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A well-studied parasitoid fly of field crickets uses multiple alternative hosts in its introduced range

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A Correction to this article was published on 21 January 2023

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Abstract

Organisms and their natural enemies can have dynamic coevolutionary trajectories, but anthropogenic effects like species introductions interrupt existing coevolutionary relationships. For parasites in particular, if they are introduced to a location without their hosts, they can only persist in the new environment if alternative hosts are (1) present, (2) detectable to parasites, and (3) capable of sustaining parasites. The circumstances surrounding the addition of alternative hosts to a parasite’s repertoire are rarely observed. The parasitoid fly Ormia ochracea locates its field cricket hosts by orienting acoustically to their conspicuous mating songs. In Hawaii, O. ochracea is only known to parasitize one species, Teleogryllus oceanicus, but rapid evolution of T. oceanicus mating song over the past 20 years has led to several prevalent morphs of the cricket that produce no song or novel songs that the flies cannot detect. Yet flies persist in populations that lack ancestral singing T. oceanicus, prompting us to investigate the possibility of alternative hosts in Hawaii. We demonstrate first that three potential alternative hosts (Gryllodes sigillatus, Gryllus bimaculatus, and Modicogryllus pacificus) are present. Second, O. ochracea exhibits a positive phonotactic response to all three species’ songs in the field and in the lab. And third, O. ochracea can successfully develop to pupae and emerge as adults in all three species. Our discovery of alternative hosts for O. ochracea in Hawaii infuses the system with intriguing complexity and offers extensive opportunities for future work.

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Data availability

Data can be found in Dryad: https://doi.org/10.5061/dryad.8gtht76sx. All sequences were deposited in NCBI GenBank (OP942437-OP942441).

Code availability:

RMarkdown file can be found in Dryad: https://doi.org/10.5061/dryad.8gtht76sx.

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References

  • Adamo SA, Robert D, Hoy RR (1995) Effects of a tachinid parasitoid, Ormia ochracea, on the behaviour and reproduction of its male and female field cricket hosts (Gryllus spp.). J Insect Physiol 41:269–277

    Article  CAS  Google Scholar 

  • Ashby B, Iritani R, Best A et al (2019) Understanding the role of eco-evolutionary feedbacks in host-parasite coevolution. J Theor Biol 464:115–125

    Article  PubMed  Google Scholar 

  • Bartholomew JL, Reno PW (2002) The history and dissemination of whirling disease. In: American fisheries society symposium. American Fisheries Society, pp 3–24

  • Betts A, Rafaluk C, King KC (2016) Host and parasite evolution in a Tangled Bank. Trends Parasitol 32:863–873

    Article  PubMed  Google Scholar 

  • Bradley CA, Altizer S (2007) Urbanization and the ecology of wildlife diseases. Trends Ecol Evol 22:95–102

    Article  PubMed  Google Scholar 

  • Broder ED, Gallagher JH, Wikle AW et al (2022) Behavioral responses of a parasitoid fly to rapidly evolving host signals. Ecol Evol 12. https://doi.org/10.1002/ece3.9193

  • Broder ED, Wikle AW, Gallagher JH, Tinghitella RM (2021) Substrate-borne vibration in Pacific field cricket courtship displays. J Orthoptera Res 30:43–50

    Article  Google Scholar 

  • Cade W (1975) Acoustically Orienting Parasitoids: fly Phonotaxis to Cricket Song. Science 190:1312–1313

    Article  Google Scholar 

  • Cade WH, Ciceran M, Murray A-M (1996) Temporal patterns of parasitoid fly (Ormia ochracea) attraction to field cricket song (Gryllus integer). Can J Zool 74:393–395

    Article  Google Scholar 

  • Carton Y, Nappi AJ, Poirie M (2005) Genetics of anti-parasite resistance in invertebrates. Dev Comp Immunol 29:9–32

    Article  CAS  PubMed  Google Scholar 

  • Chalkowski K, Lepczyk CA, Zohdy S (2018) Parasite Ecology of Invasive Species: conceptual Framework and New Hypotheses. Trends Parasitol 34:655–663

    Article  PubMed  Google Scholar 

  • Chapman JW, Dumbauld BR, Itani G, Markham JC (2012) An introduced asian parasite threatens northeastern Pacific estuarine ecosystems. Biol Invasions 14:1221–1236

    Article  Google Scholar 

  • Evenhuis NL (2003) The status of the cricket parasites Ormia ochracea and Phasioormia pallida in the Hawaiian Islands (Diptera: Tachinidae). Bish Mus Occ Pap 74:34–35

    Google Scholar 

  • Gallagher JH, Zonana DM, Broder ED et al (2022) Decoupling of sexual signals and their underlying morphology during rapid phenotypic diversification. Evolution Letters

  • Gandon S (2004) Evolution of multihost parasites. Evolution 58:455–469

    PubMed  Google Scholar 

  • Gray DA, Banuelos C, Walker SE et al (2007) Behavioural specialization among populations of the acoustically orienting parasitoid fly Ormia ochracea utilizing different cricket species as hosts. Anim Behav 73:99–104

    Article  Google Scholar 

  • Gray DA, Kunerth HD, Zuk M et al (2019) Molecular biogeography and host relations of a parasitoid fly. Ecol Evol 9:11476–11493

    Article  PubMed  PubMed Central  Google Scholar 

  • Heinen-Kay JL, Zuk M (2019) When Does Sexual Signal Exploitation Lead to Signal Loss? Frontiers in Ecology and Evolution 7.: https://doi.org/10.3389/fevo.2019.00255

  • Heinze G, Ploner M, Dunkler D et al (2022) Package ‘logistf’

  • Hellgren O, Pérez-Tris J, Bensch S (2009) A jack-of‐all‐trades and still a master of some: prevalence and host range in avian malaria and related blood parasites. Ecology

  • Hoberg EP, Brooks DR (2008) A macroevolutionary mosaic: episodic host-switching, geographical colonization and diversification in complex host-parasite systems. J Biogeogr 35:1533–1550

  • Illingworth JF (1927) Insects collected in the pineapple growing section on the island of Lanai, August, 1927. Proc Haw Ent Soc VII

  • Ingrisch S (1998) The genera Velarifictorus, Modicogryllus and Mitius in Thailand (Ensifera: Gryllidae, Gryllinae). Insect Syst Evol 29(3):315–359

    Article  Google Scholar 

  • Jaenike J, Dombeck I (1998) General-purpose genotypes for host species utilization in a nematode parasite of Drosophila. Evolution 52:832–840

    Article  PubMed  Google Scholar 

  • Janzen DH (1980) When is it coevolution? Evolution 34:611–612

    Article  PubMed  Google Scholar 

  • Johnson KP, Adams RJ, Page RDM, Clayton DH (2003) When do parasites fail to speciate in response to host speciation? Syst Biol 52:37–47

    Article  PubMed  Google Scholar 

  • Kevan DK (1990) Introduced grasshoppers and crickets in Micronesia. Bol Sanid Veg Plagas

  • Kirk RS (2003) The impact of Anguillicola crassus on european eels. Fish Manag Ecol 10:385–394

    Article  Google Scholar 

  • König K, Krimmer E, Brose S et al (2015) Does early learning drive ecological divergence during speciation processes in parasitoid wasps? Proc Biol Sci 282:20141850

    PubMed  PubMed Central  Google Scholar 

  • Kostarakos K, Hennig MR, Römer H (2009) Two matched filters and the evolution of mating signals in four species of cricket. Front Zool 6:22

    Article  PubMed  PubMed Central  Google Scholar 

  • Lankheet MJ, Cerkvenik U, Larsen ON, van Leeuwen JL (2017) Frequency tuning and directional sensitivity of tympanal vibrations in the field cricket Gryllus bimaculatus. J R Soc Interface 14. https://doi.org/10.1098/rsif.2017.0035

  • Lehmann GUC (2003) Review of biogeography, host range and evolution of acoustic hunting in Ormiini (Insecta, Diptera, Tachinidae), parasitoids of night-calling bushcrickets and crickets (Insecta, Orthoptera, Ensifera). Zoologischer Anzeiger-A Journal of Comparative Zoology 242:107–120

    Article  Google Scholar 

  • Lenth R (2019) Emmeans: Estimated marginal means, aka least-squares means. Retrieved from https://CRAN.R-project.org/package=emmeans

  • Libersat F, Murray JA, Hoy RR (1994) Frequency as a releaser in the courtship song of two crickets, Gryllus bimaculatus (de Geer) and Teleogryllus oceanicus: a neuroethological analysis. J Comp Physiol A 174:485–494

    Article  CAS  PubMed  Google Scholar 

  • Lymbery AJ, Morine M, Kanani HG et al (2014) Co-invaders: the effects of alien parasites on native hosts. Int J Parasitol Parasites Wildl 3:171–177

    Article  PubMed  PubMed Central  Google Scholar 

  • Miyashita A, Kizaki H, Sekimizu K, Kaito C (2016) No effect of body size on the frequency of calling and courtship song in the two-spotted cricket, Gryllus bimaculatus. PLoS ONE 11:e0146999

    Article  PubMed  PubMed Central  Google Scholar 

  • Montealegre-Z F, Windmill JFC, Morris GK, Robert D (2009) Mechanical phase shifters for coherent acoustic radiation in the stridulating wings of crickets: the plectrum mechanism. J Exp Biol 212:257–269

    Article  PubMed  Google Scholar 

  • Murdoch WW (1969) Switching in general predators: experiments on predator specificity and stability of prey populations. Ecol Monogr 39:335–354

    Article  Google Scholar 

  • Otte D (1994) The crickets of Hawaii: Origin, Systematics, and evolution. The Orthopterists’ Society; Academy of Natural Sciences., Philadelphia, PA

    Google Scholar 

  • Pascoal S, Cezard T, Eik-Nes A et al (2014) Rapid convergent evolution in wild crickets. Curr Biol 24:1369–1374

    Article  CAS  PubMed  Google Scholar 

  • Paterson AM, Gray RD (1997) Host-parasite co-speciation, host switching, and missing the boat. Host-parasite evolution: General principles and avian models 236–250

  • Paur J, Gray DA (2011) Individual consistency, learning and memory in a parasitoid fly, Ormia ochracea. Anim Behav 82:825–830

    Article  Google Scholar 

  • Prenter J, Macneil C, Dick JTA, Dunn AM (2004) Roles of parasites in animal invasions. Trends Ecol Evol 19:385–390

    Article  PubMed  Google Scholar 

  • Rayner JG, Aldridge S, Montealegre-Z F, Bailey NW (2019) A silent orchestra: convergent song loss in hawaiian crickets is repeated, morphologically varied, and widespread. Ecology 100:e02694

    Article  PubMed  Google Scholar 

  • Rehn JA, Hebard M (1905) A contribution to the knowledge of the Orthoptera of South and Central Florida.Proc Acad Nat Sci Philadelphia29–55

  • Robert D, Amoroso J, Hoy RR (1992) The evolutionary convergence of hearing in a parasitoid fly and its cricket host. Science 258:1135–1137

    Article  CAS  PubMed  Google Scholar 

  • Sakaluk SK (1987) Reproductive Behaviour of the decorated cricket, Gryllodes Supplicans (Orthoptera: Gryllidae): calling schedules, spatial distribution, and mating. Behaviour 100:202–225

    Article  Google Scholar 

  • Sakaluk SK, Belwood JJ (1984) Gecko phonotaxis to cricket calling song: a case of satellite predation. Anim Behav 32:659–662

    Article  Google Scholar 

  • Santiago-Alarcon D, Merkel J (2018) New host-parasite Relationships by host-switching. In: Parker PG (ed) Disease Ecology: Galapagos Birds and their parasites. Springer International Publishing, Cham, pp 157–177

    Chapter  Google Scholar 

  • Simmons LW (1988) The calling song of the field cricket, Gryllus bimaculatus (de geer): constraints on transmission and its role in intermale competition and female choice. Anim Behav 36:380–394

    Article  Google Scholar 

  • Strauss SY, Sahli H, Conner JK (2005) Toward a more trait-centered Approach to diffuse (Co)evolution. New Phytol 165:81–89

    Article  PubMed  Google Scholar 

  • Tanner JC, Swanger E, Zuk M (2019) Sexual signal loss in field crickets maintained despite strong sexual selection favoring singing males. Evolution 73:1482–1489

    Article  PubMed  Google Scholar 

  • Ter Hofstede HM, Ratcliffe JM (2016) Evolutionary escalation: the bat–moth arms race. J Exp Biol 219:1589–1602

    Article  PubMed  Google Scholar 

  • Thomson IR, Vincent CM, Bertram SM (2012) Success of the Parasitoid Fly Ormia ochracea (Diptera: Tachinidae) on Natural and Unnatural Cricket Hosts. flen 95:43–48

  • Tinghitella RM, Broder ED, Gallagher JH et al (2021) Responses of intended and unintended receivers to a novel sexual signal suggest clandestine communication. Nat Commun 12:797

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Tinghitella RM, Broder ED, Gurule-Small GA et al (2018) Purring crickets: the evolution of a novel sexual Signal. Am Nat 192:773–782

    Article  PubMed  Google Scholar 

  • Torchin ME, Lafferty KD, Dobson AP et al (2003) Introduced species and their missing parasites. Nature 421:628–630

    Article  CAS  PubMed  Google Scholar 

  • Vincent CM, Bertram SM (2009) The Parasitoid Fly Ormia ochracea (Diptera: Tachinidae) Can Use Juvenile Crickets as Hosts. Fla Entomol 92:598–600

  • Vincent CM, Bertram SM (2010) Collection and Laboratory Culture of Ormia ochracea (Diptera: Tachinidae). J Entomol Sci 45:1–7

    Google Scholar 

  • Vinson SB (1990) How parasitoids deal with the immune system of their host: an overview. Arch Insect Biochem Physiol 13(1:2):3–27

    Article  Google Scholar 

  • Walker TJ (1989) A live trap for monitoring Euphasiopteryx and tests with E. ochracea (Diptera: Tachinidae). Fla Entomol 72:314–319

    Article  Google Scholar 

  • Wineriter SA, Walker TJ (1990) Rearing phonotactic parasitoid flies [Diptera: Tachinidae, ormiini, ormia spp.]. Entomophaga 35:621–632

  • Woolhouse ME, Taylor LH, Haydon DT (2001) Population biology of multihost pathogens. Science 292:1109–1112

    Article  CAS  PubMed  Google Scholar 

  • Zuk M, Bailey NW, Gray B, Rotenberry JT (2018) Sexual signal loss: the link between behaviour and rapid evolutionary dynamics in a field cricket. J Anim Ecol 87:623–633

    Article  PubMed  Google Scholar 

  • Zuk M, Rotenberry JT, Tinghitella RM (2006) Silent night: adaptive disappearance of a sexual signal in a parasitized population of field crickets. Biol Lett 2:521–524

    Article  PubMed  PubMed Central  Google Scholar 

  • Zuk M, Simmons LW, Cupp L (1993) Calling characteristics of parasitized and unparasitized populations of the field cricket Teleogryllus oceanicus. Behav Ecol Sociobiol 33:339–343

    Google Scholar 

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Acknowledgements

We would like to thank the group of people who helped us identify Modicogryllus pacificus. Specifically, Daniel Otte advised on dissection methods and visually confirmed the identification of the species. Our research in Kalaupapa National Park would not have been possible without support from Pastor Richard, Sister Barbara Jean, Sister Damien Alisha, Nancy Holman, Kelly Moore, and Rosa Key, as well as support from community members including Glauco, Tim, Kristen, and picturesque Mackenzie. We acknowledge that the land on which these data were collected, Hawaii, is part of the larger territory recognized by indigenous Hawaiians as their ancestral grandmother, Papahānaumoku. We recognize that generations of indigenous Hawaiians and their knowledge systems shaped Hawaii in a sustainable way that allow us to enjoy her gifts today. For this, we are truly grateful (land acknowledgement from University of Hawai’i Manoa). This work was supported by funding from the National Science Foundation to RMT (IOS 1846520 and DEB 2012041), DMZ (DBI 2010983), TJF (DBI 2208825), and a Graduate Research Fellowship Program grant to AWW). Personnel on this project were also supported by a Morris Animal Foundation grant to RMT (D20ZO-025).

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EDB: Conceptualization (lead), Data curation (equal), Formal analysis (supporting), Investigation (equal), Methodology (equal), Project administration (lead), Supervision (lead), Visualization (lead), Writing-first draft (lead), Writing-reviewing and editing (lead); JHG: Conceptualization (equal), Investigation (equal), Methodology (equal), Visualization (supporting), Writing-first draft (supporting), Writing-reviewing and editing (equal); AWW: Conceptualization (equal), Data curation (equal), Formal analysis (lead), Investigation (equal), Writing-reviewing and editing (supporting); GTW: Investigation (equal), Methodology (equal), Formal analysis (equal), Writing-first draft (supporting), Writing-reviewing and editing (equal); DMZ: Investigation (equal), Formal analysis (equal), Writing-reviewing & editing (equal); TJF: Investigation (equal), Methodology (equal), Formal analysis (supporting), Writing-reviewing and editing (supporting); RMT: Conceptualization (equal), Investigation (equal), Methodology (equal), Visualization (supporting), Writing-first draft (supporting), Writing-reviewing and editing (equal), Supervision (equal), Project administration (equal), Funding acquisition (lead).

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Correspondence to E Dale Broder.

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James H Gallagher, Aaron W Wikle and Gabrielle T Welsh contributed equally

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Broder, E.D., Gallagher, J.H., Wikle, A.W. et al. A well-studied parasitoid fly of field crickets uses multiple alternative hosts in its introduced range. Evol Ecol 37, 477–492 (2023). https://doi.org/10.1007/s10682-022-10225-1

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