Abstract
Mate discrimination contributes to the co-existence of related species by reducing the risk of interspecific copulation. In pollination mutualistic systems where pollinators utilize host plants as mating places, sharing of host plants with other related species could increase non-adaptive interspecific copulation. Although such host-sharing species are expected to have strong mate discrimination systems, little is known about whether and how they discriminate species for mating. Here, we investigate mate discrimination of two fly species, Colocasiomyia xenalocasiae and C. alocasiae (Diptera: Drosophilidae), which share host plants; they are essentially anthophilous, depending exclusively on specific aroid host plants throughout their entire life cycles. Our field observations showed that the males of C. alocasiae and C. xenalocasiae preferentially paired with conspecific, but not heterospecific, females. This indicates that they discriminate species for mating in the natural habitat. Such mate discrimination was also observed under laboratory conditions. To investigate how these flies discriminate species, we defined distinct behavioral elements in courtship sequence in both species, and compared sexual interactions in each element between conspecific and heterospecific pairs. We found that males discriminate female whilst tapping, whereas females discriminate male before or during males’ attempted mounting. This suggests that mate discrimination systems in both males and females reduce the incidence of heterospecific mounting; mounting is a necessary step in the sequence of courtship for successful copulation. The mate discrimination system found in this study potentially allows for the co-existence of C. xenalocasiae and C. alocasiae on the same host plant by effectively suppressing interspecific copulation.
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Data Availability
Data of mounding index in C. xenalocasiae and C. alocasiae in conspecific and heterospecific pairs are provided in the electronic supplementary material 10.
References
Ahmed OM, Avila-Herrera A, Tun KM et al (2019) Evolution of mechanisms that control mating in Drosophila males. Cell Rep 27:2527-2536e4
Billeter JC, Atallah J, Krupp JJ et al (2009) Specialized cells tag sexual and species identity in Drosophila melanogaster Nature 461:987–991
Chen CC, Watada M, Miyake H et al (2013) Courtship patterns in the Drosophila montium species subgroup: Repeated loss of precopulatory courtship? Zoolog Sci 30:1056–1062
Chen A, li, Chen C, cheng, Katoh T et al (2019) Evolution and diversity of the courtship repertoire in the Drosophila montium species group (Diptera: Drosophilidae). J Evol Biol 32:1124–1140
Coyne JA, Orr HA (1989) Patterns of speciation in Drosophila Evolution 43:362–381
Ding Y, Lillvis JL, Cande J et al (2019) Neural evolution of context-dependent fly song. Curr Biol 29:1089-1099e7
Friberg M, Vongvanich N, Borg-Karlson AK et al (2008) Female mate choice determines reproductive isolation between sympatric butterflies. Behav Ecol Sociobiol 62:873–886
Greenspan RJ, Ferveur JF (2000) Courtship in Drosophila Annu Rev Genet 34:205–232
Hagedorn J, Hailpern J, Karahalios KG (2008) VCode and VData: illustrating a new framework for supporting the video annotation workflow. In: Working Conference on Advanced Visual Interfaces. Naples, Italy, pp 317–321
He Z, Luo Y, Shang X et al (2019) Chemosensory sensilla of the Drosophila wing express a candidate ionotropic pheromone receptor. PLoS Biol 17:1–27
Hoikkala A, Crossley S, Castillo-Melendez C (2000) Copulatory courtship in Drosophila birchii and D. serrata, species recognition and sexual selection. J Insect Behav 13:361–373
Jallon J-M, David JR (1987) Variation in cuticular hydrocarbons among the eight species of the Drosophila melanogaster subgroup. Evolution 41:294–302
Khallaf MA, Cui R, Weißflog J et al (2021) Large-scale characterization of sex pheromone communication systems in Drosophila Nat Commun 12:4165
Kubli E (1992) My favorite molecule. The sex-peptide. BioEssays 14:779–784
Massey JH, Chung D, Siwanowicz I et al (2019) The yellow gene influences Drosophila male mating success through sex comb melanization. Elife 8:e49388
McKinney RM, Vernier C, Ben-Shahar Y (2015) The neural basis for insect pheromonal communication. Curr Opin Insect Sci 12:86–92
Miyake T, Yafuso M (2003) Floral scents affect reproductive success in fly-pollinated Alocasia odora (Araceae). Am J Bot 90:370–376
Miyake T, Yafuso M (2005) Pollination of Alocasia cucullata (Araceae) by two Colocasiomyia flies known to be specific pollinators for Alocasia odora Plant Species Biol 20:201–208
Noor MAF (1999) Reinforcement and other consequences of sympatry. Heredity (Edinb) 83:503–508
Okada T (1975) The oriental drosophilids breeding with flowers. Kontyu 43:356–363
Okada T (1980) Synhospitalic evolution of the genus Drosophilella Duda (Diptera. Drosophilidae), with description of a new species from Okinawa and Taiwan. Kontyu 48:218–225
Okada T, Yafuso M (1989) The genus Colocasiomyia Duda (Diptera, Drosophilidae) from Sulawesi. Proc Jpn Soc Syst Zool 39:48–55
Sakai S (2002) A review of brood-site pollination mutualism: Plants providing breeding sites for their pollinators. J Plant Res 115:161–168
Seeholzer LF, Seppo M, Stern DL, Ruta V (2018) Evolution of a central neural circuit underlies Drosophila mate preferences. Nature 559:564–569
Setoguchi S, Kudo A, Takanashi T et al (2015) Social context-dependent modification of courtship behaviour in Drosophila prolongata Proc R Soc B Biol Sci 282:20151377
Shahandeh MP, Pischedda A, Turner TL (2018) Male mate choice via cuticular hydrocarbon pheromones drives reproductive isolation between Drosophila species. Evolution 72:123–135
Spieth HT (1952) Mating behavior within the genus Drosophila (Diptera). Bulletin of the AMNH; v. 99, article 7. 9
Sultana F, Hu YG, Toda MJ et al (2006) Phylogeny and classification of Colocasiomyia (Diptera, Drosophilidae), and its evolution of pollination mutualism with aroid plants. Syst Entomol 31:684–702
Takano-Takenaka K, Repin R, Mohamed MB, Toda MJ (2012) Pollination mutualism between Alocasia macrorrhizos (Araceae) and two taxonomically undescribed Colocasiomyia species (Diptera: Drosophilidae) in Sabah, Borneo. Plant Biol 14:555–564
Takano-Takenaka K, Gao J, Hu Y et al (2021) Phylogeny, taxonomy and flower-breeding ecology of the Colocasiomyia cristata species group (Diptera: Drosophilidae), with descriptions of ten new species. Zootaxa 5079:1–70
Takenaka K, Yin JT, Wen SY, Toda MJ (2006) Pollination mutualism between a new species of the genus Colocasiomyia de Meijere (Diptera: Drosophilidae) and Steudnera colocasiifolia (Araceae) in Yunnan, China. Entomol Sci 9:79–91
Tanaka R, Higuchi T, Kohatsu S et al (2017) Optogenetic activation of the fruitless-labeled circuitry in Drosophila subobscura males induces mating motor acts. J Neurosci 37:11662–11674
Wang F, Wang K, Forknall N et al (2020) Circuit and behavioral mechanisms of sexual rejection by Drosophila females. Curr Biol 30:3749-3760e3
Wen S-Y, Li Y-F (2011) An evolutionary view on courtship behavior of Drosophila: From a comparative approach. Low Temp Sci 69:87–100
Yafuso M (1983) Interspecific relationship between synhospitalic Drosophilella species (Diptera, Drosophilidae) inhabiting Alocasia odora on Okinawa Is. Japan Kontyu 51:520–527
Yafuso M (1993) Thermogenesis of Alocasia odora (Araceae) and the role of Colocasiomyia flies (Diptera: Drosophilidae) as cross-pollinators. Environ Entomol 22:601–606
Yafuso M (1994) Life history traits related to resource partitioning between synhospitalic species of Colocasiomyia (Diptera, Drosophilidae) breeding in inflorescences of Alocasia odora (Araceae). Ecol Entomol 19:65–73
Yukilevich R, Peterson EK (2019) The evolution of male and female mating preferences in Drosophila speciation. Evolution 73:1759–1773
Acknowledgements
We thank Dr. Kohei Takenaka Takano and Dr. Matthew Paul Su for discussion; Ryota Nishimura at Technical Center of Nagoya University for production of the chambers for the behavioral experiments. This study was supported by MEXT KAKENHI Grants-in-Aid for Scientific Research (B) (Grant JP20H03355 to AK; JP18H02488 to YI), Scientific Research on Innovative Areas “Evolinguistics” (Grant JP20H04997 to AK), “Systems science of bio-navigation” (Grant JP19H04933 to AK), ”Evolutionary theory for constrained and directional diversities” (Grant JP20H04865 to YI), Grant-in-Aid for Transformative Research Areas (A) “iPlasticity” (Grant JP21H05689 to AK), Challenging Research (Exploratory) (Grant JP19K22453 to YI), Grant-in Aid for Early-Career Scientists (JP19K16186 and JP21K15137 for RT), JST FOREST (Grant JPMJFR2147 to AK) and JST PRESTO (Grant JPMJPR21S2 to YI), Japan.
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RT, YI, and AK contributed to the study conception and design. Material preparation and data collection were performed by RT and HT. Analysis was performed by RT. The first draft of the manuscript was written by RT, YI, and AK. All authors commented on previous versions of the manuscript. All authors read and approved the final manuscript.
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ESM 1
Mounting index of C. xenalocasiae in conspecific or heterospecific pairs in each chamber (14 chambers for conspecific pairs; 18 chambers for heterospecific pairs). (CSV 1.11 KB)
ESM 2
Mounting index of C. alocasiae in conspecific or heterospecific pairs in each chamber (14 chambers for conspecific pairs; 36 chambers for heterospecific pairs). (CSV 1.22 KB)
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Tanaka, R., Takekata, H., Ishikawa, Y. et al. Mate Discrimination of Colocasiomyia xenalocasiae and C. alocasiae (Diptera: Drosophilidae) as a Possible Factor Contributing to their Co-Existence on the Same Host Plant. J Insect Behav 35, 44–55 (2022). https://doi.org/10.1007/s10905-022-09798-0
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DOI: https://doi.org/10.1007/s10905-022-09798-0