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Convergent evolution of intraguild predation in phytotelm-inhabiting mosquitoes

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Abstract

Intraguild predation (IGP) is a type of biological interaction involving the killing and consuming of competing species that exploit similar and often limited resources. This phenomenon is widespread among a great variety of taxonomic groups and has already been reported for mosquito (Diptera: Culicidae) larvae. Moreover, the larvae of certain mosquito species of the tribe Sabethini have evolved modified mouthparts ending in rigid apical structures signaling their capacity to be effective intraguild predators. We assumed that IGP confers a selective advantage under severe competitive conditions by both providing an immediate energetic gain and reducing potential competition. Because potential competition is likely to increase with decreasing habitat size, we hypothesized that the proportion of species with modified mouthparts would increase in smaller aquatic habitats. We tested this hypothesis by examining the mosquito species naturally associated with phytotelmata of decreasing sizes in French Guiana. We show that the degree of specialization in mosquito-phytotelm associations is high, suggesting a long coevolutive process. Indeed, short-term interaction experiments confirmed that species with modified mouthparts are able to prey upon similarly-sized intraguild prey and are, thus, effective intraguild predators. In addition, these species are larger and associated with smaller phytotelmata than those with typical mouthparts. Moreover, below a certain threshold of phytotelm size, only species with modified mouthparts were present. These results show that IGP confers a selective advantage under severe competitive conditions and results from the coadaptation of mosquito species to their specific phytotelm habitat. The presence of functionally analogous structures in different mosquito genera also implies that IGP has emerged from convergent evolution in small phytotelmata.

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References

  • Arim M, Marquet PA (2004) Intraguild predation: a widespread interaction related to species biology. Ecol Lett 7(7):557–564

    Article  Google Scholar 

  • Blüthgen N, Menzel F, Blüthgen N (2006) Measuring specialization in species interaction networks. BMC Ecol 6(1):9

    Article  PubMed  PubMed Central  Google Scholar 

  • Brown JL, Twomey E, Morales V, Summers K (2008) Phytotelm size in relation to parental care and mating strategies in two species of Peruvian poison frogs. Behaviour 145(9):1139–1165

    Article  Google Scholar 

  • Church SC, Sherratt TN (1996) The selective advantages of cannibalism in a Neotropical mosquito. Behav Ecol Sociobiol 39(2):117–123

    Article  Google Scholar 

  • Clements AN (1990) The biology of mosquitoes: development, nutrition and reproduction, vol 1. Chapman & Hall, London

    Google Scholar 

  • Dézerald O, Céréghino R, Corbara B, Dejean A, Leroy C (2015) Temperature: diet interactions affect survival through foraging behavior in a bromeliad-dwelling predator. Biotropica 47(5):569–578

    Article  Google Scholar 

  • Dunne JA, Williams RJ, Martinez ND (2002) Network structure and biodiversity loss in food webs: robustness increases with connectance. Ecol Lett 5(4):558–567

    Article  Google Scholar 

  • Dyar HG (1928) The mosquitoes of the Americas. Carnegie Institution, Washington

    Google Scholar 

  • Edgerly JS, Willey MS, Livdahl T (1999) Intraguild predation among larval treehole mosquitoes, Aedes albopictus, Ae. aegypti, and Ae. triseriatus (Diptera: Culicidae), in laboratory microcosms. J Med Entomol 36(3):394–399

    Article  CAS  PubMed  Google Scholar 

  • Fisher RA, Corbet AS, Williams CB (1943) The relation between the number of species and the number of individuals in a random sample of an animal population. J Anim Ecol 12(1):42–58

    Article  Google Scholar 

  • Funk V, Hollowell T, Berry P, Kelloff C, Alexander SN (2007) Checklist of the plants of the Guiana Shield (Venezuela: Amazonas, Bolivar, Delta Amacuro; Guyana, Surinam, French Guiana). Smithsonian Institution, Contr US Natl Herb, vol 55, pp 1–584

  • Gaffigan T, Pecor J (1997) Collecting, rearing, mounting and shipping mosquitoes. http://wrbu.si.edu/techniques.html

  • Harbach RE, Peyton EL (1993) Morphology and evolution of the larval maxilla and its importance in the classification of the Sabethini (Diptera: Culicidae). Mosq Syst 25(1):1–17

    Google Scholar 

  • Judd DD (1996) Review of the systematic and phylogenetic relationships of the Sabethini (Diptera: Culicidae). Syst Entomol 21(2):129–150

    Article  Google Scholar 

  • Juliano SA (2009) Species interactions among larval mosquitoes: context dependence across habitat gradients. Annu Rev Entomol 54(1):37–56

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kitching RL (2000) Food webs and container habitats: the natural history and ecology of phytotelmata. Cambridge University Press, Cambridge

    Book  Google Scholar 

  • Knight KL, Harbach RE, Chang MCC (1977) Maxillae of fourth stage mosquito larvae (Diptera: Culicidae). Mosq Syst 9(4):455–477

    Google Scholar 

  • Lounibos LP (1983) Behavioral convergences among fruit-husk mosquitoes. Fla Entomol 66(1):32–41

    Article  Google Scholar 

  • Merritt RW, Dadd RH, Walker ED (1992) Feeding behavior, natural food, and nutritional relationships of larval mosquitoes. Annu Rev Entomol 37(1):349–374

    Article  CAS  PubMed  Google Scholar 

  • Mogi M, Sembel DT (1996) Predator-prey system structure in patchy and ephemeral phytotelmata: aquatic communities in small aroid axils. Res Popul Ecol 38(1):95–103

    Article  Google Scholar 

  • Motta MA, Lourenço-de-Oliveira R (2000) The subgenus Dendromyia Theobald: a review with redescriptions of four species (Diptera: Culicidae). Mem Inst Oswaldo Cruz 95(5):649–683

    Article  CAS  Google Scholar 

  • Muturi EJ, Kim CH, Jacob B, Murphy S, Novak RJ (2010) Interspecies predation between Anopheles gambiae ss and Culex quinquefasciatus larvae. J Med Entomol 47(2):287–290

    Article  PubMed  PubMed Central  Google Scholar 

  • Navarro JC, Liria J, Pinango H, Barrera R (2007) Biogeographic area relationships in Venezuela: a Parsimony analysis of Culicidae–Phytotelmata distribution in National Parks. Zootaxa 1547(1):1–19

    Google Scholar 

  • Polis GA, Myers CA, Holt RD (1989) The ecology and evolution of intraguild predation: potential competitors that eat each other. Annu Rev Ecol Syst 20:297–330

    Article  Google Scholar 

  • R Development Core Team (2013) R: a language and environment for statistical computing. R Foundation for statistical computing, Vienna. http://www.R-project.org/

  • Reichstein B, Schröder A, Persson L, De Roos AM (2013) Habitat complexity does not promote coexistence in a size-structured intraguild predation system. J Anim Ecol 82(1):55–63

    Article  PubMed  Google Scholar 

  • Schröder A, Nilsson KA, Persson L, van Kooten T, Reichstein B (2009) Invasion success depends on invader body size in a size-structured mixed predation–competition community. J Anim Ecol 78(6):1152–1162

    Article  PubMed  Google Scholar 

  • Summers K, McKeon CS (2004) The evolutionary ecology of phytotelmata use in Neotropical poison frogs. Misc Publ Mus Zool Univ Mich 193:55–73

    Google Scholar 

  • Sunahara T, Ishizaka K, Mogi M (2002) Habitat size: a factor determining the opportunity for encounters between mosquito larvae and aquatic predators. J Vector Ecol 27(1):8–20

    PubMed  Google Scholar 

  • Talaga S, Murienne J, Dejean A, Leroy C (2015a) Online database for mosquito (Diptera, Culicidae) occurrence records in French Guiana. ZooKeys 532:107–115

    Article  Google Scholar 

  • Talaga S, Dejean A, Carinci R, Gaborit P, Dusfour I, Girod R (2015b) Updated checklist of the mosquitoes (Diptera: Culicidae) of French Guiana. J Med Entomol 52(5):770–782

    Article  PubMed  Google Scholar 

  • Wilbur HM (1980) Complex life cycles. Annu Rev Ecol Syst 11:67–93

    Article  Google Scholar 

  • Zavortink TJ (1979) Mosquito studies (Diptera, Culicidae) XXXV. The new sabethine genus Johnbelkinia and a preliminary reclassification of the composite genus Trichoprosopon. Contrib Am Entomol Inst 17(1):1–61

    Google Scholar 

Download references

Acknowledgments

We are grateful to Pascal Petronelli for identifying the phytotelm plant species, as well as to Hector Rodriguez, Marceau Minot and Clémence Mouza for field assistance. We would also like to thank Andrea Yockey-Dejean for proofreading the manuscript. Financial support was provided by the French Agence Nationale de la Recherche through an “Investissement d’Avenir” (Grant ANR-10-LABX-25-01) and the Rainwebs project (Grant ANR-12-BSV7-0022-01). ST was funded by a Ph.D. fellowship from the Université Antilles-Guyane.

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Correspondence to Stanislas Talaga.

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Talaga, S., Leroy, C., Céréghino, R. et al. Convergent evolution of intraguild predation in phytotelm-inhabiting mosquitoes. Evol Ecol 30, 1133–1147 (2016). https://doi.org/10.1007/s10682-016-9862-3

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