperament)、行为类型(behavioral types)等(李天韵等, 2022), 是指不同个体间存在差异的、且在不同时间至少部分情景下可以重复的一系列行为特征(Gosling & John, 1999; Dall et al, 2004; Sih et al, 2004; Dingemanse & Réale, 2005), 反映了个体的行为倾向或内在的行为一致性(behavioral consistency)。测量动物个性的方法主要分为两大类(Highfill et al, 2010; Fox & Millam, 2014): 一类是借助行为实验或跟踪观察, 直接测量能指示性格类型的稳定行为指标, 如对同类攻击性(Spoon et al, 2004; Laubu et al, 2016)、探索距离与探索新事物的倾向(Gabriel & Black, 2012)等; 另一类是对饲养员等熟悉研究动物的人员进行问卷调查, 从而获得对动物各类行为的描述并进行评估(Gold & Maple, 1994; Lloyd et al, 2007)。不同个体的个性差异已被证明与动物的繁殖成功率及存活率(Smith & Blumstein, 2008)、圈养动物的生活质量(Weiss et al, 2006)等有关, 并且是配偶选择关注的重要性状(Wiley, 1973; Budaev et al, 1999; Schuett et al, 2010)。

在配对水平上, 有研究得出亲本中某些个性组合出现的概率会高于随机组合(Schuett et al, 2010; Rabdeau et al, 2021), 或对配对亲本的繁殖存在影响。如Dingemanse等(2004)捕获野生大山雀(Parus major)后在实验室条件下对其进行新环境探索行为测试(记录个体进入笼舍后2 min内的移动次数), 并在放归后统计了不同配对的后代数及其质量, 结果发现在某些年份, 亲代个性组合类型会影响后代数量, 且具有相似极端探索倾向(无论最倾向还是最不倾向探索)的配对拥有羽翼质量最好的雏鸟, Both等(2005)的进一步研究表明, 其后代的状况受亲本双方探索倾向的相互作用情况影响。Sinn等(2006)在实验室中对捕获的野生塔斯马尼亚四盘耳乌贼(Euprymna tasmanica)进行了威胁测试(threat test)与喂食测试(feeding test), 通过主成分分析(principal component analysis, PCA)将所得行为变量简化为包括个体胆量在内的3个主要个性指标, 并在两周后使其配对交配, 结果表明“胆大”或“中间类型”的雌性只在与同类型雄性配对时产生存活后代, 而“胆小”的雌性则与三类雄性都有存活后代, 提示亲本个性组合可能影响繁殖结果有关, 至于不同性格类型雌性的差异, 研究者推测这可能与雄性存在强迫交配有关。Gabriel和Black (2012)以野生暗冠蓝鸦(Cyanocitta stelleri)种群为研究对象, 选择个体与领地中心的最远活动距离和对陌生人工喂食器的探索时间与速度作为其探索倾向指标, 选择个体对熟悉的人工陷阱的行为反应作为其冒险倾向指标, 发现在探索和冒险情境中表现相似的暗冠蓝鸦伴侣通常更早开始筑巢, 也更有可能抚育出成功出飞的后代; 在关于大熊猫(Ailuropoda melanoleuca)的研究中, Martin-Wintle (2017)通过对饲养员进行问卷调查和对动物进行新颖性测试(novelty test)测定了不同个体的个性, 发现具有特定个性特征组合的配对更容易交配成功并产生后代。

通过控制遗传因素的作用, 研究人员发现亲代的个性或行为倾向组合主要对繁殖结果存在直接影响。Schuett等(2011)以人工饲养的斑胸草雀(Taeniopygia guttata)种群为研究对象, 在繁殖前后通过新环境测试(novel environment test)和镜子测试(mirror test)对亲代的行为个性进行了评估, 通过交叉孵卵、改变育雏亲代及雏鸟数量构建了不同的繁殖模式, 并以雏鸟独立时的头喙比、体重和状态(体重/头喙比)作为亲本的适合度指标, 结果显示雏鸟独立时的各项指标与其遗传父母性格及其相互作用无关, 而受养父母个性与组合情况影响, 并且具有相似性格的配对能产生质量更好的后代。表明亲本在育雏阶段的表现与双方性格、行为倾向的组合及相互作用有关, 不同配对间相容性的差异导致繁殖成功率的差异。

由于对繁殖结果存在影响, 行为相容性也因此与物种应对环境变化的能力等密切相关。在对野生东蓝鸲(Sialia sialis)的研究中, Harris和Siefferman (2014)通过放置笼养东蓝鸲并播放鸣声模拟物种入侵, 测试了不同野生配对的反应时间与攻击倾向, 结果发现, 在种间竞争激烈的地区, 攻击性表现极端(最具攻击性或最不具攻击性)且配对双方倾向相似的东蓝鸲后代体重更大; 类似地, Burtka和Grindstaff (2015)以东蓝鸲的主要竞争物种家麻雀(Sturnus vulgaris)为模拟入侵者, 通过观察被入侵配对的盘旋次数与攻击次数量化其巢穴防御强度, 发现影响雏鸟成功出飞数最显著的因素是亲代双方防御行为的相似度, 而非个体防御行为或整体防御强度。这提示我们, 行为相容性可能因影响动物适应环境的能力而对物种的存续有着更深远的影响。

2 配偶行为相容性对繁殖影响的研究进展

2.1 产生原因与表现

亲代的个性组合之所以与行为相容性的差异有关, 可能是因为不同的个性会导致个体在亲代抚育方面具有不同的投资准则或响应规则(Royle et al, 2010), 进而有不同的行为模式或策略, 因而不同个性组合具有不同的行为相容性。类似地, 研究者发现一些物种倾向选年龄与自己相近的同类配对, 可能是因为年龄相近的伴侣有相似的繁殖经验与繁殖预期(如剩余生育价值), 行为倾向类似, 因此有更高的相容性, 更容易磨合成功(Marzluff & Balda, 1988)。譬如对蓝头鸦的行为观察发现, 年龄差异小的配对在平均分配工作方面比差异大的表现得更好, 减少了亲本在巢中停留的时间, 从而有可能降低被捕食的风险(①Marzluff JM (1983) Factors Affecting Reproductive Success and Behavior at the Nest in Pinyon Jays (Gymnorhinus cyanocephalus). Master dissertation, Northern Arizona Univesity, Flagstaff.)。不相容的个性意味着双方在面对相同的生存问题时, 可能会采取不匹配的解决方法或行为策略, 降低了配对双方在亲代抚育方面的协调性(Harvey et al, 2003); 相反, 相容的个性组合将提高配对的行为相容性, 有利于减少两性的冲突、提高繁殖效率(Triver, 1972; Schuett et al, 2011)。

亲本行为相容的具体表现主要包括配对双方的社交互动情况与繁殖活动的合作情况。相容性高的配偶双方通常对彼此的攻击性更低、亲密行为(如互相整饰等)更多, 整体行为特征为高一致性和低不一致性(Marzluff & Balda, 1988; Baltz, 1998; Spoon et al, 2004; Fox & Millam, 2014)。同时, 相容性高的配对在协调、分配繁殖工作方面也常表现得更好, 如孵化期间能更好地交替坐巢(Spoon et al, 2006)以避免一方承担过多、育雏期间回巢同步率高(Mariette & Griffith, 2012)从而能避免巢址暴露以及有效协调对幼鸟的食物分配等。

2.2 配偶行为相容性的调节

行为相容性可以随个体、时间、环境条件等因素发生动态变化。当低行为相容性对繁殖结果造成负面作用时, 动物除了选择“离婚”, 还可能采取婚外配等策略, 或改变自身行为方式来提高行为相容性, 从而弥补低行为相容性配对带来的适合度下降。

Spoon等(2007)在对笼养鸡尾鹦鹉的行为观察中发现, 配对中一方或双方均有婚外配行为的, 两者的行为相容性显著低于表现忠诚的配对; Wang等(2020)通过人工选择控制雄性斑胸草雀求偶率后, 发现雌性婚外配行为的发生概率主要取决于雌雄组合间的互动而非伴侣的“吸引力”。雌性强烈的个体特异性择偶偏好可能与行为相容性有关(Wang et al, 2021), 当被迫与不喜欢的伴侣配对时, 雌性的婚外配行为会增加(Forstmeier et al, 2021)。

在橘斑娇丽鱼(Amatitlania siquia)中, 行为倾向不同的个体配对后, 一些个体会根据另一方的行为表现改变自己, 使两者相似度增加从而提高繁殖成功率(Laubu et al, 2016)。也有研究发现, 配对时间越长的伴侣通常繁殖成功率越高, 其原因可能是随着时间推移配对行为相容度不断提高, 进而可能刺激个体的繁殖欲望, 使其在繁殖活动中表现得更积极、对后代照顾更好(Coulson, 1972)。

3 对配偶行为相容性研究的展望

3.1 研究领域

研究配对相容性, 尤其是行为相容性对动物繁殖的影响, 对进化、保护等领域的工作开展均有重要意义(图2)。

图2

图2   配偶行为相容性的未来研究方向及研究方法

Fig. 2   Future research fields and methods of behavioral compatibility


3.1.1 进化领域

基于行为相容性的配偶选择结果与选择的个体有关, 并不倾向于特定行为性状, 因此不会导致定向的性选择(Cunningham & Birkhead, 1998; Shuster & Wade, 2003), 同时这种选择模式下也没有所谓“最佳配偶”的概念, 因为配偶质量不仅与配对个体的质量有关, 还取决于个体与其潜在伴侣的行为相容性, 即两者行为的相互作用情况(Ryan &Altmann, 2001)。这种非定向的性选择可能在动物个性的进化与个体差异的维持中扮演了重要角色(Dingemanse & Réale, 2005; Schuett et al, 2010), 尤其是在有双亲抚育的物种中(Schuett et al, 2011)。因此验证行为相容性的存在及其对动物繁殖的影响方式, 或将有助于进一步回答动物个性进化起源和维持有关的问题, 如相同环境下同一种群为何存在有不同行为反应的个体, 以及个体为何在环境条件变化时仍保持自身的行为一致性等。

另一方面, 配对层面新特性的产生, 使配对(pair)不仅仅是个体与个体的简单相加, 而如果这种因配对产生的特性在一夫一妻制物种中广泛出现且都对繁殖有影响, 则意味着“配对”可能也是一个有功能的进化单元(Marzluff & Balda, 1988), 是自然选择的作用对象之一, 这或许也使得有性生殖具有了不同于无性生殖的特殊性。对该假设的验证将有助于进一步丰富相关的进化理论, 而这无疑需要对更多存在长期稳定配对关系的物种展开更深入的研究。

3.1.2 保护领域

不同物种对环境变化的适应性、濒危程度可能与亲本配对相容性高低有关。例如, 对于东蓝鸲, 在竞争激烈的栖息地, 亲本对入侵者攻击性的相似度会影响其繁殖结果, 表明亲本相容性可能影响其对入侵种的抵抗能力(Harris & Siefferman, 2014; Burtka & Grindstaff, 2015)。在橘斑娇丽鱼中, 个体可以根据配偶调整自身行为倾向以使两者相容性提高, 从而改善繁殖成功率, 但这种调节能力存在个体差异, 于是有的配对能通过调整行为提高适合度, 而另一些调节能力差的配对依然受限于低相容性(Laubu et al, 2016)。

因此, 可能对于某些物种而言, 当不相容的个体因环境压力或其他因素被迫配对后, 其无法根据配偶的特点调节自身行为, 配偶间相容性将一直处于较低水平, 于是繁殖成功率也相对低; 而另一些物种有较为灵活的调节能力, 即使迫于压力与相容性不高的同类配对后, 也能通过后期调整提高配对的相容性, 从而增加适合度。这提示我们从配对水平出发、完善对不同物种相容性的研究将有利于进一步理解物种濒危的原因、适应性差异的来源等科学问题并采取针对性的保护措施。

除此之外, 行为相容性研究也能为人工繁育提供辅助。对于关键物种, 尤其是数量较少的珍稀濒危物种, 除了划定自然保护区进行就地保护外, 往往还需要通过繁殖维持一定量的圈养种群, 以便增加野生个体数量或通过再引入恢复已绝灭种群(Comizzoli & Holt, 2019)。但在实际保护工作中, 常存在繁育成功率低、种群可持续性低等问题(Lees & Wilcken, 2009), 许多人工种群中的个体即使表现健康、有配对对象也不进行繁殖。过去在动物园等人工饲养环境里, 为圈养动物挑选配偶时我们通常更关注从哪里获得另一个个体或如何维持基因多样性(Curio, 1998), 而较少考虑动物本身的配偶选择意愿或双方在行为层面的相容性, 这或是造成人工种群繁殖能力差、可持续性低的原因之一。已有研究表明, 与偏好对象配对的侏儒兔(Brachylagus idahoensis)有更高的产仔概率和产仔数量(Martin & Shepherdson, 2012); 在斑胸草雀中, 人为强制配对的繁殖情况常差于自由组合的配对(Ihle et al, 2015); 在大熊猫中, 允许个体与其偏好对象配对提高了繁殖成功率(Martin-Wintle et al, 2015); 对加氏袋狸(Perameles gunnii)的研究也发现, 与偏好雄性配对的雌性更有可能产生后代, 并且需要的时间更少(Hartnett et al, 2017)。因此, 允许动物与偏好伴侣交配或许是提高人工圈养种群可持续性的关键(Martin-Wintle et al, 2019)。一些圈养动物的繁殖失败可能归结于行为相容性低导致的对内攻击性高、繁殖协调性差(Anderson, 1984; Fox & Millam, 2014), 如朱鹮(Nipponia nippon)在日本本土的灭绝, 便可能与最后圈养个体间的行为不相容有关——日本动物园试图促成本土仅存的两只朱鹮配对以挽救种群, 但两个个体在繁殖季冲突激烈, 最终未能交配产下后代(Anderson, 1984)。这些案例表明, 除了保证人工种群的遗传多样性, 我们也应关注配对双方的相容性, 以更有效地提高人工繁殖成功率和种群繁殖的可持续性, 完善珍稀濒危物种保护工作。

个性特征评估目前已在一些动物园中被用于动物圈养管理(Gold & Maple, 1994; Freeman et al, 2004; Watter & Powell, 2011), 但以往的评估大多基于个体, 缺少配对水平的考量。因此在人工繁育方面, 有必要对繁育物种建立针对行为相容性的评估体系, 从而在有繁殖需要时能通过表型性状、个性特征、行为特点等评价双方的相容性, 以预测繁育成功的可能, 如果发现双方对彼此攻击性很强、相处不和谐就应当及时止损, 避免强行“牵线搭桥”导致雌雄发生激烈争斗、造成损失, 以更有效地实现生物多样性保护。

3.2 研究方法

物种配对相容性, 尤其是行为相容性的度量需要建立在对动物个性、行为特征以及不同个体互动情况的完整了解上。对于不同物种, 同一性状组合的相容性高低可能存在差异, 比如觅食时空间同步, 对于一个物种可能是配对相容, 在另一个物种中却可能因增加配偶间竞争降低相容性(Spoon et al, 2006)。因此我们需要借助更先进的设备, 完善环志、项圈佩戴、GPS定位工作以及进行长期的行为观察, 以获取更加精确详细的个体特征、物种行为数据和个体间互动频次等信息。Wang等(2022)在对斑胸草雀的研究中通过在个体身上固定二维码标识, 实现了对个体的精确识别以及活动情况的监控, 由此, 研究人员不仅可以确定个体身份, 还可以了解种群的社会关系网络构建情况, 实现对不同个体社会关系数量及关联强度的定量分析, 从而可以更严谨精确地比较个体与配偶及配对外个体互动情况的差异。此类方法在实验室条件下较为容易实现。对于野外研究, 除了需要投入足够的人力物力外, 也有必要考虑技术的革新, 如改进动物项圈功能, 使其除了提供GPS位点外, 也可以在两个戴项圈个体接近时发送信号, 令研究者能通过信号频率得知不同个体的近距情况, 以此判断其亲密程度。

由于行为相容性本身有许多不同的表现, 而影响配偶选择、亲本投入、繁殖成功率的因素又纷繁复杂, 如研究目标的喂养条件(野生/圈养) (Cooke et al, 1976; Royle et al, 2006; Mariette & Griffith, 2012)、个体差异、环境条件(Dingemanse et al, 2004; Both et al, 2005)等, 所以我们需要进行更严谨巧妙的实验设计。通过行为实验、人工创造特定的繁殖条件等对变量进行控制(Choudhury, 1995; Santema et al, 2019), 分析差异来源与各因素的作用强度, 以厘清不同配对模式、配偶选择标准如何受到选择、有怎样的适合度差异, 并对各类假设进行验证。以笼养鸟类研究为例, 通过交换不同巢的卵可改变子代的养父母, 从而控制遗传因素对后代质量的影响(Schuett et al, 2011), 也可为研究鸣唱方式等种群文化因素对配偶选择的影响创造条件(Wang et al, 2022)。对于野外种群, 通过人工干预控制变量常存在较大的困难, 因此如何实现个体识别以获得年龄、配对时长、社会关系组成等背景信息, 以及获得目标物种的完整行为谱从而筛选出合适的研究指标, 是开展研究时首先需要考虑的问题; 其次是如何选择与设计行为学实验或问卷调查类型, 以确保获得行为数据的同时能尽可能减少对野生动物的干扰。

此外, 为解决前述与进化有关的问题、分析影响动物适合度的主要因素以及研究亲本的合作策略, 比如亲本在合作繁殖时是否遵循特定的策略、相容性不同的配对所遵循策略是否不同, 还需要数学建模的应用(Choudhury, 1995; Shuster & Wade, 2003)。但数学模型在生物学领域的建立与应用往往伴随着大量问题, 如模型是否符合生物学规律、用于对照比较动物有无特殊行为策略的“随机”组是否真的随机等。Johnstone等(2014)在对大山雀的研究中建立了有关双亲条件合作的数学模型并与野外观察数据进行了对比, 发现模型模拟与野外数据相吻合, 因此认为大山雀亲本存在有条件的合作, 会根据自己和配偶喂养雏鸟的情况调整回巢喂食的频率, 即当最后一次喂养雏鸟的是自己时降低喂食频率, 为配偶时则增加喂食频率, 这种合作模式被认为能降低由于双亲利益冲突带来的子代损失(因为亲本总希望另一方多付出而自己少付出, 从而最大化个体利益, 这会使双方都减少对后代的抚育, 因此对后代是不利的)。但该结论受到了一些研究者的质疑, 一方面在于其对“随机”的定义可能存在偏倚, 另一方面在于该模型建立的前提是亲本回巢率只在喂食事件发生时变化且不受其他因素影响, 但实际上亲本回巢率还受天敌、食物质量等众多因素影响(Schlicht et al, 2016; Santema et al, 2019)。因此, 尽管数学方法的应用以及结合野外观察结果的研究方式是重要且必需的, 但如何建立严谨、可信的模型仍有赖于研究者进一步的探索努力。

综上, 本文概述了配对相容性的研究历史、表现, 并着重介绍了行为相容性的概念来源、研究进展、现有结果及研究领域与方法的拓展方向, 展现了行为相容性在进化、保护等领域的重要研究意义和广阔应用前景, 其对生物多样性保护尤其是珍稀濒危动物、旗舰物种的濒危机制研究和保育繁殖具有深远影响, 而该领域的长远发展将有赖于工具技术的更新、多学科方法的融合以及更合理全面的实验设计。

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DOI:10.1038/ncomms10125      PMID:26670381      [本文引用: 2]

Martin-Wintle, Meghan S.; Swaisgood, Ronald R. San Diego Zoo Global, Div Appl Anim Ecol, Inst Conservat Res, San Diego, CA 92027 USA. Martin-Wintle, Meghan S. PDXWildlife, Portland, OR 97219 USA. Martin-Wintle, Meghan S.; Shepherdson, David Portland State Univ, Dept Biol, Portland, OR 97201 USA. Martin-Wintle, Meghan S.; Shepherdson, David Oregon Zoo, Conservat Div, Portland, OR 97221 USA. Zhang, Guiquan; Zhang, Hemin; Li, Desheng; Zhou, Xiaoping; Li, Rengui China Conservat & Res Ctr Giant Panda, Wolong 623006, Sichuan, Peoples R China.

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:10.1002/zoo.21450      PMID:30474268      [本文引用: 1]

Many breeding programs managed by the Association of Zoos and Aquariums' (AZA) Species Survival Plans® (SSPs) are not meeting goals for population size and genetic diversity due to failure of recommended pairs to breed successfully. According to AZA Population Management Center analyses, as many as 80% of recommended breeding pairs fail to produce young before the next breeding and transfer plan is issued. Determining reasons for failure and ensuring that a specific pairing produces offspring can be challenging. Mate incompatibility, one possible reason for failure, might be addressed by allowing mate choice. Although many SSP® coordinators and breeding managers, who implement breeding recommendations at their institutions, recognize the potential benefits of mate choice, examples and models for presenting and assessing choice are lacking. Here we review examples from birds, rodents, lagomorphs, marsupials, carnivores, fishes, and insects where mate choice has been incorporated. These examples provide strong evidence that free mate choice and mating with preferred partners increase a variety of reproductive success measurements when compared to assigned mate pairings. We suggest innovative housing and breeding arrangements for better incorporating mate choice into the management strategies for species held ex situ. Further, we discuss the fitness consequences and welfare implications of allowing choice. We advocate for a more systematic use of behavioral research in cooperative breeding programs. Behavioral management for mating can yield more successful programs, thus ensuring SSP® genetic and demographic goals are met, while simultaneously improving welfare.© 2018 Wiley Periodicals, Inc.

Marzluff JM, Balda RP (1988)

The advantages of, and constraints forcing, mate fidelity in Pinyon Jays

The Auk, 105, 286-295.

DOI:10.2307/4087492      URL     [本文引用: 6]

Mays HL, Hill GE (2004)

Choosing mates: Good genes versus genes that are a good fit

Trends in Ecology & Evolution, 19, 554-559.

DOI:10.1016/j.tree.2004.07.018      URL     [本文引用: 1]

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:15643948      [本文引用: 1]

Why are females so choosy when it comes to mating? This question has puzzled and marveled evolutionary and behavioral ecologists for decades. In mating systems in which males provide direct benefits to the female or her offspring, such as food or shelter, the answer seems straightforward--females should prefer to mate with males that are able to provide more resources. The answer is less clear in other mating systems in which males provide no resources (other than sperm) to females. Theoretical models that account for the evolution of mate choice in such nonresource-based mating systems require that females obtain a genetic benefit through increased offspring fitness from their choice. Empirical studies of nonresource-based mating systems that are characterized by strong female choice for males with elaborate sexual traits (like the large tail of peacocks) suggest that additive genetic benefits can explain only a small percentage of the variation in fitness. Other research on genetic benefits has examined nonadditive effects as another source of genetic variation in fitness and a potential benefit to female mate choice. In this paper, we review the sexual selection literature on genetic quality to address five objectives. First, we attempt to provide an integrated framework for discussing genetic quality. We propose that the term 'good gene' be used exclusively to refer to additive genetic variation in fitness, 'compatible gene' be used to refer to nonadditive genetic variation in fitness, and 'genetic quality' be defined as the sum of the two effects. Second, we review empirical approaches used to calculate the effect size of genetic quality and discuss these approaches in the context of measuring benefits from good genes, compatible genes and both types of genes. Third, we discuss biological mechanisms for acquiring and promoting offspring genetic quality and categorize these into three stages during breeding: (i) precopulatory (mate choice); (ii) postcopulatory, prefertilization (sperm utilization); and (iii) postcopulatory, postfertilization (differential investment). Fourth, we present a verbal model of the effect of good genes sexual selection and compatible genes sexual selection on population genetic variation in fitness, and discuss the potential trade-offs that might exist between mate choice for good genes and mate choice for compatible genes. Fifth, we discuss some future directions for research on genetic quality and sexual selection.

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:10.1086/515511      URL     [本文引用: 1]

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.

[本文引用: 1]

Potts WK, Manning CJ, Wakeland EK (1991)

Mating patterns in seminatural populations of mice influenced by MHC genotype

Nature, 352, 619-621.

DOI:10.1038/352619a0      [本文引用: 1]

Potts WK, Wakeland EK (1990)

Evolution of diversity at the major histocompatibility complex

Trends in Ecology & Evolution, 5, 181-187.

DOI:10.1016/0169-5347(90)90207-T      URL     [本文引用: 1]

Pryke SR, Griffith SC (2009)

Postzygotic genetic incompatibility between sympatric color morphs

Evolution, 63, 793-798.

DOI:10.1111/j.1558-5646.2008.00584.x      PMID:19087185      [本文引用: 1]

Alternative genetically determined color morphs within a population or species are believed to successfully interbreed within a population. However, the occurrence of prezygotic or ecological selection in a number of polymorphic systems may lead to nonrandom mating and prevent genetic morphs from fully interbreeding. Here we show that postzygotic incompatibility significantly limits gene flow between the sympatric red and black color morphs of the Gouldian finch (Erythrura gouldiae). Using a balanced within-female experimental design, in which individuals were forced to breed in pure and mixed morph crosses, we found large inviability effects (>30%) in offspring resulting from genetically mixed genotypes. The consistent mortality effects across different stages of development (e.g., prehatching, juvenile, adulthood), unconfounded by environmentally derived parental effects or social environments, reveal an underlying genetic incompatibility between different genotypes. Furthermore, mortality in mixed morph genotypes was particularly severe (43.6%) for the heterogametic sex (daughters), which is consistent with Haldane's rule predicted for postzygotic incompatibilities between hybridizing species. This significant, but incomplete, postzygotic isolation suggests that the sympatric morphs may represent transient stages in the speciation-hybridization process.

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:10.1126/science.1192407      PMID:20724639      [本文引用: 3]

Individuals in socially monogamous species may participate in copulations outside of the pair bond, resulting in extra-pair offspring. Although males benefit from such extra-pair behavior if they produce more offspring, the adaptive function of infidelity to females remains elusive. Here we show that female participation in extra-pair copulations, combined with a genetically loaded process of sperm competition, enables female finches to target genes that are optimally compatible with their own to ensure fertility and optimize offspring viability. Such female behavior, along with the postcopulatory processes demonstrated here, may provide an adaptive function of female infidelity in socially monogamous animals.

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:10.1016/j.pld.2021.01.004      [本文引用: 1]

The difficulty of effectively monitoring and managing the environment to conserve biodiversity is as yet an unsolved conundrum. A project of the Chinese Academy of Sciences has concluded that progress can be made through the use of flagship species selected using criteria drawn from conservation biology, ecosystem function, socio-economics, and cultural importance. Inclusion of the latter three criteria will help attract and maintain the commitment of the public to play full parts in carrying out any conservation measures needed. A system is proposed for scoring species to select those that are most suitable as flagships. This method can be used regardless of the size of the area chosen for attention, whether it is a region, a country, or a particular protected area.

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)

[本文引用: 1]

[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.]

[本文引用: 1]

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:10.1093/biolinnean/blaa233      URL     [本文引用: 1]

Behavioural combination within pairs depending on personality and plasticity might influence reproductive success. However, studies testing this hypothesis are rare, especially in the case of monogamous species with bi-parental care in which the sexes exhibit different behavioural roles. In this study, we investigated the pairing patterns for both boldness and boldness plasticity in Montagu’s harriers (Circus pygargus), a species with sex-specific care, and the consequences for their reproductive success. We measured individual boldness and plasticity for both sexes, and we assessed the pairing pattern in the Montagu’s harrier population for these two traits. We calculated four indices to characterize the behavioural association within pairs: pair boldness, boldness similarity within pairs, pair plasticity and plasticity similarity within pairs. The relationship between the behaviour of the parents and the reproductive success was then tested through these four indices. We found a pattern of assortative pairing based on both boldness and plasticity in the Montagu’s harrier population. Within-pair similarity of plasticity had a significant effect on the reproductive success, which was higher for less similar pairs than for more similar pairs. Our results question the origin of this pairing pattern and suggest that ecological constraint and not sexual selection could be the major driver.

Radwan J, Tkacz A, Kloch A (2008)

MHC and preferences for male odour in the bank vole

Ethology, 114, 827-833.

DOI:10.1111/eth.2008.114.issue-9      URL     [本文引用: 1]

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:10.1016/j.evolhumbehav.2004.09.002      URL     [本文引用: 1]

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:10.1016/j.anbehav.2005.09.023      URL     [本文引用: 1]

Royle NJ, Schuett W, Dall SRX (2010)

Behavioral consistency and the resolution of sexual conflict over parental investment

Behavioral Ecology, 21, 1125-1130.

DOI:10.1093/beheco/arq156      URL     [本文引用: 1]

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:10.1007/s002650100385      URL     [本文引用: 3]

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:10.3389/fevo.2019.00094      URL     [本文引用: 2]

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:10.1093/beheco/arw036      URL     [本文引用: 1]

Schuett W, Dall SRX, Royle NJ (2011)

Pairs of zebra finches with similar ‘personalities’ make better parents

Animal Behaviour, 81, 609-618.

DOI:10.1016/j.anbehav.2010.12.006      URL     [本文引用: 6]

Schuett W, Tregenza T, Dall SRX (2010)

Sexual selection and animal personality

Biological Reviews, 85, 217-246.

DOI:10.1111/brv.2010.85.issue-2      URL     [本文引用: 3]

Shuster SM, Wade MJ (2003) Mating Systems and Strategies. Princeton University Press, Princeton.

[本文引用: 2]

Sih A, Bell A, Johnson JC (2004)

Behavioral syndromes: An ecological and evolutionary overview

Trends in Ecology & Evolution, 19, 372-378.

DOI:10.1016/j.tree.2004.04.009      URL     [本文引用: 1]

Sinn DL, Apiolaza LA, Moltschaniwskyj NA (2006)

Heritability and fitness-related consequences of squid personality traits

Journal of Evolutionary Biology, 19, 1437-1447.

PMID:16910975      [本文引用: 2]

Dumpling squid, Euprymna tasmanica, show consistent individual differences in behaviour that can be classified according to indices reflecting shy-bold, activity and reactivity responses. Using crosses of wild-caught single males to multiple females with known behavioural phenotypes, this study estimated patterns of additive genetic and residual variance in these behavioural traits from offspring of squid in two contexts, a threat (antipredator) and feeding (foraging) test. Genetic contributions to behavioural expression were dependent on test context. Behaviours in antipredator contexts had significant heritabilities (h(2) = 0.2-0.8) while behaviours from foraging contexts had lesser additive genetic and greater residual components (h(2) = 0.05-0.08). Personality trait variation in females was not related to her fecundity. Female boldness in foraging situations, which co-varied with body size, explained small but significant variation ( approximately 21%) in brood hatching success, while successful fertilization was determined by positive assortion of mate pairs according to their shy-bold phenotype. These results are discussed in terms of the ecological and evolutionary significance of animal "personality" traits in wild populations of animals.

Smith BR, Blumstein DT (2008)

Fitness consequences of personality: A meta-analysis

Behavioral Ecology, 19, 448-455.

DOI:10.1093/beheco/arm144      URL     [本文引用: 1]

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:10.1163/1568539042729711      URL     [本文引用: 4]

Pair relationships and their emergent properties represent potentially significant sources of proximate and ultimate influence on mating systems, but the study of such relational factors has been rare compared to the volume of literature dedicated to individual-level measures of mate quality. This study assessed variation in the stability of pair relationships in cockatiels (Nymphicus hollandicus) and sought sources for that variation in both the behavior of mated individuals and their compatibility. Pair relationships represent an especially salient aspect of the social system of cockatiels, a socially monogamous species with long-term pairing.In a semi-natural, captive setting, this study compared (1) the social interactions between cockatiel mates to those individuals' interactions with opposite-sex non-mates, (2) the roles of males and females in pair relationships, and (3) the various pairs in their displays of intrapair and extrapair interactions. We also assessed the behavioral features underlying pair relationships by examining the interrelationships among social behaviors within pairs and the degree to which emergent properties structure pair relationships. Interactions between mates, as compared to opposite-sex non-mates, were characterized by closer proximity, greater behavioral synchrony, less aggression, more allopreening, and greater sexual behavior. Males and females displayed little dimorphism in many intrapair and extrapair behaviors; however, males approached and courted their mates more than females did, and males but not females exhibited more intersexual aggression to non-mates than to their mates. Social interactions between mates varied significantly among pairs in ways that reflected variation in the degree of behavioral compatibility between mates. In other words, suites of highly correlated behaviors characterized the interactions between mates such that pairs exhibiting greater affiliative or accordant behaviors exhibited less aggressive or discordant behaviors and vice versa. Emergent properties appeared to play an especially important role in compatibility. By examining significant within-species variation in pair relationships, this study complements the increasing knowledge of mating relationships gained from comparative studies and illustrates the importance of emergent, pair-level behavior in the maintenance of long-term monogamous pair-bonds.

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:10.1016/j.anbehav.2005.03.034      URL     [本文引用: 7]

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:10.1016/j.anbehav.2006.10.010      URL     [本文引用: 1]

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:10.1111/mec.v29.19      URL     [本文引用: 1]

Tregenza T, Wedell N (2000)

Genetic compatibility, mate choice and patterns of parentage: Invited Review

Molecular Ecology, 9, 1013-1027.

PMID:10964221      [本文引用: 1]

There is growing interest in the possibility that genetic compatibility may drive mate choice, including gamete choice, particularly from the perspective of understanding why females frequently mate with more than one male. Mate choice for compatibility differs from other forms of choice for genetic benefits (such as 'good genes') because individuals are expected to differ in their mate preferences, changing the evolutionary dynamics of sexual selection. Recent experiments designed to investigate genetic benefits of polyandry suggest that mate choice on the basis of genetic compatibility may be widespread. However, in most systems the mechanisms responsible for variation in compatibility are unknown. We review potential sources of variation in genetic compatibility and whether there is any evidence for mate choice driven by these factors. Selfish genetic elements appear to have the potential to drive mate compatibility mate choice, though as yet there is only one convincing example. There is abundant evidence for assortative mating between populations in hybrid zones, but very few examples where this is clearly a result of selection against mating with genetically less compatible individuals. There are also numerous cases of inbreeding avoidance, but little evidence that mate choice or differential fertilization success driven by genetic compatibility occurs between unrelated individuals. The exceptions to this are a handful of situations where both the alleles causing incompatibility and the alleles involved in mate choice are located in a chromosome region where recombination is suppressed. As yet there are only a few potential sources of genetic compatibility which have clearly been shown to drive mate choice. This may reflect limitations in the potential for the evolution of mate choice for genetic compatibility within populations, although the most promising sources of such incompatibilities have received relatively little research.

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.

[本文引用: 1]

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:10.1016/j.anbehav.2021.09.001      URL     [本文引用: 1]

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:10.1038/s41467-022-28881-w      PMID:35347115      [本文引用: 3]

Culturally transmitted communication signals - such as human language or bird song - can change over time through cultural drift, and the resulting dialects may consequently enhance the separation of populations. However, the emergence of song dialects has been considered unlikely when songs are highly individual-specific, as in the zebra finch (Taeniopygia guttata). Here we show that machine learning can nevertheless distinguish the songs from multiple captive zebra finch populations with remarkable precision, and that 'cryptic song dialects' predict strong assortative mating in this species. We examine mating patterns across three consecutive generations using captive populations that have evolved in isolation for about 100 generations. We cross-fostered eggs within and between these populations and used an automated barcode tracking system to quantify social interactions. We find that females preferentially pair with males whose song resembles that of the females' adolescent peers. Our study shows evidence that in zebra finches, a model species for song learning, individuals are sensitive to differences in song that have hitherto remained unnoticed by researchers.© 2022. The Author(s).

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:10.1111/evo.13905      PMID:31883103      [本文引用: 1]

Why do females of socially monogamous species engage in extra-pair copulations? This long-standing question remains a puzzle, because the benefits of female promiscuous behavior often do not seem to outweigh the costs. Genetic constraint models offer an answer by proposing that female promiscuity emerges through selection favoring alleles that are either beneficial for male reproductive success (intersexual pleiotropy hypothesis) or beneficial for female fecundity (intrasexual pleiotropy hypothesis). A previous quantitative genetic study on captive zebra finches, Taeniopygia guttata, reported support for the first, but not for the second hypothesis. Here, we re-examine both hypotheses based on data from lines selected for high and low male courtship rate. In contrast to previous conclusions, our new analyses clearly reject the hypothesis that male and female promiscuity are genetically homologous traits. We find some support for a positive genetic correlation between female promiscuity and fecundity. This study also shows that the behavioral outcome of extra-pair courtships primarily depends on individual-specific female preferences and not on the "attractiveness" of the social mate. In contrast, patterns of paternity are strongly influenced by the social partner and the pair bond, presumably reflecting variation in copulation behavior, fertility, or sperm competitiveness.© 2019 The Authors. Evolution © 2019 The Society for the Study of Evolution.

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:10.1002/zoo.20379      URL     [本文引用: 1]

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.

[本文引用: 1]

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:10.1037/0022-3514.90.3.501      URL     [本文引用: 1]

Westerdahl H (2004)

No evidence of an MHC-based female mating preference in great reed warblers

Molecular Ecology, 13, 2465-2470.

PMID:15245418      [本文引用: 1]

Female mate-choice based on genetic compatibility is an area of growing interest. The major histocompatibility complex (MHC) genes are likely candidates for such mate-choice since these highly polymorphic genes may both increase offspring viability and also provide direct cues for mate-choice. In great reed warblers, females actively choose a breeding partner out of a handful of males that they visit and evaluate; thus, female preference for compatible or heterozygous MHC genes could have evolved. Here, I investigate whether great reed warbler females preferentially mate with males with dissimilar MHC class I alleles or with males that are heterozygous at MHC class I. Despite favourable conditions, a thorough screening method and a large sample size, there was no evidence of an MHC-based female mating preference based on either genetic compatibility or heterozygosity in this population. Power analyses of the data sets revealed that relatively small differences (15% and 8%, respectively) between true and random pairs should have been detected.Copyright 2004 Blackwell Publishing Ltd

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.

[本文引用: 1]

Wiley RH (1973)

Territoriality and non-random mating in sage grouse, Centrocercus urophasianus

Animal Behaviour Monographs, 6, 85-169.

DOI:10.1016/0003-3472(73)90004-3      URL     [本文引用: 1]

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:10.1111/mec.13920      PMID:27859823      [本文引用: 5]

Genes of the major histocompatibility complex (MHC) in vertebrates are integral for effective adaptive immune response and are associated with sexual selection. Evidence from a range of vertebrates supports MHC-based preference for diverse and dissimilar mating partners, but evidence from human mate choice studies has been disparate and controversial. Methodologies and sampling peculiarities specific to human studies make it difficult to know whether wide discrepancies in results among human populations are real or artefact. To better understand what processes may affect MHC-mediated mate choice across humans and nonhuman primates, we performed phylogenetically controlled meta-analyses using 58 effect sizes from 30 studies across seven primate species. Primates showed a general trend favouring more MHC-diverse mates, which was statistically significant for humans. In contrast, there was no tendency for MHC-dissimilar mate choice, and for humans, we observed effect sizes indicating selection of both MHC-dissimilar and MHC-similar mates. Focusing on MHC-similar effect sizes only, we found evidence that preference for MHC similarity was an artefact of population ethnic heterogeneity in observational studies but not among experimental studies with more control over sociocultural biases. This suggests that human assortative mating biases may be responsible for some patterns of MHC-based mate choice. Additionally, the overall effect sizes of primate MHC-based mating preferences are relatively weak (Fisher's Z correlation coefficient for dissimilarity Zr = 0.044, diversity Zr = 0.153), calling for careful sampling design in future studies. Overall, our results indicate that preference for more MHC-diverse mates is significant for humans and likely conserved across primates.© 2016 John Wiley & Sons Ltd.

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:10.1084/jem.144.5.1324      PMID:1032893      [本文引用: 1]

When a male mouse is presented with two H-2 congenic two female in estrus, his choice of a mate is influenced by their H-2 types. The term "strain preference" is used to describe the general tendency of the male population of one inbred strain to prefer two female of one H-2 type rather than another. The term "consistency of choice" is used to describe the added tendency of particular two males of one inbred strain, in sequential mating trials, to prefer two females of the H-2 type they chose in previous trials. Statistical analysis showed trends in the data that support the following conclusions: (a) The choice is made by the male, not the female. (b) The strain preference of two males may favor two females of dissimilar H-2 type (four of six comparisons), or of similar H-2 type (one of six comparisons). (c) Consistency of choice does not always correspond with strain preference. In one of six comparisons of H-2 genotypes there was no strain preference but pronounced consistency of choice by individual two male. This suggests memory, but fortuitous bias is not excluded. (d) Strain preference of the same male population may favor two male of the same or a different H-2 type, depending on which different H-2 type is offered as the choice alternative to self. These findings conform to a provisional model in which olfactory mating preference is governed by two linked genes in the region of H-2, one for the female signal and one for the male receptor. These mating preferences could in natural populations serve the purpose of increasing the representation of particular H-2 haplotypes or of maintaining heterozygosity of genes in the region of H-2.

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:10.1002/ece3.4419      PMID:30271533      [本文引用: 1]

Major histocompatibility complex genes (MHC), a gene cluster that controls the immune response to parasites, are regarded as an important determinant of mate choice. However, MHC-based mate choice studies are especially rare for endangered animals. The giant panda (), a flagship species, has suffered habitat loss and fragmentation. We investigated the genetic variation of three MHC class II loci, including DRB1, DQA1, and DQA2, for 19 mating-pairs and 11 parent-pairs of wild giant pandas based on long-term field behavior observations and genetic samples. We tested four hypotheses of mate choice based on this MHC variation. We found no supporting evidence for the MHC-based heterosis, genetic diversity, genetic compatibility and "good gene" hypotheses. These results suggest that giant pandas may not use MHC-based signals to select mating partners, probably because limited mating opportunities or female-biased natal dispersal restricts selection for MHC-based mate choice, acknowledging the caveat of the small sample size often encountered in endangered animal studies. Our study provides insight into the mate choice mechanisms of wild giant pandas and highlights the need to increase the connectivity and facilitate dispersal among fragmented populations and habitats.

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:10.1002/(ISSN)1099-0755      URL     [本文引用: 1]

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