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睾酮对鸟类繁殖各阶段的作用分析

来源:生态学杂志 作者:董飞;万冬梅;王娟
发布于:2020-02-07 共13762字

  摘    要: 类固醇激素睾酮是影响鸟类繁殖最重要的性激素之一,与鸟类的繁殖行为的各个方面息息相关。睾酮通过影响鸟类的羽色、鸣声等来影响鸟类的配偶选择,同时睾酮可以调节配偶选择和繁殖投入之间的平衡。睾酮水平影响出雏数、出飞数、孵化率成功率等繁殖成效。睾酮还对个体的免疫活性和个体的存活率等产生影响。目前关于睾酮对鸟类繁殖影响的研究大多是通过外源性植入睾酮的方式来改变个体睾酮的浓度,其研究结果也常出现相互矛盾之处,对于自然状态下影响睾酮水平变化的因素尚缺乏了解,睾酮对雌雄鸟在繁殖过程中的影响也不尽相同,有必要继续深入研究。

  关键词: 睾酮; 鸟类繁殖; 配偶选择; 繁殖投入; 繁殖成效;

  Abstract: Steroid hormone testosterone is one of the most important sex hormones affecting bird reproduction, which is closely related to breeding behavior. Testosterone affects sexual selection by affecting feather color, song and so on. Testosterone also regulates the trade-off between sexual selection and reproductive input. Testosterone affects the reproductive efficiency including nestling size, fledging size and hatching success rate. Testosterone also affects the immune activity and survival rate of individuals. In general, most studies focusing on bird breeding are based on exogenous testosterone implantation. The results of these studies are often contradictory. The changes of testosterone level under natural conditions and the influencing factors are not well understood. The effects of testosterone on the reproductive process of the male and female bird are also different. Thus, it is necessary to continue in-depth studies on the effect of testosterone on breeding birds.

  Keyword: testosterone; bird breeding; spouse selection; reproductive input; reproductive effect;

  鸟类的繁殖行为是鸟类行为生态学研究中备受关注的领域,繁殖行为包括占区、求偶、配对、筑巢、产卵、孵化、育雏和领域防卫等(郑光美等, 1989)。类固醇激素睾酮是影响鸟类繁殖最重要的性激素,主要由雄性的睾丸间质细胞以及雌性的卵泡膜细胞产生,受下丘脑一垂体一性腺轴(HPG)和许多细胞因子的调控,在雄鸟中具有促进精子发生相关蛋白质和细胞因子的表达、启动和维持雄性正常生殖活动的作用。在雌鸟中,睾酮具有促进卵泡发育成熟和排卵的作用(Apfelbeck et al., 2017)。在鸟类的繁殖周期中,循环中的睾酮水平对鸟类的繁殖起着至关重要的调节作用,探究睾酮与鸟类繁殖间的关系成为目前鸟类生理生态学领域的一个热点问题。我们以Web of ScienceTM核心合集为数据源,以“testosterone”、“breeding”和“bird”为主题词,检索了2010—2019年科学、社会科学、艺术和人文科学领域的学术期刊、书籍和会议录内的相关文章,共检索获得310篇相关论文,其中直接进行睾酮对繁殖影响的研究有94篇。在中国知网数据库中,以“睾酮”、“繁殖”为主题词,检索了1985年至2019年该领域的所有文章,获得论文229篇,其中以鸟类为研究对象的论文有20篇,多为家禽类和朱鹮、褐马鸡等珍稀保护物种的繁殖研究。本文将从睾酮对鸟类繁殖各阶段(配偶选择、繁殖投入、繁殖成效、个体发育及繁殖节律等)的影响方面对前人的文献进行全面梳理,以期为睾酮的进一步研究提供参考。

  1、 睾酮对鸟类配偶选择的影响

  配偶选择是影响鸟类繁殖适合度的重要因素(Kokko et al., 2003),鸟类对潜在配偶的选择是一个极其复杂的过程,需要对配偶的形态体征、基因质量以及生理状况等信息进行综合考察。睾酮作为重要的生理指标,其浓度高低可调节鸟类的配偶选择。

  睾酮通过激活和控制个体行为直接影响鸟类配偶选择,在大多数温带物种中,在繁殖季开始时,睾酮水平达到峰值。在繁殖季节,采用雄激素受体拮抗剂处理显着降低个体的求偶行为(Fusani et al., 2007),多配制鸟类缎蓝园丁鸟(Ptilonorhynchus violaceus)的研究中发现,含有高睾酮水平的雄性能够建造更高质量的凉亭,从而获得更优秀的配偶(Borgia et al., 1991)。

  睾酮通过影响鸟类的羽色、鸣声等,间接影响鸟类的配偶选择。羽色以及斑块大小是鸟类性选择过程中重要的视觉因素,睾酮水平会影响雄性羽毛的表型。在繁殖季,暗眼灯草鹀(Junco hyemalis)血浆睾酮水平与其尾部白色深浅程度呈正相关关系,拥有较大白色尾羽的雄性暗眼灯草鹀更易获得雌鸟的青睐,从而获得更优秀的配偶(McGlothlin et al., 2008)。研究发现,日本鹌鹑(Coturnix japonica)雌性择偶偏好与雄性循环睾酮浓度呈显着正相关,雄性脸颊羽毛黑色素含量呈睾酮依赖性增长,睾酮浓度高的个体,其颜色更鲜艳,而雌鸟在繁殖条件下由于视网膜红敏视红色素的上调而对这种颜色产生了敏锐的感觉,最终引起雌性的求偶偏好(Hiyama et al., 2018)。鸣声作为鸣禽独有的特征,在配偶选择过程中起到至关重要的作用。研究发现,雄性家朱雀(Carpodacus mexicanus)睾酮浓度越高,红色羽毛越多,其鸣叫率越高,在种群中拥有更高的地位,间接提高了其对配偶的吸引力(Duckworth et al., 2004)。
 

睾酮对鸟类繁殖各阶段的作用分析
 

  此外,睾酮也影响着鸟类的其他独特“魅力”,进而影响鸟类配偶选择。研究发现,雌性斑胸草雀(Taeniopygia guttata)希望自己的子代中拥有更多的雄性,因此雌鸟在繁殖后,无论繁殖成功与否,均会增加对含有较高比例雄性子代的成年雄性的好感度,这是因为后代性别比例反映了受精时雄性亲本的睾酮水平,睾酮水平越高,后代中雄性子代比例越大(Drullion et al., 2011)。

  在不同鸟类中,睾酮对配偶选择的影响并不完全一致。研究发现,北美家燕(Hirundo rustica erythrogaster)繁殖前期雌鸟并不喜欢与拥有高水平睾酮的雄鸟交配,雄性睾酮浓度对雌性择偶没有显着的直接作用(Eikenaar et al., 2011)。在合作繁殖的尖尾娇鹟(Chiroxiphia lanceolata)中,雄鸟的求偶炫耀行为与睾酮浓度并无相关性(DuVal et al., 2011)。

  2、 睾酮对鸟类个体繁殖投入的影响

  寻找配偶和提供亲代抚育是鸟类基本的繁殖行为,但彼此间常常存在冲突,特别是在配偶选择和亲代抚育之间,个体必须权衡交配努力和亲代投入,多数情况下,如果寻找配偶耗费大量时间和精力则很难对子代提供更高质量的亲代抚育(Magrath et al., 2003)。进化内分泌学中的一个原则是,睾酮是一种介导交配与父本抚育之间权衡的激素,其核心内容是高水平的睾酮会促进鸟类的交配努力并抑制父本抚育。有研究在雄性赭红尾鸲(Phoenicurus ochruros)中验证了此项原则,该实验研究采用注射促性腺激素释放激素(GnRH)的方法诱导赭红尾鸲雄性个体睾酮浓度短暂升高,与空白组相比,注射组雄性睾酮浓度升高,育雏投入显着降低(Goymann et al., 2017)。外源性植入睾酮会抑制雄性蓝头莺雀(Vireo solitarius)的孵化行为,并降低其递食率(Van Roo, 2004)。但现有证据仍存在分歧,在栗领铁爪鹀(Calcariusornatus)(Lynn et al., 2002)和欧亚大山雀(Parus major)(Van Duyse et al., 2002)的研究中发现,外源性睾酮植入对父本育雏投入无影响。在铁爪鹀(Calcariuslapponicus)的研究中发现外源性植入睾酮受体阻滞剂会导致该巢父本育雏投入短暂下降,虽然会短暂地影响雏鸟的质量,但对最终的雏鸟质量或巢的繁殖成功率没有影响(Hunt et al., 2019)。此外,在亲代抚育期间,睾酮有助于提高雄鸟的配偶保护及巢防卫行为,间接增加雄鸟的繁殖投入(Lynn et al., 2002)。研究发现,巢防卫强的黑尾鸥(Larus crassirostris)雄性比巢防卫弱的雄性拥有更高浓度的血浆睾酮(Kazama et al., 2011)。因此,在交配努力和亲代繁殖投入之间,睾酮似乎起到了调节作用。但在东蓝鸲(Sialia sialis)的研究中,睾酮水平与其巢防卫强度间无相关性(Ambardar et al., 2017)。

  对于雌性亲鸟,睾酮会影响雌鸟的孵卵行为和筑巢行为。在暗眼灯草鹀的研究中发现,睾酮浓度高的雌鸟孵卵次数减少,但却更频繁地建筑、修整巢穴,更频繁地喂养雏鸟,在产下的卵中会沉积更多的睾酮(Gerlach et al., 2013)。在一项关于大山雀的研究中,通过翼下植入充满睾酮晶体的硅橡胶管,提高雌性大山雀血浆睾酮水平,发现睾酮处理后的雌鸟产卵时间较晚,在孵化期间保持较低的孵化温度,但孵育时间与未被处理的鸟类几乎相同(De Jong et al., 2016)。在蓝山雀(Cyanistes caeruleus)中,外源性翼下植入含睾酮的硅橡胶管,提高雌性蓝山雀的血浆睾酮水平,其筑巢速度显着加快(De Jong, 2013)。综上,尽管睾酮对雌鸟的繁殖投入产生一定作用,但关于睾酮是如何影响雌鸟繁殖投入的仍然未知,仍需要进行大量实验探究。

  3 、睾酮对鸟类繁殖成效的影响

  繁殖关系到个体乃至种群的存活,是鸟类生活史的关键环节。繁殖成效则是检验繁殖是否成功的指标,鸟类个体繁殖成效受多种因素的影响,研究发现,个体睾酮水平对鸟类繁殖成效有影响。在纯色椋鸟(Sturnus unicolor)(Rosvall, 2013a, 2013b)及暗眼灯草鹀(Gerlach et al., 2013)的研究中均发现,通过外源性植入方法,实验性增加雌鸟的睾酮水平导致出雏数和出飞数下降。在双色树燕(Tachycineta bicolor)的研究中发现,与正常的雌鸟相比,外源性植入睾酮的雌鸟的孵化率会降低(Rosvall, 2013a)。McGlothlin等(2010)通过外源性注射GnRH诱导睾酮分泌发现,具有较高睾酮的雄性暗眼灯草鹀存活率和子代数均增加,该结果与繁殖与生存权衡的理论所预测的结果相反,表明内源性睾酮可能是调节个体生存与繁殖的重要权衡。

  子代个体质量同样受到母本赋予的睾酮水平的影响。研究表明,卵黄睾酮浓度会影响子代的生长发育(Eising et al., 2006)。雌性大山雀在产卵过程中会逐渐增加卵黄中的睾酮沉积,产下的最后一枚卵孵出的幼鸟体内睾酮水平最高(Podlas et al., 2013),高浓度睾酮可以增强子代乞食行为,以此来平衡先后孵化的雏鸟间的竞争。北美穴鸮(Athene cunicularia hypugaea)是异步孵化鸟类,其卵内睾酮浓度随着产卵顺序的增加而增加,卵内睾酮可能有助于这些雏鸟与年长的兄弟姐妹争夺巢内的食物,使其长大后变得更有竞争力(Welty et al., 2012)。以上研究表明雌性可能通过调节卵细胞中睾酮含量,提高最后孵出的雏鸟的竞争力,来补偿不同步孵化的负面影响。

  睾酮在一次繁殖和二次繁殖中的影响也不尽相同。有研究表明,在一次繁殖过程中,卵黄睾酮注射会显着加速胚胎发育,缩短孵化时间(Eising et al., 2003),但不影响雏鸟体型大小(Tobler et al., 2007)或雏鸟14日龄时的存活率(Von Engelhardt et al., 2005);然而,在亲鸟二次繁殖时,卵黄睾酮注射导致雏鸟死亡率增加(Schwabl et al., 2012),但对雏鸟发育无影响(Tobler et al., 2007)。在纯色椋鸟(Sturnus unicolor)研究中同样发现,在一次繁殖中,增加卵中睾酮浓度可以缩短胚胎发育时间,使雏鸟免疫力增强;,但在二次繁殖中睾酮处理时,会使雏鸟存活率降低(Muriel et al., 2015)。

  4 、睾酮水平对个体发育的影响

  个体早期所经历的社会和生态条件对其生存和发展有着重要的影响,雏鸟血液中睾酮水平差异可转化为个体适合度差异。雀形目鸟类在雏鸟时期就能产生睾酮(Silverin et al., 1996),有研究表明,睾酮分泌量较高的雏鸟后期身体状况更好、成活率更高(López-Rull et al., 2011)。研究发现,当与自己喜欢的雄鸟交配时,灰山鹑(Perdix perdix)雌鸟的后代卵黄睾酮水平明显高于与自己不喜欢的配偶交配的雌鸟的后代中卵黄睾酮水平,由于灰山鹑是早成鸟,在其出雏后受到的亲代抚育较少,因此较高的睾酮水平意味着其拥有着更健康的身体从而提高其存活率(Garcia-Fernandez et al., 2010)。在红翅黑鹂发育过程中发现,高浓度睾酮可以增加雏鸟运动神经元的活动,影响肌肉的发育,尤其是对乞食很重要的肌肉,从而增加其乞食频率(Lipar et al., 2000)。在细嘴锯鹱(Pachyptila belcheri)的研究中发现,睾酮浓度与雏鸟的乞食强度呈正相关(Quillfeldt et al., 2006)。

  研究表明,幼鸟血浆睾酮浓度受巢内雏鸟数量影响,雏鸟在面对兄弟姐妹间的竞争时,会改变自身睾酮的分泌,如巢中雏数较多的斑胸草雀幼鸟与巢中雏数较少的幼鸟相比,前者睾酮浓度更高(Naguib et al., 2004)。但在纯色椋鸟的实验中发现,巢内雏鸟个体的睾酮浓度与巢内雏鸟数量规模呈负相关(Gil et al., 2008)。保持较高的睾酮浓度,也可能会增加个体的发育代价,研究发现,高浓度睾酮会使金丝雀雏鸟生长发育速度下降(Buchanan et al., 2007),使红隼(Falco tinnunculus)的免疫功能下降(Fargallo et al., 2007),在斑胸草雀的研究中也发现了类似的结果(Naguib et al., 2004);高的个体睾酮浓度还可导致大山雀羽毛颜色变淡(Fargallo et al., 2007)。

  5、 睾酮对鸟类繁殖周期的影响

  对周期性繁殖的鸟类来说,繁殖时机的选择是至关重要的,动物个体感受外界环境变化,启动其繁殖行为,这种个体内部的行为变化往往是由激素与环境因素共同介导的。目前普遍认为,光周期的改变导致GnRH-I分泌增加(Millar et al., 1983),GnRH-I刺激垂体黄体生成素(LH)和卵泡刺激素(FSH)的合成和释放(Hattori et al., 1986),这两种激素分泌到血液中并诱导性腺成熟,成熟的性腺通过分泌睾酮(T)和雌二醇(E2)来启动繁殖行为(Lam et al., 1976)。将日照时长由8 h增加到12 h后可以迅速刺激扬州鹅睾丸发育,增加血浆睾酮浓度,启动其季节性生殖活动(Zhu et al., 2017)。采用不同光照处理非繁殖季东北籽鹅,公鹅的睾酮浓度随着光照时间的延长而增加,长光照组个体睾酮水平会接近繁殖期睾酮水平(王秋菊等, 2014)。

  Dunn(2004)在对大量研究的回顾中发现,在79%(57种中的45种)物种中,产蛋期与春季环境温度之间存在显着的负相关关系。在对亚洲短趾百灵鸟种群的研究中发现,HPG内分泌轴的激活与环境温度密切相关,2014年4月份温度最高,血浆睾酮、雌二醇浓度最快达到峰值,产卵、孵化最早;2016年4月份温度最低,睾酮浓度升高最慢,繁殖时间推迟。表明睾酮是调节环境温度对繁殖节律影响的重要生理因素(Zhang et al., 2017)。

  6、 睾酮在鸟类其他方面的研究及目前常用的研究方法

  有研究发现,高质量的个体可以降低睾酮生产相关的成本(Folstad et al., 1992),所以血浆睾酮水平的差异可能反映潜在的个体质量(即内在因素,如遗传或母体效应)或环境变化(即外在因素,如社会和生态环境)的差异(Isabel et al., 2011)。如在靛蓝彩鹀(Passerina cyanea)的研究中发现,其个体上蓝色羽毛的总体比例与睾酮水平和身体状况呈正相关(Hudson et al., 2018)。高睾酮水平与东蓝鸲(Sialia sialis)体表的装饰性色彩程度之间存在负相关关系(Grindstaff et al., 2012)。睾酮广泛参与机体生命代谢活动并产生免疫抑制作用(张阳海等, 2018)。植入睾酮的非繁殖期的雄性歌带鹀(Melospiza melodia)与正常雄鸟相比,细胞介导免疫反应和体液免疫反应都有所降低,说明高浓度的睾酮会降低个体的免疫活性(Owen-Ashley et al., 2004);实验性增加卵黄中的睾酮水平会降低雄性斑胸草雀雏鸟的抗氧化能力(Tobler et al., 2009)。

  作为最重要的性激素之一,睾酮浓度的周期性变化受地域、繁殖时间、繁殖状态、繁殖密度等的影响。卡特琳娜岛雄性红毛莺的睾酮浓度在整个繁殖期始终保持较高的水平,其产卵期睾酮浓度显着高于阿拉斯加州的雄性个体(Horton et al., 2010)。旱季繁殖的雄性哥斯达黎加红颈麻雀(Zonotrichia capensis costaricensis)血浆睾酮水平显着高于在雨季繁殖的及没有繁殖的雄性个体(Addis et al., 2010)。成功配对的雄性褐马鸡(Crossoptilon mantchuricum)在3—5月间睾酮浓度一直持续升高,而未配对的雄性虽然体内睾酮浓度也呈升高趋势,但幅度明显比配对个体小(张文博等, 2015)。在热带鸟类线尾娇鹟(Pipra filicauda)的研究中发现,拥有领地的优势雄鸟的睾酮水平要显着大于没有领地的雄鸟(Ryder et al., 2011)。在蓝黑草鹀(Volatinia jacarina)的研究中发现,竞争环境越激烈,雄性密度越高,睾酮水平会越早升高(Lacava et al., 2011)。雄性东王霸鹟(Tyrannus tyrannus)的睾酮浓度随种群中可育雌鸟的数量增加而增加,随着巢密度的增加而降低(Redmond et al., 2016)。对于迁徙鸟类而言,繁殖准备与春季迁徙有大量重叠,睾酮在调节迁徙与繁殖间过渡的过程中起着重要作用,迁徙期雄性黄眉灶莺(Parkesia noveboracensis)、纹胸林莺(Setophaga magnolia)的睾酮水平显着上升,为之后的繁殖做好准备,但雌鸟的睾酮激素水平保持不变(Covino et al., 2015)。

  目前研究大多是通过外源性植入睾酮缓释体系增加机体睾酮浓度(Goymann et al., 2017)或使用睾酮阻断剂抑制机体内睾酮活性(Hunt et al., 2019)的方法,来探讨睾酮对繁殖期雌雄亲鸟行为及育雏方面的影响,外源性植入方法简单可靠;然而,该方法导致的血浆睾酮浓度变化远超出自然值,睾酮作为一种激素,其含量的微小改变必然导致行为的大幅度变化,因此,在研究自然状态下个体行为变化时,睾酮植入方法可能存在一定的风险。胚胎期(卵期)睾酮植入是目前研究睾酮对雏鸟影响的常用技术手段,通过对卵内睾酮注射方法,观察植入后雏鸟个体的体征及免疫状态。

  对于自然状态下睾酮浓度测定的方法主要是采用Elisa方法测定鸟类个体血浆、粪便或羽毛中激素水平,血浆睾酮测定方法取血量较少,对个体的损伤小,能直接反映实时状态下个体睾酮浓度,但技术要求高,血液需低温保存,增加野外实验难度;且目前国内Elisa试剂盒准确度较低,不同厂家、不同批次的试剂盒测定误差大,国外进口试剂盒价格昂贵,增加实验成本,高灵敏、高精度、快速、微量的睾酮含量测定方法是目前亟待解决的问题。

  7、 展 望

  睾酮作为最重要的性激素之一,与鸟类的繁殖行为的各个方面息息相关。在过去的几十年中,人们对于睾酮如何调节行为有一定的了解,但缺乏深入机理的探究。早期的研究侧重于确定个体睾酮浓度对繁殖过程作用的一般机制,但睾酮是否可以被看作是可遗传的特征,睾酮对个体发育的影响以及睾酮与行为之间的关系是否可以表现出对选择的进化反应,这些问题仍然存在争议。在机制层面上,尽管睾酮作用的一些分子机制正在被阐明,但睾酮与个体行为之间关系的定量模式仍不清楚,充分理解睾酮调整个体行为的机制,以及这些机制如何进化以适应不断变化的环境,将是至关重要的。

  关于睾酮对鸟类繁殖的研究,我国学者目前多集中于对朱鹮、褐马鸡等国家重点保护动物的性激素的调节,对一些具有特殊繁殖行为鸟类的睾酮研究开展的较少,例如:拥有较高婚外配现象的杂色山雀(Sittiparus varius),拥有典型帮手行为的地山雀(Pseudopodoces humilis)等,它们独特的繁殖现象是否和它们的睾酮水平有关呢?这些都有待我们深入探究。

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作者单位:辽宁大学生命科学院辽宁省动物资源与疫病防治重点实验室
原文出处:董飞,万冬梅,王娟.睾酮对鸟类繁殖影响研究进展[J/OL].生态学杂志:1-9[2020-02-07].https://doi.org/10.13292/j.1000-4890.202004.013.
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