Abstract
Invasive species are one of the greatest threats to biodiversity, with endemic species on islands being at particular risk. Management programs can help to minimize these impacts, but such programs are most successful when they are well-informed. In the Galápagos Islands, Ecuador, a recently introduced avian parasitic fly, Philornis downsi, has had strong negative effects on the survival of multiple endemic bird species, including several species of Darwin’s finches. The fly now populates most of the major islands within the Archipelago and the need to better understand the population structure and connectivity patterns of this invasive fly has become increasingly apparent as various management efforts are being considered. Here, we use genomic and phylogenetic approaches to estimate population structure and connectivity for P. downsi collected from five islands within the Galápagos Islands and several sites in mainland Ecuador, which is the presumptive origin of the invasive population. Genomic data showed very little genetic differentiation between island populations of P. downsi relative to the mainland. Phylogenetic analyses, which used more conservative genetic markers than the genomics approach, showed that island and mainland populations of flies were highly related. Our study provides some of the first results using genetic data to quantify differentiation among mainland and island populations of P. downsi. In addition, our study found very little genetic differentiation between island populations of flies, suggesting that there may be considerable gene flow among islands; however, further sampling is needed to determine the extent to which this could be occurring. As management techniques aimed at controlling the impact of this parasite on endemic bird populations are being considered, our study provides important insights into the history of P. downsi’s invasion to the Galápagos Islands and current population connectivity patterns.
Similar content being viewed by others
References
Abdelkrim J, Pascal M, Calmet C, Samadi S (2005) Importance of assessing population genetic structure before eradication of invasive species: examples from insular Norway rat populations. Conserv Biol 19:1509–1518
Akaike H (1973) Information theory and an extension of the maximum likelihood principle. In: Petrov BN, Csaki F (eds) Proceedings of second international symposium on information theory. Akademia Kiado, Budapest, pp 267–281
Boulton RA, Bulgarella M, Ramirez IE, Causton CE (2019) Management of the invasive avian parasitic fly, Philornis downsi, in the Galapagos Islands: is biological control a viable option? In: Veitch CR, Clout MN, Martin AR, Russell JC, West CJ (eds) Island Invasives: scaling up to meet the challenge. IUCN, Gland, pp 360–363
Bulgarella M, Quiroga MA, Boulton RA, Ramirez IE, Moon RD, Causton CE, Heimpel GE (2017) Life cycle and host specificity of the parasitoid Conura annulifera (Hymenoptera: Chalcididae), a potential biological control agent of Philornis downsi (Diptera: Muscidae) in the Galapagos Islands. Ann Entomol Soc Am 110:317–328
Bulgarella M, Quiroga MA, Brito vera GA, Dregni JS, Cunningham F, Mosquera Munoz DA, Monje LD, Causton CE, Heimpel GE (2015) Philornis downsi (Diptera: Muscidae), an avian nest parasite invasive to the Galapagos Islands, in mainland Ecuador. Ann Entomol Soc Am 108(3):248–250
Bulgarella M, Quiroga MA, Heimpel GE (2019) Additive negative effects of Philornis nest parasitism on small and declining Neotropical bird populations. Bird Conserv Int 29:339–360
Catchen J, Hohenlohe P, Bassham S, Amores A, Cresko W (2013) Stacks: an analysis tool set for population genomics. Mol Ecol 22:3124–3140
Causton CE, Moon RD, Cimadom A, Boulton RA, Cedeno D, Lincango MP, Tebbich S, Ulloa A (2019) Population dynamics of an invasive bird parasite, Philornis downsi (Diptera: Muscidae), in the Galapagos Islands. PLoS ONE 14:e0224125
Causton CE, Sevilla CR, Porter SD (2005) Eradication of the little fire ant, Wasmannia auropunctata (Hymenoptera: Formicidae), from Marchena Island, Galapagos: on the edge of success? Fla Entomol 88:159–168
Cha DH, Mieles AE, Lahuatte PF, Cahuana A, Lincango MP, Causton CE, Tebbich S, Cimadom A, Teale SA (2016) Identification and optimization of microbial attractants for Philornis downsi, an invasive fly parasitic on Galapagos birds. J Chem Ecol 42:1101–1111
Charles H, Dukes JS (2008) Impacts of invasive species on ecosystem services. Springer, Berlin
Cimadom A, Causton C, Cha DH, Damiens D, Fessl B, Hood-Nowotny R, Lincango P, Mieles AE, Nemeth E, Semler EM, Teale SA, Tebbich S (2016) Darwin’s finches treat their feathers with a natural repellent. Sci Rep 6:34559
Cimadom A, Ulloa A, Meidl P, Zottl M, Zottl E, Fessl B, Nemeth E, Dvorak M, Cunninghame F, Tebbich S (2014) Invasive parasites, habitat change and heavy rainfall reduce breeding success in Darwin’s finches. PLoS ONE 9(9):e107518
Common LK, Dudaniec RY, Colombelli-Negrel D, Kleindorfer S (2019) Taxonomic shifts in Philornis larval behaviour and rapid changes in Philornis downsi Dodge & Aitken (Diptera: Muscidae): an invasive avian parasite on the Galápagos Islands. In: Sarwar M (ed) Life cycle and development of Diptera. InTech Open, London
Common LK, O’Connor JA, Dudaniec RY, Peters KJ, Kleindorfer S (2020) Evidence for rapid downward fecundity selection in an ectoparasite (Philornis downsi) with earlier host mortality in Darwin’s finches. J Evol Biol 33(4):524–533
Couri MS (1999) Myiasis caused by obligatory parasites. 1a. Philornis Meinert (Muscidae). In: Guimaraes JH, Papavero N (eds) Myiasis in man and animals in the Neotropical region. Bibliographic data base. FAPESP, Sao Paulo, pp 51–70
Cruz F, Donlan CJ, Campbell K, Carrion V (2005) Conservation action in the Galapagos: feral pig (Sus scrofa) eradication from Santiago Island. Biol Conserv 121:473–478
Cunninghame F, Fessl B, Sevilla CR, Young GR, La Greco N (2017) Manejo de la conservacion a largo plazo para salvar al pinzon de manglar (Camarhynchus heliobates) en peligro critico de extincion. In: Informe Galapagos 2015–2016. DPNG, CGREG, FCD and GC, Puerto Ayora, Galapagos, pp 163–170
Danecek P, Auton A, Abecasis G, Albers CA, Banks E, DePristo MA, Handsaker RE, Lunter G, Marth GT, Sherry ST, McVean G, Durbin R, Genomes Project Analysis Group (2011) The variant call format and VCF tools. Bioinformatics 27:2156–2158
de Carvalho M, Couri M (1999) New associations between Philornis Meinert (Diptera, Muscidae) and Thamnophilidae (Aves, Passeriformes). Rev Bras Zool 16(4):116
Dodge HR, Aitken THG (1968) Philornis flies from Trinidad (Diptera: Muscidae). J Kans Entomol Soc 41:134–154
Doherty TS, Glen AS, Nimmo DG, Ritchie EG, Dickman CR (2016) Invasive predators and global biodiversity loss. Proc Natl Acad Sci USA 113:11261–11265
Dudaniec RY, Fessl B, Kleindorfer S (2007) Interannual and interspecific variation in intensity of the parasitic fly, Philornis downsi, in Darwin’s finches. Biol Conserv 139:325–332
Dudaniec RY, Gardner MG, Donnellan S, Kleindorfer S (2008) Genetic variation in the invasive avian parasite, Philornis downsi (Diptera, Muscidae) on the Galapagos Archipelago. BMC Ecol 8:13
Dudaniec RY, Gardner MG, Kleindorfer S (2010) Offspring genetic structure reveals mating and nest infestation behaviour of an invasive parasitic fly (Philornis downsi) of Galapagos birds. Biol Invasions 12:581–592
Dvorak M, Vargas H, Fessl B, Tebbich S (2004) On the verge of extinction: a survey of the mangrove finch Cactospiza heliobates and its habitat on the Galápagos Islands. Oryx 38:1–9
Etter PD, Bassham S, Hohenlohe PA, Johnson EA, Cresko WA (2011) SNP discovery and genotyping for evolutionary genetics using RAD sequencing. In: Orgogozo V, Rockman MV (eds) Molecular methods for evolutionary genetics SE-9. Humana Press, Totowa, pp 157–178
Evanno G, Regnaut S, Goudet J (2005) Detecting the number of clusters of individuals using the software STRUCTURE: a simulation study. Mol Ecol 14:2611–2620
Felsenstein J (1985) Confidence-limits on phylogenies—an approach using the bootstrap. Evolution 39:783–791
Fessl B, Couri MS, Tebbich S (2001) Philornis downsi Dodge & Aitken, new to the Galapagos Islands, (Diptera, Muscidae). Stud Dipterol 8:317–322
Fessl B, Heimpel G, Causton C (2018) Invasion of an avian nest parasite, Philornis downsi, to the Galapagos Islands: colonization history, adaptations to novel ecosystems, and conservation challenges. In: Parker P (ed) Disease ecology, social and ecological interactions in the Galapagos Islands. Springer, Cham
Fessl B, Sinclair BJ, Kleindorfer S (2006) The life-cycle of Philornis downsi (Diptera: Muscidae) parasitizing Darwin’s finches and its impacts on nestling survival. Parasitology 133:739–747
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
Foll M, Gaggiotti O (2008) A genome-scan method to identify selected loci appropriate for both dominant and codominant markers: a Bayesian perspective. Genetics 180:977–993
Goslee SC, Urban DL (2007) The ecodist package for dissimilarity-based analysis of ecological data. J Stat Softw 22:1–19
Goudet J (2005) hierfstat, a package for r to compute and test hierarchical F-statistics. Mol Ecol Notes 5:184–186
Grant PR (1999) Ecology and evolution 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
Heimpel GE (2017) Could biological control protect Darwin’s finches from an invasive parasite? Biocontrol News Inf 38:21N–22N
Heimpel GE, Hillstrom A, Freund D, Knutie SA, Clayton DH (2017) Invasive parasites and the fate of Darwin’s finches in the Galapagos Islands: the case of the vegetarian finch (Platyspiza crassirostris). Wilson J Ornithol 129:345–349
Heimpel GE, Mills NJ (2017) Biological control: ecology and applications. Cambridge University Press, Cambridge
Hejda M, Hanzelka J, Kadlec T, Strobl M, Pysek P, Reif J (2017) Impacts of an invasive tree across trophic levels: species richness, community composition and resident species’ traits. Divers Distrib 23:997–1007
Hendrichs HJ, Franz G, Rendon P (1995) Increased effectiveness and applicability of the sterile insect technique through male-only releases for control of Mediterranean fruit flies during fruiting seasons. J Appl Entomol 119:371–377
Huelsenbeck JP, Ronquist F (2001) MRBAYES: Bayesian inference of phylogenetic trees. Bioinformatics 17:754–755
Hufbauer RA, Roderick GK (2005) Microevolution in biological control: mechanisms, patterns, and processes. Biol Control 35:227–239
Hulme PE (2009) Trade, transport and trouble: managing invasive species pathways in an era of globalization. J Appl Ecol 46:10–18
Janes JK, Miller JM, Dupuis JR, Malenfant RM, Gorrell JC, Cullingham CI, Andrew RL (2017) The K = 2 conundrum. Mol Ecol 26:3594–3602
Jimenez-Uzcategui G, Llerena W, Milstead WB, Lomas EE, Wiedenfeld DA (2011) Is the population of Floreana Mockingbird Mimus trifasciatus declining? Cotinga 33(1):1–7
Jombart T (2008) adegenet: a R package for the multivariate analysis of genetic markers. Bioinformatics 24:1403–1405
Jombart T, Devillard S, Balloux F (2010) Discriminant analysis of principal components: a new method for the analysis of genetically structured populations. BMC Genet 11:94
Jones HP, Holmes ND, Butchart SHM, Tershy BR, Kappes PJ, Corkery I, Aguirre-Munoz A, Armstrong DP, Bonnaud E, Burbidge AA, Campbell K, Courchamp F, Cowan PE, Cuthbert RJ, Ebbert S, Genovesi P, Howald GR, Keitt BS, Kress SW, Miskelly CM, Oppel S, Poncet S, Rauzon MJ, Rocamora G, Russell JC, Samaniego-Herrera A, Seddon PJ, Spatz DR, Towns DR, Croll DA (2016) Invasive mammal eradication on islands results in substantial conservation gains. Proc Natl Acad Sci USA 113:4033–4038
Kamvar ZN, Tabima JF, Grunwald NJ (2014) Poppr: an R package for genetic analysis of populations with clonal, partially clonal, and/or sexual reproduction. PeerJ 2:e281
Klassen W, Curtis C (2005) History of the sterile insect technique. In: Dyck V, Hendrichs J, Robinson A (eds) Sterile insect technique principles and practice in area-wide integrated pest management. Springer, Dordrecht, pp 3–36
Kleindorfer S, Dudaniec RY (2016) Host–parasite ecology, behavior and genetics: a review of the introduced fly parasite Philornis downsi and its Darwin’s finch hosts. BMC Zool 1:1
Kleindorfer S, Sulloway F (2016) Naris deformation in Darwin’s finches: experimental and historical evidence for a post-1960s arrival of the parasite Philornis downsi. Glob Ecol Conserv 7:122–131
Knutie SA, McNew SM, Bartlow AW, Vargas DA, Clayton DH (2014) Darwin’s finches combat introduced nest parasites with fumigated cotton. Curr Biol 24:R355–R356
Koop JAH, Huber SK, Laverty SM, Clayton DH (2011) Experimental demonstration of the fitness consequences of an introduced parasite of Darwin’s finches. PLoS ONE 6:e19706. https://doi.org/10.11371/journal.pone.0019706
Koop JAH, Kim PS, Knutie SA, Adler F, Clayton DH (2015) Introduced parasitic fly may lead to local extinction of Darwin’s finch populations. J Appl Ecol 53(2):511–518
Koop JAH, Le Bohec C, Clayton DH (2013) Dry year does not reduce invasive parasitic fly prevalence or abundance in Darwin’s finch nests. Rep Parasitol 3:11–17
Kopelman NM, Mayzel J, Jakobsson M, Rosenberg NA, Mayrose I (2015) Clumpak: a program for identifying clustering modes and packaging population structure inferences across K. Mol Ecol Resour 15:1179–1191
Krafsur ES (2005) Role of population genetics in the sterile insect technique. In: Dyck VA, Hendrichs J, Robinson AS (eds) Sterile insect technique: principles and practice in area-wide integrated pest management. Springer, Dordrecht, pp 389–406
Lack D (1947) Darwin’s finches: an essay on the general biological theory of evolution. Cambridge University Press, Cambridge
Linsley E, Usinger R (1966) Insects of the Galapagos Islands. In: Proceedings of the California Academy of Sciences
Lischer HE, Excoffier L (2012) PGDSpider: an automated data conversion tool for connecting population genetics and genomics programs. Bioinformatics 28:298–299
Lomas EE (2008) Dispersion de insectos por las luces de los barcos en las islas Galapagos: una prioridad de conservacion. Universidad central del Ecuador y Fundacion Charles Darwin
Lunt DH, Zhang DX, Szymura JM, Hewitt GM (1996) The insect cytochrome oxidase I gene: evolutionary patterns and conserved primers for phylogenetic studies. Insect Mol Biol 5:153–165
McGeoch MA, Butchart SHM, Spear D, Marais E, Kleynhans EJ, Symes A, Chanson J, Hoffmann M (2010) Global indicators of biological invasion: species numbers, biodiversity impact and policy responses. Divers Distrib 16:95–108
McNew SM, Clayton DH (2018) Alien invasion: biology of Philornis flies highlighting Philornis downsi, an introduced parasite of Galapagos birds. Annu Rev Entomol 63:369–387
Meirmans PG (2015) Seven common mistakes in population genetics and how to avoid them. Mol Ecol 24:3223–3231
Meirmans PG (2019) Subsampling reveals that unbalanced sampling affects STRUCTURE results in a multi-species dataset. Heredity (Edinb) 122:276–287
Meirmans PG (2020) genodive version 3.0: easy-to-use software for the analysis of genetic data of diploids and polyploids. Mol Ecol Resour 20(4):1126–1131
Mieles AE (2018) Semiochemical attractants of the parasitic fly Philornis downsi in the Galapagos Islands. State University of New York
Monje LD, Quiroga M, Manzoli D, Couri MS, Silvestri L, Venzal JM, Cuervo P, Beldomenico PM (2013) Sequence analysis of the internal transcribed spacer 2 (ITS2) from Philornis seguyi (Garcia, 1952) and Philornis torquans (Nielsen, 1913) (Diptera: Muscidae). Syst Parasitol 86:43–51
Mooney HA (2005) Invasive Alien Species: the nature of the problem. In: Mooney HA, Mack RN, McNeely JA, Neville LE, Schei PJ, Waage JK (eds) Invasive alien species: a new synthesis. Island Press, Washington, DC, pp 1–15
Paris JR, Stevens JR, Catchen JM (2017) Lost in parameter space: a road map for stacks. Methods Ecol Evol 8:1360–1373
Peters KJ, Kleindorfer S (2018) Avian population trends in Scalesia forest on Floreana Island (2004–2013): Acoustical surveys cannot detect hybrids of Darwin’s tree finches Camarhynchus spp. Bird Conserv Int 28:319–335
Pimentel D, Zuniga R, Morrison D (2005) Update on the environmental and economic costs associated with alien-invasive species in the United States. Ecol Econ 52:273–288
Posada D, Crandall KA (1998) MODELTEST: testing the model of DNA substitution. Bioinformatics 14:817–818
R Development Core Team (2013) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna
Ragionieri L, Cutuli G, Sposimo P, Spano G, Navone A, Capizzi D, Baccetti N, Vannini M, Fratini S (2013) Establishing the eradication unit of Molara Island: a case of study from Sardinia, Italy. Biol Invasions 15:2731–2742
Raizada P, Raghubanshi AS, Singh JS (2008) Impact of invasive alien plant species on soil processes: a review. Proc Natl Acad Sci India B 78:288–298
Reaser JK, Meyerson LA, Cronk Q, De Poorter M, Eldrege LG, Green E, Kairo M, Latasi P, Mack RN, Mauremootoo J, O’Dowd D, Orapa W, Sastroutomo S, Saunders A, Shine C, Thrainsson S, Vaiutu L (2007) Ecological and socioeconomic impacts of invasive alien species in island ecosystems. Environ Conserv 34:98–111
Robertson BC, Gemmell NJ (2004) Defining eradication units to control invasive pests. J Appl Ecol 41:1042–1048
Rochette NC, Catchen JM (2017) Deriving genotypes from RAD-seq short-read data using Stacks. Nat Protoc 12:2640–2659
Rowles AD, O’Dowd DJ (2007) Interference competition by Argentine ants displaces native ants: implications for biotic resistance to invasion. Biol Invasions 9:73–85
Savidge JA, Hopken MW, Witmer GW, Jojola SM, Pierce JJ, Burke PW, Piaggio AJ (2012) Genetic evaluation of an attempted Rattus rattus eradication on Congo Cay, U.S. Virgin Islands, identifies importance of eradication units. Biol Invasions 14:2343–2354
Sax DF, Gaines SD (2008) Species invasions and extinction: the future of native biodiversity on islands. Proc Natl Acad Sci USA 105:11490–11497
Silvestri L, Antoniazzi L, Couri MS, Monje L, Beldomenico P (2010) First record of the avian ectoparasite Philornis downsi Dodge and Aitken, 1968 (Diptera: Muscidae) in Argentina. Syst Parasitol 80:137–140
Simberloff D (2013) Invasive species: what everyone needs to know. Oxford University Press, New York
Simon C, Frati F, Beckenbach A, Crespi B, Liu H, Flook P (1994) Evolution, weighting, and phylogenetic utility of mitochondrial gene-sequences and a compilation of conserved polymerase chain-reaction primers. Ann Entomol Soc Am 87:651–701
Swofford DL (2002) PAUP*: Phylogenetic analysis using parsimony (*and other methods), version 4. Sinauer Associates, Sunderland
Tershy BR, Shen KW, Newton KM, Holmes ND, Croll DA (2015) The importance of islands for the protection of biological and linguistic diversity. Bioscience 65:592–597
Toral-Granda MV, Causton CE, Jager H, Trueman M, Izurieta JC, Araujo E, Cruz M, Zander KK, Izurieta A, Garnett ST (2017) Alien species pathways to the Galapagos Islands, Ecuador. PLoS ONE 12:e0184379
Vila M, Espinar JL, Hejda M, Hulme PE, Jarosik V, Maron JL, Pergl J, Schaffner U, Sun Y, Pysek P (2011) Ecological impacts of invasive alien plants: a meta-analysis of their effects on species, communities and ecosystems. Ecol Lett 14:702–708
Vilcinskas A, Stoecker K, Schmidtberg H, Rohrich CR, Vogel H (2013) Invasive Harlequin ladybird carries biological weapons against native competitors. Science 340:862–863
Vreysen MJB, Saleh KM, Ali MY, Abdulla AM, Zhu ZR, Juma KG, Dyck VA, Msangi AR, Mkonyi PA, Feldmann HU (2000) Glossina austeni (Diptera: Glossinidae) eradicated on the Island of Unguja, Zanzibar, using the sterile insect technique. J Econ Entomol 93:123–135
Walsh JR, Carpenter SR, Vander Zanden MJ (2016) Invasive species triggers a massive loss of ecosystem services through a trophic cascade. Proc Natl Acad Sci USA 113:4081–4085
Wiedenfeld DA, Jimenez GA, Fessl B, Kleindorfer S, Valarezo JC (2007) Distribution of the introduced parasitic fly Philornis downsi (Diptera, Muscidae) in the Galapagos Islands. Pac Conserv Biol 13:14–19
Wilcove DS, Rothstein D, Dubow J, Phillips A, Losos E (1998) Quantifying threats to imperiled species in the United States. Bioscience 48:607–615
Acknowledgements
We thank Gabriel Brito, Sarah Knutie, David Anchundia, Francesca Cunninghame, Birgit Fessl, Paola Lahuatte, Courtney Pike and Ismael Ramirez for collecting and processing the flies. Thanks to Genevieve Kozak and Christy Wails for their assistance with data analyses. Permission to conduct this study was granted by the Galápagos National Park Directorate (Project PC-35-19, PC-07-18 and PC-08-17: Control of the Invasive Parasite, P. downsi and its Impact on Biodiversity) and the Ecuadorian Ministry of the Environment (MAE-DNB-CM-2016-0043). This work was funded by a Grant from the Galápagos Conservancy (Award Number 1-68-308), International Community Foundation (with a Grant awarded by The Leona M. and Harry B. Helmsley Charitable Trust) (Award Number 20140045), Lindblad Expeditions-National Geographic (Award Number 1-01-106) and National Geographic Research and Exploration Grant (Award Number 9847-16). This is contribution number 2348 of the Charles Darwin Foundation for the Galápagos Islands.
Author information
Authors and Affiliations
Corresponding author
Additional information
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Electronic supplementary material
Below is the link to the electronic supplementary material.
10592_2020_1315_MOESM2_ESM.xlsx
Supplementary file2 (XLSX 9 kb) Table S1 Locality and specimen information for the Philornis downsi samples included in thegenomics and phylogenetic studies
Rights and permissions
About this article
Cite this article
Koop, J.A.H., Causton, C.E., Bulgarella, M. et al. Population structure of a nest parasite of Darwin’s finches within its native and invasive ranges. Conserv Genet 22, 11–22 (2021). https://doi.org/10.1007/s10592-020-01315-0
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10592-020-01315-0