西双版纳三种非传粉小蜂性比研究
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摘要
性比理论是进化生物学研究的热点问题之一,也是进化生物学研究较为成功的领域之一。根据局域配偶竞争理论预测,非传粉小蜂性比(雄性后代数量占总后代数量的比例)偏雌,随着在单个榕果上产卵的繁殖雌蜂数量的增加,后代性比逐渐上升;当繁殖雌蜂数量相同时,交配模式遵循部分局域配偶竞争的非传粉小蜂的性比高于遵循局域配偶竞争的非传粉小蜂。直到目前为止,关于非传粉小蜂的性比对局域配偶竞争的响应机制的研究主要是在自然种群基础上进行。本研究主要以寄生在钝叶榕果内的Sycobia sp.和Diaziella yangi以及鸡嗉果榕内的Apocryptaphagus sp.3种非传粉小蜂为研究对象,采用控制放蜂实验以及观察产卵行为、交配行为的方法,并配合统计自然条件下斜叶榕、垂叶榕、歪叶榕、聚果榕、钝叶榕、鸡嗉果榕内寄生的非传粉小蜂的雌雄分配研究局域配偶竞争或部分局域配偶竞争对非传粉小蜂性比的影响;另外,通过控制在单个榕果产卵的2头D. yangi雌蜂是否具有姐妹关系(来自同一繁殖雌蜂),研究相互作用的繁殖雌蜂之间的亲缘关系对非传粉小蜂后代性比的影响。主要研究结果如下:
1.自然条件下6种榕树果内寄生的22种非传粉小蜂,除了垂叶榕内寄生的Wakerella benjamini外,其余各种非传粉小蜂的平均性比都低于0.5,性比偏雌,与局域配偶竞争理论预测一致。雄蜂有翅型和雄蜂无翅型各自组内,除了D. yangi外,每种非传粉小蜂的平均性比与寄生果实的比率成显著的正相关,即随着某种非传粉小蜂寄生果实比率的增加,其后代性比逐渐上升;对于D. yangi、Sycobia sp.和Apocryptaphagus sp.,平均性比与寄生果实的比率在种内没有显著的相关。
2.钝叶榕内6种常见的榕小蜂具有特殊的出蜂顺序,除Philotrypesis sp.和Sycoscopter sp.外,其余3种非传粉小蜂Sycobia sp.、Lipothymus sp.和D. yangi都先于传粉小蜂离开榕果,榕果苞片口在成熟时自动张开,它们都不需要传粉小蜂雄蜂打迁出出蜂口,并且Sycobia sp.雌雄蜂都能从各自寄生的瘿花旁的榕果壁咬孔离开;而鸡嗉果榕内寄生的Apocryptaphagus sp.几乎与传粉小蜂同时羽化出蜂,雌蜂离开榕果依赖传粉小蜂雄蜂打迁出出蜂孔。
3.非传粉小蜂的交配场所和交配行为与根据雄蜂翅型预测的结果并不完全一致。D. yangi雄蜂虽然有翅,但是其大部分交配发生在寄生的榕果内,并且雄蜂为争夺交配的雌蜂,发生激烈的打斗,胜利者获得交配机会,失败者离去寻找其它雌蜂或者离开榕果到果外寻找从其它榕果羽化出来的未交配的雌蜂;Lipothymus sp.雄蜂虽然无翅,但是有部分交配发生在寄生的榕果外;雄蜂有翅型的Sycobia sp.的交配场所与根据雄蜂翅型预测的结果一致,交配全部发生在寄生的榕果外,以上3种的交配模式都遵循部分局域配偶竞争;雄蜂无翅型的Apocryptaphagus sp.、Philotrypesis sp.和Sycoscopter sp.的交配全部发生在寄生的榕果内,遵循局域配偶竞争。说明简单地根据雄蜂翅型推测非传粉小蜂的交配场所以及交配行为是不准确的。
4.控制在单个榕果上产卵的繁殖雌蜂的数量,随着繁殖雌蜂数量的增加,Apocryptaphagus sp.性比显著上升,而Sycobia sp.和D. yangi的性比却没有显著的变化;当繁殖雌蜂数量都为1头时,D. yangi雄蜂虽然有翅,平均性比为0.0825±0.0093(SE, n =16) ,显著低于雄蜂无翅型的Apocryptaphagus sp.的平均性比0.2876±0.1989(SE, n =17),雄蜂有翅型的Sycobia sp.性比最高:0.382±0.062(SE, n =10)。部分结果与理论预测不一致,说明简单地用雄蜂翅型来估计非传粉小蜂的性比是不准确的,应当考虑其交配行为等因素。
5.当控制放1头D. yangi、Sycoabia sp.以及Apocryptophagus sp.繁殖雌蜂各自在一个榕果上产卵时,后代性比与后代数量呈现出不同的变化规律:随着后代数量的增加,Apocryptaphagus sp.后代性比逐渐降低,性比与后代数量具有显著的负相关;而另外2种非传粉小蜂的后代性比与后代数量没有显著的相关。不同的种,后代性比对产卵量呈现出不同的响应机制。
6.控制在同一榕果上产卵的2头D. yangi雌蜂是否具有姐妹关系,来自蜂源1号树的2头具有姐妹关系的繁殖雌蜂产下的后代平均性比为0.195±0.028,来自2号蜂源树2头具有姐妹关系的繁殖雌蜂产下的后代平均性比为0.189±0.043,来自不同蜂源树的亲缘关系较远的2头繁殖雌蜂产下的后代平均性比为0.240±0.030,三者没有显著的差异;单个榕果内后代的性比在分布上,3种放蜂处理之间也没有显著的差异,即具有姐妹关系的2头繁殖雌蜂产生的后代性比与没有姐妹关系的2头繁殖雌蜂后代性比相比,没有明显的偏左分布。说明D. yangi繁殖雌蜂之间的亲缘关系对后代性比并没有显著影响。
The theory of sex ratio is one of the topics and the most successful fields in evolutionary ecology. Local mate competition (LMC) predicted that the sex ratio of non-pollinating fig wasps was female-biased, and increased with the number of foundress oviposited in a fig. Up to now, the study on how the sex ratio of non-pollinating fig wasps responded to LMC mainly focused on natural population. Through controlling the number of foundress oviposited in a fig, and combining with investigating the distribution of females and males of non-pollinating fig wasps hosting in Ficus curtipes, F. semicordata, F. cyrtophylla, F. racemosa, F. benjamina, F. tinctoria under natural condition, and observing the oviposition behaviors and mate behaviors, the sex ratios of three non-pollinating fig wasps species, Diaziella yangi, Sycobia sp. and Apocryptaphagus sp. were studied, the former two species parasited in Ficus curtipes, and the last one parasited in Ficus semicordata. Meanwhile, through controlling the relatedness of two foundress of D. yangi oviposited in a fig, the influence of foundress’relatedness on sex ratio also was studied. The main results are as follows.
1. All the sex ratios of 22 non-pollinating fig wasps species hosting in six fig species under natural condition were lower than 0.5, and were biased-female, which was identical to LMC, besides the Wakerella benjamini in Ficus benjamini. Considering the winged and wingless species separately, there were significant positive correlations between the average sex ratio of a species and the proportion of fruit in which it occurred, except for D. yangi. Within species there were no significant correlations found for D. yangi, Sycobia sp. and the Apocryptaphagus sp.
2. The six fig wasps species of Ficus curtipes showed special emergencing sequence. Apart from Philotrypesis sp. and Sycoscopter sp., all the emergences of Sycobia sp., Lipothymus sp. and D. yangi were prior to Eupristina sp. (pollinator). The dispersion of these non-pollinating fig wasps didn’t depend on males of pollinator. Furthermore, the females and males of Sycobia sp. could dispersed the figs through the holes chewed by themselves on fig wall near the galls in which they developed; Apocryptaphagus sp. emerged at the same time with pollinator, and the females of Apocryptaphagus sp. left through a hole chewed by pollinator males on the ostile.
3. The mating places and behaviors of non-pollinating fig wasps were not identical to the results thoroughly predicted by wing morphs of males. Although it is winged, most of D. yangi mated inside the figs in which they developed, and males had intensely fighting behavior for mating females; On the contrary, although Lipothymus sp. was wingless, part of mates occurred outside the figs; All the mates of Sycobia sp. with winged males occurred outside the figs, which was identical to theory prediction, the mate of these three species followed the partial LMC. All the mates of Apocryptaphagus sp., Philotrypesis sp. and Sycocopter sp. with wingless males occurred inside the figs in which they developed, which followed LMC. This showed that it was not correct to predict the mating places and behaviors only according to male morphs.
4. With the increase of number of foundress oviposited in a fig, the sex ratio of Apocryptaphagus sp. increased, but there was no significant variation for Sycobia sp. and D. yangi. When foundress number was one, the average sex ratio of D. yangi was 0.0825±0.0093(SE, n =16), lower than Apocryptaphagus sp., which was 0.2876±0.1989(SE, n =17). The sex ratio of Sycobia sp. was the highest, which was 0.382±0.062(SE, n =10). Parts of results were not identical to prediction of theory, which implied that it was not correct to estimate the sex ratio of non-pollinating fig wasps by male morphs simply. Other factors, for example, mating behavior should be considered.
5. When one foundress of D. yangi, Sycobia sp. and Apocryptaphagus sp. oviposited in a fig respectively, there were different correlation between offspring sex ratio and brood size. The sex ratio of Apocryptaphagus sp. decreased with the increase of brood size, but this correlation not found for other two species. Offspring sex ratio showed different response systems for different species.
6. By controlling the relatedness between two foundress of D. yangi oviposited in a fig, the average sex ratio of offspring produced by two sisters foundress was 0.195±0.028 and 0.189±0.043 respectively, the average sex ratio of offspring produced by two unrelated foundress which were from different tree was 0.240±0.030. There were no significant differences among them. Considering the distribution of sex ratio in each fig, there was no significant difference among the three treatments. This implied that the relatedness between foundress of D. yangi oviposited in a fig didn’t affect the sex ratio of offspring significantly.
1.自然条件下6种榕树果内寄生的22种非传粉小蜂,除了垂叶榕内寄生的Wakerella benjamini外,其余各种非传粉小蜂的平均性比都低于0.5,性比偏雌,与局域配偶竞争理论预测一致。雄蜂有翅型和雄蜂无翅型各自组内,除了D. yangi外,每种非传粉小蜂的平均性比与寄生果实的比率成显著的正相关,即随着某种非传粉小蜂寄生果实比率的增加,其后代性比逐渐上升;对于D. yangi、Sycobia sp.和Apocryptaphagus sp.,平均性比与寄生果实的比率在种内没有显著的相关。
2.钝叶榕内6种常见的榕小蜂具有特殊的出蜂顺序,除Philotrypesis sp.和Sycoscopter sp.外,其余3种非传粉小蜂Sycobia sp.、Lipothymus sp.和D. yangi都先于传粉小蜂离开榕果,榕果苞片口在成熟时自动张开,它们都不需要传粉小蜂雄蜂打迁出出蜂口,并且Sycobia sp.雌雄蜂都能从各自寄生的瘿花旁的榕果壁咬孔离开;而鸡嗉果榕内寄生的Apocryptaphagus sp.几乎与传粉小蜂同时羽化出蜂,雌蜂离开榕果依赖传粉小蜂雄蜂打迁出出蜂孔。
3.非传粉小蜂的交配场所和交配行为与根据雄蜂翅型预测的结果并不完全一致。D. yangi雄蜂虽然有翅,但是其大部分交配发生在寄生的榕果内,并且雄蜂为争夺交配的雌蜂,发生激烈的打斗,胜利者获得交配机会,失败者离去寻找其它雌蜂或者离开榕果到果外寻找从其它榕果羽化出来的未交配的雌蜂;Lipothymus sp.雄蜂虽然无翅,但是有部分交配发生在寄生的榕果外;雄蜂有翅型的Sycobia sp.的交配场所与根据雄蜂翅型预测的结果一致,交配全部发生在寄生的榕果外,以上3种的交配模式都遵循部分局域配偶竞争;雄蜂无翅型的Apocryptaphagus sp.、Philotrypesis sp.和Sycoscopter sp.的交配全部发生在寄生的榕果内,遵循局域配偶竞争。说明简单地根据雄蜂翅型推测非传粉小蜂的交配场所以及交配行为是不准确的。
4.控制在单个榕果上产卵的繁殖雌蜂的数量,随着繁殖雌蜂数量的增加,Apocryptaphagus sp.性比显著上升,而Sycobia sp.和D. yangi的性比却没有显著的变化;当繁殖雌蜂数量都为1头时,D. yangi雄蜂虽然有翅,平均性比为0.0825±0.0093(SE, n =16) ,显著低于雄蜂无翅型的Apocryptaphagus sp.的平均性比0.2876±0.1989(SE, n =17),雄蜂有翅型的Sycobia sp.性比最高:0.382±0.062(SE, n =10)。部分结果与理论预测不一致,说明简单地用雄蜂翅型来估计非传粉小蜂的性比是不准确的,应当考虑其交配行为等因素。
5.当控制放1头D. yangi、Sycoabia sp.以及Apocryptophagus sp.繁殖雌蜂各自在一个榕果上产卵时,后代性比与后代数量呈现出不同的变化规律:随着后代数量的增加,Apocryptaphagus sp.后代性比逐渐降低,性比与后代数量具有显著的负相关;而另外2种非传粉小蜂的后代性比与后代数量没有显著的相关。不同的种,后代性比对产卵量呈现出不同的响应机制。
6.控制在同一榕果上产卵的2头D. yangi雌蜂是否具有姐妹关系,来自蜂源1号树的2头具有姐妹关系的繁殖雌蜂产下的后代平均性比为0.195±0.028,来自2号蜂源树2头具有姐妹关系的繁殖雌蜂产下的后代平均性比为0.189±0.043,来自不同蜂源树的亲缘关系较远的2头繁殖雌蜂产下的后代平均性比为0.240±0.030,三者没有显著的差异;单个榕果内后代的性比在分布上,3种放蜂处理之间也没有显著的差异,即具有姐妹关系的2头繁殖雌蜂产生的后代性比与没有姐妹关系的2头繁殖雌蜂后代性比相比,没有明显的偏左分布。说明D. yangi繁殖雌蜂之间的亲缘关系对后代性比并没有显著影响。
The theory of sex ratio is one of the topics and the most successful fields in evolutionary ecology. Local mate competition (LMC) predicted that the sex ratio of non-pollinating fig wasps was female-biased, and increased with the number of foundress oviposited in a fig. Up to now, the study on how the sex ratio of non-pollinating fig wasps responded to LMC mainly focused on natural population. Through controlling the number of foundress oviposited in a fig, and combining with investigating the distribution of females and males of non-pollinating fig wasps hosting in Ficus curtipes, F. semicordata, F. cyrtophylla, F. racemosa, F. benjamina, F. tinctoria under natural condition, and observing the oviposition behaviors and mate behaviors, the sex ratios of three non-pollinating fig wasps species, Diaziella yangi, Sycobia sp. and Apocryptaphagus sp. were studied, the former two species parasited in Ficus curtipes, and the last one parasited in Ficus semicordata. Meanwhile, through controlling the relatedness of two foundress of D. yangi oviposited in a fig, the influence of foundress’relatedness on sex ratio also was studied. The main results are as follows.
1. All the sex ratios of 22 non-pollinating fig wasps species hosting in six fig species under natural condition were lower than 0.5, and were biased-female, which was identical to LMC, besides the Wakerella benjamini in Ficus benjamini. Considering the winged and wingless species separately, there were significant positive correlations between the average sex ratio of a species and the proportion of fruit in which it occurred, except for D. yangi. Within species there were no significant correlations found for D. yangi, Sycobia sp. and the Apocryptaphagus sp.
2. The six fig wasps species of Ficus curtipes showed special emergencing sequence. Apart from Philotrypesis sp. and Sycoscopter sp., all the emergences of Sycobia sp., Lipothymus sp. and D. yangi were prior to Eupristina sp. (pollinator). The dispersion of these non-pollinating fig wasps didn’t depend on males of pollinator. Furthermore, the females and males of Sycobia sp. could dispersed the figs through the holes chewed by themselves on fig wall near the galls in which they developed; Apocryptaphagus sp. emerged at the same time with pollinator, and the females of Apocryptaphagus sp. left through a hole chewed by pollinator males on the ostile.
3. The mating places and behaviors of non-pollinating fig wasps were not identical to the results thoroughly predicted by wing morphs of males. Although it is winged, most of D. yangi mated inside the figs in which they developed, and males had intensely fighting behavior for mating females; On the contrary, although Lipothymus sp. was wingless, part of mates occurred outside the figs; All the mates of Sycobia sp. with winged males occurred outside the figs, which was identical to theory prediction, the mate of these three species followed the partial LMC. All the mates of Apocryptaphagus sp., Philotrypesis sp. and Sycocopter sp. with wingless males occurred inside the figs in which they developed, which followed LMC. This showed that it was not correct to predict the mating places and behaviors only according to male morphs.
4. With the increase of number of foundress oviposited in a fig, the sex ratio of Apocryptaphagus sp. increased, but there was no significant variation for Sycobia sp. and D. yangi. When foundress number was one, the average sex ratio of D. yangi was 0.0825±0.0093(SE, n =16), lower than Apocryptaphagus sp., which was 0.2876±0.1989(SE, n =17). The sex ratio of Sycobia sp. was the highest, which was 0.382±0.062(SE, n =10). Parts of results were not identical to prediction of theory, which implied that it was not correct to estimate the sex ratio of non-pollinating fig wasps by male morphs simply. Other factors, for example, mating behavior should be considered.
5. When one foundress of D. yangi, Sycobia sp. and Apocryptaphagus sp. oviposited in a fig respectively, there were different correlation between offspring sex ratio and brood size. The sex ratio of Apocryptaphagus sp. decreased with the increase of brood size, but this correlation not found for other two species. Offspring sex ratio showed different response systems for different species.
6. By controlling the relatedness between two foundress of D. yangi oviposited in a fig, the average sex ratio of offspring produced by two sisters foundress was 0.195±0.028 and 0.189±0.043 respectively, the average sex ratio of offspring produced by two unrelated foundress which were from different tree was 0.240±0.030. There were no significant differences among them. Considering the distribution of sex ratio in each fig, there was no significant difference among the three treatments. This implied that the relatedness between foundress of D. yangi oviposited in a fig didn’t affect the sex ratio of offspring significantly.
引文
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Kjellberg F(2005) Clutch size: a major sex ratio determinant in fig pollinating fig? Comptes rendus Biologies 328: 471-476
Leigh EG, Herre EA and Fischer EA(1985) Sex allocation in animals. Experientia, 41: 1265-1276
Moore JC, Compton SG, Hatcher MJ, et al.(2002) Quantitative tests of sex ratio models in a pollinating fig wasp. Animal Behavior 64: 23-32
Murray MG(1987) The closed environment of the fig receptacle and its influence on male conflict in the Old Word fig wasp, Philotrypesis pilosa. Animal Behaviour 35: 488-506 Nason JD, Herre EA and Hamrich JL(1998) The breeding structure of a tropical keystone plant resource. Nature 391: 685-687
Peng YQ(彭艳琼),Yang DR(杨大荣) and Wang QY(王秋艳)(2005) Adjustment and stabilization of sex ratio in Ceratosolen solmsi marchali.Acata Ecologica Sinica (生态学报) 25:1347-1350(in Chinese with English abstract)
Pickering J, Read AF and Guerrero S, et al. (2000) Sex ratio and virulence in two species of lizard malaria parasites. Evolutionary Ecological Research 2: 171-184
Read AF, Anwar M and Shutler D, et al.(1995) Sex allocation and population structure in malaria and related parasitic protozoa. Biological Science 260: 359-363
Reece SE, Shuker DM and Pen LD(2004) Kin discrimination and sex ratios in a parasitoid wasp. Journal of Evolutionary Biology 17: 208-216
Reeve HK(1998) Game theory, reproductive skew, and nepotism. In: Dugatkin L, Reeve H K. ed. Game theory and Animal Behavior. Oxford University Press, New York: 118-145
Rodrigo ASP (2005) Non-pollinating wasps distort the sex ratio of pollinating fig wasps.Oikos, 110: 613-619
Roeder C, Harmsen R and Mouldey S(1996) The effects of relatedness on progeny sex ratio in spider mites. Journal of Evolutionary Biology 9: 143-151
Shuker DM(2006)Male influence on sex allocation in the parasitoid wasp, Nasonia vitripennis. Behavioral Ecological and Sociobiololgy 59: 829-835
Shuker DM, Reece SE and Whitehorn PR (2004) Sib-mating does not lead to facultative sex ratio adjustment in the parasitoid wasp: Nasonia vitripennis. Evolutionary Ecological Research 6: 673-480
Stubblefield JW and Seger J(1990) Local mate competition with variable fecundity: dependence of offspring sex ratios on information utilization and mode of male production. Behavioral Ecology 1: 68-80
Suzuki L and Iwasa Y(1982) A sex ratio theory of gregarious parasitoids. Researches on Population Ecology 22: 366-382
Taylor PD, Crespi BJ(1994) Evolutionarily stable strategy sex ratios when correlates of relatedness can be assessed. Animal Naturalist 143: 297-316
Wang QY(王秋艳), Yang DY(杨大荣) and Peng YQ(彭艳琼)(2003) Pollination behavior and propagation of pollinator wasps on Ficus semicordata in Xishuangbanna, China. Acta Entomologica Sinica (昆虫学报) 46: 27-34 (in Chinese with English abstract) Weiblen GD(2002) How to be a fig wasp. Annual Review of Entomology 47: 299-330 Werren JH(1980) Sex ratio adaptation to local mate competition in a parasitic wasp. Science 208: 1157-1159
West SA and Herre EA(1994) The ecology of the New World fig-parasitizing wasps Idarnes and implications for the evolution of the fig-pollinator mutualism. Proceedings of the Royal Society B 258:67-72
West SA and Herre EA(1997) A comparative study of virginity in fig wasps. Animal Behavior 54: 437-450
West SA and Herre EA(1998) Partial local mate competition and the sex ratio: A study on non-pollinating fig wasps. Journal of .evolutional biology 11: 531-548
Wu ZY(吴征益), Zhou ZK(周哲昆) and Michael GG(2003) Flora of China(中国植物志) 5: 37-71(www.efloras.org)
Xu ZF(许再富)(1994) Ficus-a keystone plant species in the tropical rainforest ecosystem of south Yunnan. Biodiversity Science(生物多样性) 2: 21-23 (in Chinese with English abstract)
Yang DR(杨大荣), Zhao TZ(赵庭周), Wang RW(王瑞武), Zhang GM(张光明) and Song QS(宋启示)(2001) Study of pollination ecology of fig wasp (Ceratosolen sp.) in the tropical rainforest of Xishuangbanna, China. Zoological Reserch (动物学研究) 22: 131-139 (in Chinese with English abstract)
Yang DR(杨大荣), Peng YQ(彭艳琼), Wang QY(王秋艳), Xu L(徐磊) and Wei ZD(魏作东)(2003) The structure of insect communities and the ecological characteristics of the functional groups in syconia of three fig trees species in Xishuangbanna, China. Acta Ecoogica Sinica (生态学报) 23:1798-1806(in Chinese with English abstract)
Zhen WQ(甄文全), Huang DW(黄大卫), Yang DR(杨大荣) and Zhu CD(朱朝东)(2004) Fig wasps associated with Ficus semicordata oviposition timing and their population relationship. Acta Entomologica Sinica(昆虫学报) 47: 787-792 (in Chinese with English abstract)
Zhu H(朱华) and Cai L(蔡琳)(2005)The biogeography of tropical rainforest in Yunnan province and its suggestions to the geological history (云南热带雨林生物地理及其对地质历史的暗示) Advances in Earth Science (地球科学进展)20(Suppl.):1-57 (in Chinese without English abstract)