Abstract
The natural reproductive behaviour of invasive insects is pivotal knowledge for managing species of ecological or economic concern. We use microsatellites to examine female multiple mating and multiple nest infestations in the introduced parasitic fly, Philornis downsi, which causes high mortality in endemic birds on the Galápagos Islands. We analyse larvae and pupae within 57 nests from Santa Cruz and Floreana Islands in both the highland and lowland habitats. Sib-ship reconstructions of offspring revealed that up to five females may infest a single nest, while multiple mating in females was frequent (65% of reconstructed maternal genotypes), with an average of 1.91 (±0.06 SE) males per female. Genetic relatedness (R) of offspring within nests was generally low, though lowland nests on Floreana had higher R than highland nests. Knowledge of the reproductive behaviour of P. downsi is necessary for modelling appropriate management strategies, in particular, the sterile insect technique, for which success is greatly influenced by female multiple mating.
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References
Arredondo J, Diaz-Fleischer F (2006) Oviposition deterrents for the Mediterranean fruit fly, Ceratitis capitata (Diptera: Tephritidae) from fly faeces extracts. Bull Entomol Res 96:35–42. doi:10.1079/BER2005399
Atkinson R, McVean GAT, Stone GN (2002) Use of population genetic data to infer oviposition behaviour: species-specific patterns in four oak gallwasps (Hymenoptera: Cynipidae). P Roy Soc B-Biol Sci 269:383–390
Azeredo-Espin AML, Lessinger AC (2006) Genetic approaches for studying myiasis causing flies: molecular markers and mitochondrial geneomics. Genetica 126:111–131. doi:10.1007/s10709-005-1439-y
Bonizzoni M, Datsoyannos BI, Marguerie R et al (2002) Microsatellite analysis reveals remating by wild Mediterranean fruit fly females, Ceratitis capitata. Mol Ecol 11:1915–1921. doi:10.1046/j.1365-294X.2002.01602.x
Bush AO, Lafferty KD, Lotz JM, Shostak AW (1997) Parasitology meets ecology on its own terms: Margolis et al. revisited. J Parasitol 83:575–583. doi:10.2307/3284227
Causton CE, Peck SB, Sinclair BJ et al (2006) Alien insects: threats and implications for the conservation of the Galápagos Islands. Ann Entomol Soc Am 99:121–143. doi:10.1603/0013-8746(2006)099[0121:AITAIF]2.0.CO;2
Cayol JP, Coronado P, Taher M (2002) Sexual compatability in medfly (Diptera: Tephritidae) from different origins. Fla Entomol 85:51–57. doi:10.1653/0015-4040(2002)085[0051:SCIMDT]2.0.CO;2
Chapman RE, Wang J, Bourke AFG (2003) Genetic analysis of spatial foraging patterns and resource sharing in bumble bee pollinators. Mol Ecol 12:2801–2808. doi:10.1046/j.1365-294X.2003.01957.x
Chevillon C, Koffi BB, Barre N et al (2007) Direct and indirect inferences on parasite mating and gene transmission patterns—pangamy in the cattle tick Rhipicephalus (Boophilus) microplus. Infect Genet Evol 7:298–304. doi:10.1016/j.meegid.2006.11.007
Criscione CDP, Poulin R, Blouin MS (2005) Molecular ecology of parasites: elucidating ecological and microevolutionary processes. Mol Ecol 14:2247–2257. doi:10.1111/j.1365-294X.2005.02587.x
Cronin JT, Strong DR (1999) Dispersal-dependent oviposition and the aggregation of parasitism. Am Nat 154:24–36. doi:10.1086/303221
Diaz-Fleischer F, Aluja M (2003) Behavioural plasticity in relation to egg and time limitation: the case of two fly species in the genus Anastrepha (Diptera: Tephritidae). Oikos 100:125–133. doi:10.1034/j.1600-0706.2003.12134.x
Dudaniec RY, Kleindorfer S (2006) The effects of the parasitic flies Philornis (Diptera: Muscidae) on birds. Emu 106:13–20. doi:10.1071/MU04040
Dudaniec RY, Kleindorfer S, Fessl B (2006) Effects of the introduced ectoparasite Philornis downsi on haemoglobin level and nestling survival in Darwin’s small ground finch (Geospiza fuliginosa). Austral Ecol 31:88–94. doi:10.1111/j.1442-9993.2006.01553.x
Dudaniec RY, Kleindorfer S, Fessl B (2007) Interannual and interspecific variation in intensity of the parasitic fly, Philornis downsi, in Darwin’s finches. Biol Conserv 139:325–332. doi:10.1016/j.biocon.2007.07.006
Dudaniec RY, Gardner MG, Kleindorfer S (2008a) Isolation, characterisation and multiplex polymerase chain reaction of novel microsatellite loci for the avian parasite Philornis downsi (Diptera: Muscidae). Mol Ecol Resour 8:142–144. doi:10.1111/j.1471-8286.2007.01900.x
Dudaniec RY, Gardner MG, Donnellan S, Kleindorfer S (2008b) Genetic variation in the invasive avian parasite Philornis downsi (Diptera: Muscidae) on the Galápagos archipelago. BMC Ecol 8:13. doi:10.1186/1472-6785-8-13
Dukas R, Prokopy R, Duan JJ (2001) Effects of larval competition on survival and growth in Mediterranean fruit flies. Ecol Entomol 26:587–593. doi:10.1046/j.1365-2311.2001.00359.x
Dvorak M, Vargas H, Fessl B, Tebbich S (2004) On the verge of extinction: a survey of the mangrove finch Camarhynchus heliobates and its habitat on the Galápagos Islands. Oryx 38:171–179. doi:10.1017/S0030605304000316
Fernandez-Escudero I, Pamilo P, Seppa P (2002) Biased sperm use by polyandrous queens of the ant Proformica longiseta. Behav Ecol Sociobiol 51:207–213. doi:10.1007/s00265-001-0433-3
Fessl B, Tebbich S (2002) Philornis downsi - a recently discovered parasite on the Galápagos archipelago: a threat for Darwin’s finches? Ibis 144:445–451. doi:10.1046/j.1474-919X.2002.00076.x
Fessl B, Couri MS, Tebbich S (2001) Philornis downsi Dodge and Aitken, new to the Galápagos Islands (Diptera, Muscidae). Stud Dipterol 8:317–322
Fessl B, Kleindorfer S, Tebbich S (2006a) An experimental study on the effects of an introduced parasite in Darwin’s finches. Biol Conserv 127:55–61. doi:10.1016/j.biocon.2005.07.013
Fessl B, Sinclair BJ, Kleindorfer S (2006b) The life cycle of Philornis downsi (Diptera: Muscidae) parasitizing Darwin’s finches and its impacts on nestling survival. Parasitology 133:739–747. doi:10.1017/S0031182006001089
Frank SA (1994) Kin selection and virulence in the evolution of protocells and parasites. P Roy Soc B-Biol Sci 258:153–161
Grant PR, Grant BR (2008) How and why species multiply: The radiation of Darwin’s finches. Princeton University Press, Princeton
Grant PR, Grant BR, Petren K, Keller LF (2005) Extinction behind our backs: the possible fate of one of the Darwin’s finch species on Isla Floreana, Galápagos. Biol Conserv 122:499–503. doi:10.1016/j.biocon.2004.09.001
Hendrichs J, Robinson AS, Cayol JP, Enkerlin W (2002) Medfly areawide sterile insect technique programmes for prevention, suppression or eradication: the importance of mating behaviour studies. Fla Entomol 85:1–13. doi:10.1653/0015-4040(2002)085[0001:MASITP]2.0.CO;2
Hochberg Y (1988) A sharper Bonferroni procedure for multiple tests of significance. Biometrika 74:800–802
Kalinowski ST, Taper ML, Marshall TC (2007) Revising how the computer program CERVUS accommodates genotyping error increases success in paternity assignment. Mol Ecol 16:1099–1106. doi:10.1111/j.1365-294X.2007.03089.x
Kleindorfer S (2007) The ecology of clutch size variation in Darwin’s small ground finch, Geospiza fuliginosa: comparison between low and highland habitats. Ibis 149:730–741. doi:10.1111/j.1474-919X.2007.00694.x
Kleindorfer S, Dudaniec RY (2009) Love thy neighbour? Social nesting pattern, host mass, and nest size affect ectoparasite intensity in Darwin’s tree finches. Behav Ecol Sociobiol 63:731–739. doi:10.1007/s00265-008-0706-1
Kraaijeveld K, Katsoyannos BI, Stavrinides M, Kouloussis NA, Chapman T (2005) Remating in wild females of the Mediterranean fruit fly, Ceratitis capitata. Anim Behav 69:771–776. doi:10.1016/j.anbehav.2004.06.015
Miller SA, Dykes DD, Polesky HF (1988) A simple salting out procedure for extracting DNA from human nucleated cells. Nucleic Acids Res 16:1215. doi:10.1093/nar/16.3.1215
Minkenberg OPJM, Tatar M, Rosenheim JA (1992) Egg load as a major source of variability in insect foraging and oviposition behaviour. Oikos 65:134–142. doi:10.2307/3544896
Molbo D, Machado CA, Herre EA, Keller L (2004) Inbreeding and population structure in two pairs of cryptic fig wasp species. Mol Ecol 13:1613–1623. doi:10.1111/j.1365-294X.2004.02158.x
Muth A (2007) Control of Philornis downsi, bird parasite. Report for Department of Terrestrial Invertebrates, Charles Darwin Research Station, Santa Cruz
Otranto D, Stevens JR (2002) Molecular approaches to the study of myiasis-causing larvae. Int J Parasitol 32:1345–1360. doi:10.1016/S0020-7519(02)00095-4
Peakall R, Smouse PE (2006) Genalex 6: genetic analysis in Excel: population genetic software for teaching and research. Mol Ecol Notes 6:288–295. doi:10.1111/j.1471-8286.2005.01155.x
Puustinen S, Koskela T, Mutikainen P (2004) Relatedness affects competitive performance of a parasitic plant (Cuscuta europaea) in multiple infections. J Evol Biol 17:897–903. doi:10.1111/j.1420-9101.2004.00728.x
Queller DC, Goodnight KF (1989) Estimating relatedness using genetic markers. Evol Int J Org Evol 43:258–275. doi:10.2307/2409206
Raymond M, Rousset F (1995) GENEPOP (version 1.2): population genetics software for exact tests and ecumenicism. J Hered 86:248–249
Roderick GK (1996) Geographic structure of insect populations: gene flow, phylogeography, and their uses. Annu Rev Entomol 41:325–352. doi:10.1146/annurev.en.41.010196.001545
Schlüns EA, Wegener BJ, Schlüns H, Azuma N, Robson SKA, Crozier RH (2008) Breeding system, colony and population structure in the weaver ant (Oecophylla smaragdina). Mol Ecol 18:156–167. doi:10.1111/j.1365-294X.2008.04020.x
Song SD, Drew RAI, Hughes JM (2007) Multiple paternity in a natural population of a wild tobacco fly, Bactrocera cacuminata (Diptera: Tephritidae), assessed by microsatellite DNA markers. Mol Ecol 16:2353–2361. doi:10.1111/j.1365-294X.2007.03277.x
Steiner L, Harris EJ, Mitchell WC, Fujimoto MS, Christenson LD (1965) Melon fly eradication by overflooding with sterile flies. J Econ Entomol 58:519–522
Stephens PA, Sutherland WJ (1999) Consequences of the Allee effect for behaviour, ecology and conservation. Trends Ecol Evol 14:401–405. doi:10.1016/S0169-5347(99)01684-5
Teixeira D (1999) Myiasis caused by obligatory parasites Ib. General observations on the biology of species of the genus Philornis Meinert, 1890 (Diptera, Muscidae). In: Guimarães JH, Papavero N (eds) Myiasis in man and animals in the Neotropical Region; Bibliographic Database Editora Plêiade/FAPESP, São Paulo, pp 71–96
Vreyson MJ, Hendrichs J, Enkerlin WR (2006) The sterile insect technique as a component of sustainable area-wide integrated pest management of selected horticultural insect pests. J Fruit Ornam Plant Res 14:107–131
Wang J (2004) Sibship reconstruction from genetic data with typing errors. Genetics 166:1963–1979. doi:10.1534/genetics.166.4.1963
Wiedenfeld DA, Jiménez GA, Fessl B, Kleindorfer S, Valarezo JC (2007) Distribution of the introduced parasitic fly Philornis downsi (Diptera, Muscidae) in the Galápagos Islands. Pac Conserv Biol 13:14–19
Wikelski M, Foufopoulos J, Vargas H, Snell H (2004) Galápagos birds and diseases: invasive pathogens as threats for island species. Ecol Soc 9 (1), article 5. [online] URL: http://www.ecologyandsociety.org/vol9/iss1/art5
Witzgall P (2001) Phereomones—future techniques for insect control? Int Organ Biol Control (WPRS) Bull 24:114–122
Zavodna M, Knapp SM, Compton SG et al (2007) Reconstruction of fig wasp mating structure: how many mothers share a fig? Ecol Entomol 32:485–491. doi:10.1111/j.1365-2311.2007.00906.x
Zouros E, Krimbas CB (1970) Frequency of female digamy in a natural population of the olive fruit fly Dacus oleae as found by using enzyme polymorphism. Entomol Exp Appl 13:1–9. doi:10.1007/BF00304158
Acknowledgments
We thank the Galápagos National Park Service and the Charles Darwin Research Station for the opportunity to work on the Galápagos Archipelago. We thank: Birgit Fessl, David Wiedenfeld, Carlos Vinueza, Gustavo Jiménez, Carlos Santos, Rebekah Christensen, Jody O’Connor, Katherine Goss and Jeremy Robertson for their dedicated field assistance and Kathy Saint for molecular technical advice. We thank the community of Floreana Island for their invaluable support throughout the project. TAME airlines provided reduced airfares to the Galápagos. This study was funded by a Flinders University Establishment Grant to SK, the Max Planck Institute for Ornithology, Galápagos Conservation Trust, American Bird Conservancy and Conservation International. We thank anonymous reviewers for helpful comments on previous versions of this manuscript.
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Dudaniec, R.Y., Gardner, M.G. & Kleindorfer, S. Offspring genetic structure reveals mating and nest infestation behaviour of an invasive parasitic fly (Philornis downsi) of Galápagos birds. Biol Invasions 12, 581–592 (2010). https://doi.org/10.1007/s10530-009-9464-x
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DOI: https://doi.org/10.1007/s10530-009-9464-x