两种果蝇成虫与幼虫期的竞争及其对二者共存的影响

doi:10.17520/biods.2022603

摘要/Abstract

摘要：

昆虫均为完全或不完全变态发育, 其幼虫和成虫阶段往往有着不同的资源需求。研究昆虫在幼虫和成虫阶段的生态位和适合度, 有助于提升我们对昆虫物种共存和群落构建的认识。黑腹果蝇(Drosophila melanogaster)和伊米果蝇(D. immigrans)是全球广布的两种果蝇, 它们常常发生在相同的季节, 且均在腐烂的水果上产卵, 幼虫寄生在其中完成生长发育。本研究通过转瓶实验评估了这两种果蝇在连续竞争过程中的内禀增长率和种内与种间竞争系数, 并进一步检验了它们的成虫对产卵场所, 以及幼虫对食物的竞争强度, 据此计算了两个物种在成虫和幼虫阶段的生态位分化与适合度差异, 在当代物种共存理论的框架下分析了影响两种果蝇共存的关键因素。结果表明, 连续饲养过程中, 黑腹果蝇表现出更高的适合度, 大概率会竞争排斥掉伊米果蝇。具体而言, 两种果蝇在幼虫和成虫期均有极大的生态位重叠, 虽然伊米果蝇成虫对产卵场所有着更高的利用率, 黑腹果蝇的幼虫在生长发育阶段对饲料有着更高的利用率, 但两种果蝇在成虫、幼虫阶段竞争的结果更多地取决于谁先占据资源。本研究表明昆虫在不同发育阶段对资源利用率的变化会在一定程度上影响它们共存的可能性。

关键词: 竞争排斥, 果蝇, 发育阶段, 物种共存, 生态位, 当代物种共存理论

Abstract

Aims: Metamorphosis is a common character of insect development, wherein larval and adult insects exhibit significant differences in their resource requirement and utilization efficiency. Exploring the variations in niche and fitness difference in different development stages among competing insects can enhance our comprehension of insect species coexistence and community formation. Drosophila melanogaster and D. immigrans, two widely distributed Drosophila species, cohabit during the same season and both feed on decaying fruit. This study aims to explore the shift in ontogenetic niche and fitness difference between these two Drosophila flies, thereby undercovering the underlying mechanisms that facilitate their coexistence.
Methods: We set up microcosm experiments to estimate the inter- and intra-species competition coefficients, and the niche overlap and fitness difference of two Drosophila species. We then investigated the resource competition between adult flies for oviposition sites and between larval flies for food resources. Ultimately, we analyzed the probability of coexistence between the flies in their larval and adult stages using modern coexistence theory.
Results: The results showed that D. melanogaster exhibited greater fitness than D. immigrans and possessed a higher probability of winning in competition. Furthermore, adult D. immigrans demonstrated superiority in competing for oviposition sites compared to D. melanogaster, while larval D. melanogaster displayed higher nutrient efficiency than D. immigrans. However, there is significant overlap in the resources required by both species during their adult and larval stages. The competition outcomes in both larval and adult stages were predominantly determined by the sequence of resource access.
Conclusions: According to our competition experiments involving two Drosophila species, we have made an intriguing observation: two species can exhibit excellent competitive abilities during different developmental stages, seemingly enhancing the coexistence of these species. However, the presence of substantial niche overlap, leading to priority effects among the competing pairs, ultimately prevents their coexistence. Furthermore, the diverse competition strategies employed by the two Drosophila species offer an explanation for the victor in cases involving priority effects. Consequently, our findings provide valuable insights into the significance of developmental stages and phenotypic plasticity in species coexistence.

Key words: competitive exclusion, Drosophila, developmental stage, species coexistence, niche, modern species coexistence theory

公欣桐, 陈飞, 高欢欢, 习新强 (2023) 两种果蝇成虫与幼虫期的竞争及其对二者共存的影响. 生物多样性, 31, 22603. DOI: 10.17520/biods.2022603.

Xintong Gong, Fei Chen, Huanhuan Gao, Xinqiang Xi (2023) Larva and adult competition between two Drosophila species and the effects on species coexistence. Biodiversity Science, 31, 22603. DOI: 10.17520/biods.2022603.

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链接本文: https://www.biodiversity-science.net/CN/10.17520/biods.2022603

https://www.biodiversity-science.net/CN/Y2023/V31/I8/22603

图/表 5

图1 果蝇转瓶实验。(a)转瓶实验流程图; (b)黑腹果蝇(Dm)和伊米果蝇(Di)种群动态, 图例中黑腹单独、伊米单独代表单独转瓶实验中黑腹果蝇和伊米果蝇的种群数量, 黑腹/伊米混合代表两种果蝇混合条件下各自的种群数量; (c)基于现代物种共存理论预测转瓶实验中两种果蝇的竞争结果, 它们在虚线右侧灰色区域能稳定共存, 而在虚线左侧的优先效应区域两个物种互不能入侵到对方种群。在斜线填充区域上、下方, 伊米果蝇和黑腹果蝇能够分别赢得竞争。灰色不规则区域是由贝叶斯推断的两物种生态位分化与适合度差异。

Fig. 1 The transferring experiment of two Drosophila species. (a) The process of transferring experiment; (b) The population dynamics of D. melanogaster (Dm) and D. immigrans (Di), Dm/Di alone represents the population size of two species when they grow alone, and Dm/Di mixed represents the population size of each of the two species when they grow together; (c) Competition outcome between two Drosophila species. In region filled with oblique pattern on the right side of dashed line, two species could coexist steadily, while in ‘priority effects’ region on the left side, neither species could invade the other. In the white region above or below the grey region, D. immigrans and D. melanogaster will exclude the other one. The dark irregular grey shape are the niche and fitness difference estimated from Bayesian.

表1 在连续竞争实验以及幼虫和成虫阶段黑腹果蝇(Dm)和伊米果蝇(Di)的种内竞争系数(αDmDm和αDiDi)与种间竞争系数(αDmDi和αDiDm)、内禀增长率(R0Dm和R0Di)、生态位差异(niche difference, ND)和适合度比值(fitness ratio, FR)的均值和中位数

Table 1 The mean and median of intra- (αDmDm and αDiDi) and inter- (αDmDi and αDiDm) species competition coefficients, intrinsic growth rate (R0Dm and R0Di), niche difference (ND) and fitness ration (FR) of D. melanogaster (Dm) and D. immigrans (Di) in the continuous competition experiment and competition in larval and adult stages respectively

	连续竞争实验 Continuous competition experiment		幼虫阶段 Larval stage		成虫阶段 Adult stage
	中位数 Median	平均值 Mean	中位数 Median	平均值 Mean	中位数 Median	平均值 Mean
黑腹果蝇的种内竞争系数(α_DmDm)	0.078	0.082	0.004	0.005	0.093	0.120
黑腹果蝇对伊米果蝇的种间竞争系数(α_DiDm)	0.194	0.219	0.059	0.065	0.435	0.463
伊米果蝇的种内竞争系数(α_DiDi)	0.506	0.526	0.040	0.042	0.153	0.166
伊米果蝇对黑腹果蝇的种间竞争系数(α_DmDi)	0.153	0.162	0.055	0.060	0.181	0.217
黑腹果蝇的内禀增长率(R_0Dm)	50.340	51.280	0.843	0.881	40.950	48.160
伊米果蝇的内禀增长率(R_0Di)	46.090	47.230	0.938	0.968	123.400	129.910
生态位差异(ND)	0.141	0.112	-3.306	-3.567	-1.354	-1.405
适合度比值(FR)	0.314	0.376	0.353	0.385	1.533	1.554

图2 混合饲养时, 不同数量的黑腹果蝇和伊米果蝇幼虫羽化出的成虫数目(a)和单只成虫的鲜重(b)。图中不同小写字母表示对应的指标在处理间差异显著(n = 10, P < 0.05)。

Fig. 2 Number of emerged Drosophila melanogaster and D. immigrans adults (a) and body size of the emerged adult flies (b) in treatments with different number of larvae when they were cultured together. Different letters alongside the circles indicate significant variation among treatments (n = 10, P < 0.05).

图3 不同比例的黑腹果蝇、伊米果蝇成虫处理中两种果蝇的总产卵量(a)和单只雌蝇的产卵量(b)。图中不同字母代表处理间差异显著(n = 10, P < 0.05)。

Fig. 3 Number of eggs produced by Drosophila melanogaster and D. immigrans in treatments with different number of adult flies. Different letters beside the circles indicate significant variation among different treatments (n = 10, P < 0.05).

图4 基于现代物种共存理论预测幼虫(a)和成虫(b)阶段黑腹果蝇(Dm)和伊米果蝇(Di)种间竞争的结果

Fig. 4 Outcome of interspecific competition between Drosophila melanogaster (Dm) and Drosophila immigrans (Di) in larval (a) and adult stage (b) under the framework of the modern species coexistence theory

参考文献 37

[1]	Anaya-Rojas JM, Bassar RD, Matthews B, Goldberg JF, King L, Reznick D, Travis J (2023) Does the evolution of ontogenetic niche shifts favour species coexistence? An empirical test in Trinidadian streams. Journal of Animal Ecology, 92, 1474-1477. DOI PMID
[2]	Ayala FJ (1969) Experimental invalidation of the principle of competitive exclusion. Nature, 224, 1076-1079. DOI
[3]	Ayala FJ, Gilpin ME, Ehrenfeld JG (1973) Competition between species: Theoretical models and experimental tests. Theoretical Population Biology, 4, 331-356. PMID
[4]	Barker JSF, Podger RN (1970a) Interspecific competition between Drosophila melanogaster and Drosophila simulans. Effects of larval density and short-term adult starvation on fecundity, egg hatchability and adult viability. Ecology, 51, 855-864. DOI URL
[5]	Barker JSF, Podger RN (1970b) Interspecific competition between Drosophila melanogaster and Drosophila simulans. Effects of larval density on viability, developmental period and adult body weight. Ecology, 51, 170-189. DOI URL
[6]	Bassar RD, Travis J, Coulson T (2017) Predicting coexistence in species with continuous ontogenetic niche shifts and competitive asymmetry. Ecology, 98, 2823-2836. DOI PMID
[7]	Chesson P (2000) Mechanisms of maintenance of species diversity. Annual Review of Ecology and Systematics, 31, 343-366. DOI URL
[8]	Chu CJ, Wang YS, Liu Y, Jiang L, He FL (2017) Advances in species coexistence theory. Biodiversity Science, 25, 345-354. (in Chinese with English abstract) DOI
	[ 储诚进, 王酉石, 刘宇, 蒋林, 何芳良 (2017) 物种共存理论研究进展. 生物多样性, 25, 345-354.] DOI
[9]	de Roos AM, Persson L (2013) Population and Community Ecology of Ontogenetic Development. Princeton University Press, Princeton.
[10]	Egan JP, Gibbs S, Simons AM (2018) Trophic niches through ontogeny in 12 species of Indo-Pacific marine Clupeoidei (herrings, sardines, and anchovies). Marine Biology, 165, 153. DOI
[11]	Gao HH, Wang YP, Zhai YF, Li LL, Sun YG, Yu Y (2018) The survey and identification of the fruit flies in the main cherry-producing areas of Shandong Province. Journal of Plant Protection, 45, 585-591. (in Chinese with English abstract)
	[ 高欢欢, 王云鹏, 翟一凡, 李丽莉, 孙玉刚, 于毅 (2018) 山东省樱桃主产区果蝇的调查与鉴定. 植物保护学报, 45, 585-591.]
[12]	Gause GF (1934) Experimental analysis of Vito Volterra’s mathematical theory of the struggle for existence. Science, 79, 16-17. PMID
[13]	Godoy O, Levine JM (2014) Phenology effects on invasion success: Insights from coupling field experiments to coexistence theory. Ecology, 95, 726-736. PMID
[14]	Hardin G (1960) The competitive exclusion principle. Science, 131, 1292-1297. DOI PMID
[15]	Hart SP, Turcotte MM, Levine JM (2019) Effects of rapid evolution on species coexistence. Proceedings of the National Academy of Sciences, USA, 116, 2112-2117.
[16]	Hawlena H, Garrido M, Cohen C, Halle S, Cohen S (2022) Bringing the mechanistic approach back to life: A systematic review of the experimental evidence for coexistence and four of its classical mechanisms. Frontiers in Ecology and Evolution, 10, 898074. DOI URL
[17]	Hess C, Levine JM, Turcotte MM, Hart SP (2022) Phenotypic plasticity promotes species coexistence. Nature Ecology & Evolution, 6, 1256-1261.
[18]	Kraft NJ, Godoy O, Levine JM (2015) Plant functional traits and the multidimensional nature of species coexistence. Proceedings of the National Academy of Sciences, USA, 112, 797-802.
[19]	Lasky JR, Bachelot B, Muscarella R, Schwartz N, Forero-Montaña J, Nytch CJ, Swenson NG, Thompson J, Zimmerman JK, Uriarte M (2015) Ontogenetic shifts in trait-mediated mechanisms of plant community assembly. Ecology, 96, 2157-2169. PMID
[20]	Nakazawa T (2015) Ontogenetic niche shifts matter in community ecology: A review and future perspectives. Population Ecology, 57, 347-354. DOI URL
[21]	Nicholson DB, Ross AJ, Mayhew PJ (2014) Fossil evidence for key innovations in the evolution of insect diversity. Proceedings of the Royal Society B: Biological Sciences, 281, 20141823.
[22]	Novotny V, Basset Y, Miller SE, Weiblen GD, Bremer B, Cizek L, Drozd P (2002) Low host specificity of herbivorous insects in a tropical forest. Nature, 416, 841-844. DOI URL
[23]	R Development Core Team (2014) R: A Language and Environment for Statistical Computing. R Foundation for Statistical Computing, Vienna, Austria. http://www.R-project.org/. (accessed on 2022-06-15)
[24]	Ruhr I, Bierstedt J, Rhen T, Das D, Singh SK, Miller S, Crossley DA, Galli GLJ (2021) Developmental programming of DNA methylation and gene expression patterns is associated with extreme cardiovascular tolerance to anoxia in the common snapping turtle. Epigenetics & Chromatin, 14, 42.
[25]	Sameoto DD, Miller RS (1966) Factors controlling the productivity of Drosophila melanogaster and D. simulans. Ecology, 47, 695-704. DOI URL
[26]	Simha A, Pardo-De la Hoz CJ, Carley LN (2022) Moving beyond the diversity paradox: The limitations of competition-based frameworks in understanding species diversity. The American Naturalist, 200, 89-100. DOI URL
[27]	Stoks R, Córdoba-Aguilar A (2012) Evolutionary ecology of Odonata: A complex life cycle perspective. Annual Review of Entomology, 57, 249-265. DOI PMID
[28]	Ten Brink H, de Roos AM, Dieckmann U (2019) The evolutionary ecology of metamorphosis. The American Naturalist, 193, E116-E131.
[29]	Terry JCD, Chen JL, Lewis OT (2021) Natural enemies have inconsistent impacts on the coexistence of competing species. Journal of Animal Ecology, 90, 2277-2288. DOI PMID
[30]	Throckmorton LH (1975) The phylogeny, ecology, and geography of Drosophila. In: Handbook of Genetics (ed. King RC), pp. 421-469, Plenum Publishing Corporation, New York.
[31]	Tilman D (1977) Resource competition between plankton algae: An experimental and theoretical approach. Ecology, 58, 338-348. DOI URL
[32]	Toda MJ (2022) DrosWLD: Taxonomic Information Database for World Species of Drosophilidae. Hokkaido University, Sapporo. https://bioinfo.museum.hokudai.ac.jp/db/. (accessed on 2022-06-02)
[33]	Vijendravarma RK, Narasimha S, Kawecki TJ (2013) Predatory cannibalism in Drosophila melanogaster larvae. Nature Communications, 4, 1789. DOI PMID
[34]	Wallace B (1974) Studies on intra- and inter-specific competition in Drosophila. Ecology, 55, 227-244. DOI URL
[35]	Wang G, Zhang DY (1996) Theories of Biological Competition. Shaanxi Science and Technology Press, Xi’an. (in Chinese)
	[ 王刚, 张大勇 (1996) 生物竞争理论. 陕西科学技术出版社, 西安.]
[36]	Wang ZZ, Ren SP, Zhan LQ, Wu Q, Huang JH, Chen XX (2020) Species diversity of Drosophila and the associated parasitoid complex in waxberry orchard in Zhejiang Province. Chinese Journal of Biological Control, 36, 690-696. (in Chinese with English abstract)
	[ 王知知, 任少鹏, 詹乐晴, 吴琼, 黄健华, 陈学新 (2020) 浙江省杨梅园果蝇及其寄生性天敌种类多样性调查. 中国生物防治学报, 36, 690-696.] DOI
[37]	Whitham TG, Allan GJ, Cooper HF, Shuster SM (2020) Intraspecific genetic variation and species interactions contribute to community evolution. Annual Review of Ecology, Evolution, and Systematics, 51, 587-612. DOI URL