Section: Zoology
Topic: Population biology, Ecology

Within and among population differences in cuticular hydrocarbons in the seabird tick Ixodes uriae

Corresponding author(s): Dupraz, Marlène (marlenedupraz@gmail.com)

10.24072/pcjournal.164 - Peer Community Journal, Volume 2 (2022), article no. e51.

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The hydrophobic layer of the arthropod cuticle acts to maintain water balance, but can also serve to transmit chemical signals via cuticular hydrocarbons (CHC), essential mediators of arthropod behavior. CHC signatures typically vary qualitatively among species, but also quantitatively among populations within a species, and have been used as taxonomic tools to differentiate species or populations in a variety of taxa. Most work in this area to date has focused on insects, with little known for other arthropod groups such as ticks. The worldwide distribution and extensive host-range of the seabird tick Ixodes uriae make it a good model to study the factors influencing CHC composition. Genetically differentiated host-races of I. uriae have evolved across the distribution of this species but the factors promoting sympatric population divergence are still unknown. To test for a potential role of host-associated CHC in population isolation, we collected I. uriae specimens from two of its seabird hosts, the Atlantic puffin (Fratercula arctica) and the common guillemot (Uria aalge) in different colonies in Iceland. Using gas-chromatography and mass-spectrometry, we detected a complex cuticular mixture of 22 hydrocarbons, including n-alkanes, methyl-alkanes and alkenes ranging from 17 to 33 carbons in length. We found that each population had a distinct CHC profile. The host group explained the greatest amount of population divergence, with long-chain hydrocarbons being more abundant in puffin tick populations compared to guillemot tick populations. Future work will now be required to test whether the different CHC signals reinforce assortative mating, thereby playing a role in generating I. uriae population divergence patterns, and to evaluate diverse hypotheses on the origin of distinct population signatures.

Published online:
DOI: 10.24072/pcjournal.164
Type: Research article

Dupraz, Marlène 1; Leroy, Chloé 2; Thórarinsson, Thorkell Lindberg 3; d’Ettorre, Patrizia 2; McCoy, Karen D. 1

1 MIVEGEC, IRD, CNRS, Univ. Montpellier, Domaine La Valette - 900, rue Jean François BRETON 34090 Montpellier, France
2 Laboratoire d’Ethologie Expérimentale et Comparée UR 4443 (LEEC), Université Sorbonne Paris Nord, F-93430 Villetaneuse, France
3 Northeast Iceland Nature Research Centre, 640 Húsavík, Iceland
License: CC-BY 4.0
Copyrights: The authors retain unrestricted copyrights and publishing rights
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     title = {Within and among population differences in cuticular hydrocarbons in the seabird tick {\protect\emph{Ixodes} uriae}},
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Dupraz, Marlène; Leroy, Chloé; Thórarinsson, Thorkell Lindberg; d’Ettorre, Patrizia; McCoy, Karen D. Within and among population differences in cuticular hydrocarbons in the seabird tick Ixodes uriae. Peer Community Journal, Volume 2 (2022), article  no. e51. doi : 10.24072/pcjournal.164. https://peercommunityjournal.org/articles/10.24072/pcjournal.164/

PCI peer reviews and recommendation, and links to data, scripts, code and supplementary information: 10.24072/pci.zool.100014

Conflict of interest of the recommender and peer reviewers:
The recommender in charge of the evaluation of the article and the reviewers declared that they have no conflict of interest (as defined in the code of conduct of PCI) with the authors or with the content of the article.

[1] Andersen, S. O. Biochemistry of Insect Cuticle, Annual Review of Entomology, Volume 24 (1979) no. 1, pp. 29-59 | DOI

[2] Bagnères, A.-G.; Killian, A.; Clement, J.-L.; Lange, C. Interspecific recognition among termites of the genus Reticulitermes: Evidence for a role for the cuticular hydrocarbons, Journal of Chemical Ecology, Volume 17 (1991) no. 12, pp. 2397-2420 | DOI

[3] Bartelt, R. J.; Armold, M. T.; Schaner, A. M.; Jackson, L. L. Comparative analysis of cuticular hydrocarbons in the Drosophila virilis species group, Comparative Biochemistry and Physiology Part B: Comparative Biochemistry, Volume 83 (1986) no. 4, pp. 731-742 | DOI

[4] Bartelt, R. J.; Jackson, L. L. Hydrocarbon Component of the Drosophila virilis (Diptera: Drosophilidae) Aggregation Pheromone: (Z)-10-Heneicosene, Annals of the Entomological Society of America, Volume 77 (1984) no. 4, pp. 364-371 | DOI

[5] Bartelt, R. J.; Schaner, A. M.; Jackson, L. L. Aggregation pheromones inDrosophila borealis andDrosophila littoralis, Journal of Chemical Ecology, Volume 14 (1988) no. 4, pp. 1319-1327 | DOI

[6] Blomquist, G.; Bagnères, A.-G. Insect Hydrocarbons: Biology, Biochemistry, and Chemical Ecology, Cambridge University Press, 2010 | DOI

[7] Buckley, F. G.; Buckley, P. A. Habitat Selection and Marine Birds, Behavior of Marine Animals, Springer US, Boston, MA, 1980, pp. 69-112 | DOI

[8] Desena, M. L.; Edman, J. D.; Clark, J. M.; Symington, S. B.; Scott, T. W. Aedes aegypti (Diptera: Culicidae) Age Determination by Cuticular Hydrocarbon Analysis of Female Legs, Journal of Medical Entomology, Volume 36 (1999) no. 6, pp. 824-830 | DOI

[9] D'Ettorre, P.; Mondy, N.; Lenoir, A.; Errard, C. Blending in with the crowd: social parasites integrate into their host colonies using a flexible chemical signature, Proceedings of the Royal Society of London. Series B: Biological Sciences, Volume 269 (2002) no. 1503, pp. 1911-1918 | DOI

[10] D'ettorre, P.; Wenseleers, T.; Dawson, J.; Hutchinson, S.; Boswell, T.; Ratnieks, F. L. Wax combs mediate nestmate recognition by guard honeybees, Animal Behaviour, Volume 71 (2006) no. 4, pp. 773-779 | DOI

[11] Dietrich, M.; Beati, L.; Elguero, E.; Boulinier, T.; McCoy, K. D. Body size and shape evolution in host races of the tick Ixodes uriae, Biological Journal of the Linnean Society, Volume 108 (2013) no. 2, pp. 323-334 | DOI

[12] Dietrich, M.; Gómez-Díaz, E.; McCoy, K. D. Worldwide Distribution and Diversity of Seabird Ticks: Implications for the Ecology and Epidemiology of Tick-Borne Pathogens, Vector-Borne and Zoonotic Diseases, Volume 11 (2011) no. 5, pp. 453-470 | DOI

[13] Dietrich, M.; Lobato, E.; Boulinier, T.; McCoy, K. D. An experimental test of host specialization in a ubiquitous polar ectoparasite: a role for adaptation?, Journal of Animal Ecology, Volume 83 (2014) no. 3, pp. 576-587 | DOI

[14] Espelie, K. E.; Wenzel, J. W.; Chang, G. Surface lipids of social wasp Polistes melricus say and its nest and nest pedicel and their relation to nestmate recognition, Journal of Chemical Ecology, Volume 16 (1990) no. 7, pp. 2229-2241 | DOI

[15] Estrada-Peña, A. Climate and cuticular hydrocarbon variation in Rhipicephalus sanguineus ticks (Acari: Ixodidae), Parasitology Research, Volume 79 (1993) no. 6, pp. 512-516 | DOI

[16] Estrada-Peña, A.; CastellÁ, J.; Morel, P. C. Cuticular Hydrocarbon Composition, Phenotypic Variability, and Geographic Relationships in Allopatric Populations of Amblyomma variegatum (Acari: Ixodidae) from Africa and the Caribbean, Journal of Medical Entomology, Volume 31 (1994) no. 4, pp. 534-544 | DOI

[17] Estrada-Peña, A.; Estrada-Peña, R.; Peiró, J. M. Differentiation of Rhipicephalus Ticks (Acari: Ixodidae) by Gas Chromatography of Cuticular Hydrocarbons, The Journal of Parasitology, Volume 78 (1992) no. 6 | DOI

[18] Estrada-Peña, A.; Gray, J. S.; Kahl, O. Variability in cuticular hydrocarbons and phenotypic discrimination of Ixodes ricinus populations (Acarina: Ixodidae) from Europe, Experimental and Applied Acarology, Volume 20 (1996) no. 8, pp. 457-466 | DOI

[19] Estrada-Peña, A.; Guglielmone, A. A.; Mangold, A. J.; Castellá, J. Patterns of cuticular hydrocarbon variation and genetic similarity between natural populations of Amblyomma cajennense (Acari: Ixodidae), Acta Tropica, Volume 55 (1993) no. 1-2, pp. 61-78 | DOI

[20] Filshie, B. K. Fine Structure of the Cuticle of Insects and Other Arthropods, Insect Ultrastructure, Springer US, Boston, MA, 1982, pp. 281-312 | DOI

[21] Geiselhardt, S.; Otte, T.; Hilker, M. Looking for a similar partner: host plants shape mating preferences of herbivorous insects by altering their contact pheromones, Ecology Letters, Volume 15 (2012) no. 9, pp. 971-977 | DOI

[22] Gibbs, A.; Mousseau, T. A.; Crowe, J. H. Genetic and acclimatory variation in biophysical properties of insect cuticle lipids., Proceedings of the National Academy of Sciences, Volume 88 (1991) no. 16, pp. 7257-7260 | DOI

[23] Harris, M.; Wanless, S. The Puffin, Bloomsbury Publishing, 2011

[24] Hervé, M. Aide-mémoire de statistique appliquée à la biologie - Construire son étude et analyser les résultats à l'aide du logiciel R. Version 5, 2014

[25] Holze, H.; Schrader, L.; Buellesbach, J. Advances in deciphering the genetic basis of insect cuticular hydrocarbon biosynthesis and variation, Heredity, Volume 126 (2020) no. 2, pp. 219-234 | DOI

[26] Howard, R. W.; Blomquist, G. J. Ecological, behavioral, and biochemical aspects of insect hydrocarbons, Annual Review of Entomology, Volume 50 (2005) no. 1, pp. 371-393 | DOI

[27] Howard, R. W.; McDaniel, C. A.; Blomquist, G. J. Cuticular hydrocarbons of the eastern subterranean termite, Reticulitermes flavipes (Kollar) (Isoptera: Rhinotermitidae), Journal of Chemical Ecology, Volume 4 (1978) no. 2, pp. 233-245 | DOI

[28] Hunt, L. M. Differentiation between three species of Amblyomma ticks (Acari: Ixodidae) by analysis of cuticular hydrocarbons, Annals of Tropical Medicine & Parasitology, Volume 80 (1986) no. 2, pp. 245-249 | DOI

[29] Ichinose, K.; Lenoir, A. Ontogeny of hydrocarbon profiles in the ant Aphaenogaster senilis and effects of social isolation, Comptes Rendus Biologies, Volume 332 (2009) no. 8, pp. 697-703 | DOI

[30] Jallon, J.-M.; David, J. R. Variation in Cuticular Hydrocarbons Among the Eight Species of the Drosophila melanogaster Subgroup, Evolution, Volume 41 (1987) no. 2, pp. 294-302 | DOI

[31] Kruger, E. L.; Pappas, C. D.; Howard, R. W. Cuticular Hydrocarbon Geographic Variation Among Seven North American Populations of Aedes albopictus (Diptera: Culicidae), Journal of Medical Entomology, Volume 28 (1991) no. 6, pp. 859-864 | DOI

[32] Kuo, T.-H.; Yew, J. Y.; Fedina, T. Y.; Dreisewerd, K.; Dierick, H. A.; Pletcher, S. D. Aging modulates cuticular hydrocarbons and sexual attractiveness in Drosophila melanogaster, Journal of Experimental Biology, Volume 215 (2012) no. 5, pp. 814-821 | DOI

[33] Le Conte, Y.; Huang, Z. Y.; Roux, M.; Zeng, Z. J.; Christidès, J.-P.; Bagnères, A.-G. Varroa destructor changes its cuticular hydrocarbons to mimic new hosts, Biology Letters, Volume 11 (2015) no. 6 | DOI

[34] Lecuona, R.; Riba, G.; Cassier, P.; Clement, J. Alterations of insect epicuticular hydrocarbons during infection with Beauveria bassiana or B. brongniartii, Journal of Invertebrate Pathology, Volume 58 (1991) no. 1, pp. 10-18 | DOI

[35] Léger, E.; Vourc’h, G.; Vial, L.; Chevillon, C.; McCoy, K. D. Changing distributions of ticks: causes and consequences, Experimental and Applied Acarology, Volume 59 (2013) no. 1-2, pp. 219-244 | DOI

[36] Leonovich, S. Phenol and lactone receptors in the distal sensilla of the Haller's organ in Ixodes ricinus ticks and their possible role in host perception, Experimental and Applied Acarology, Volume 32 (2004) no. 1/2, pp. 89-102 | DOI

[37] Liang, D.; Silverman, J. “You are what you eat”: Diet modifies cuticular hydrocarbons and nestmate recognition in the Argentine ant, Linepithema humile, Naturwissenschaften, Volume 87 (2000) no. 9, pp. 412-416 | DOI

[38] Lockey, K. H. Lipids of the insect cuticle: origin, composition and function, Comparative Biochemistry and Physiology Part B: Comparative Biochemistry, Volume 89 (1988) no. 4, pp. 595-645 | DOI

[39] McCoy, K. B. N.; (Eds.) Tiques et maladies à tiques, IRD Éditions, Marseille, 2015 | DOI

[40] Mccoy, K. D.; Boulinier, T.; Tirard, C.; Michalakis, Y. Host specificity of a generalist parasite: genetic evidence of sympatric host races in the seabird tick Ixodes uriae, Journal of Evolutionary Biology, Volume 14 (2001) no. 3, pp. 395-405 | DOI

[41] McCoy, K. D.; Chapuis, E.; Tirard, C.; Boulinier, T.; Michalakis, Y.; Bohec, C. L.; Maho, Y. L.; Gauthier-Clerc, M. Recurrent evolution of host-specialized races in a globally distributed parasite, Proceedings of the Royal Society B: Biological Sciences, Volume 272 (2005) no. 1579, pp. 2389-2395 | DOI

[42] McCoy, K. D.; Léger, E.; Dietrich, M. Host specialization in ticks and transmission of tick-borne diseases: a review, Frontiers in Cellular and Infection Microbiology, Volume 3 (2013) | DOI

[43] McCoy, K. D.; Tirard, C. Reproductive Strategies of the Seabird Tick Ixodes uriae (Acari: Ixodidae), Journal of Parasitology, Volume 88 (2002) no. 4, pp. 813-816 | DOI

[44] McCoy, K. D.; Tirard, C.; Michalakis, Y. Spatial genetic structure of the ectoparasite Ixodes uriae within breeding cliffs of its colonial seabird host, Heredity, Volume 91 (2003) no. 4, pp. 422-429 | DOI

[45] Nazzi, F.; Le Conte, Y. Ecology of Varroa destructor, the Major Ectoparasite of the Western Honey Bee, Apis mellifera, Annual Review of Entomology, Volume 61 (2016) no. 1, pp. 417-432 | DOI

[46] Paulmier, I.; Bagnères, A.-G.; Afonso, C. M. M.; Dusticier, G.; Rivière, G.; Clément, J.-L. Alkenes as a sexual pheromone in the alfalfa leaf-cutter bee Megachile rotundata, Journal of Chemical Ecology, Volume 25 (1999) no. 3, pp. 471-490 | DOI

[47] Peschke, K.; Metzler, M. Cuticular hydrocarbons and female sex pheromones of the rove beetle, Aleochara curtula (Goeze) (Coleoptera:Staphylinidae), Insect Biochemistry, Volume 17 (1987) no. 1, pp. 167-178 | DOI

[48] Randolph, S. Ticks are not Insects: Consequences of Contrasting Vector Biology for Transmission Potential, Parasitology Today, Volume 14 (1998) no. 5, pp. 186-192 | DOI

[49] Randolph, S. E.; Storey, K. Impact of Microclimate on Immature Tick-Rodent Host Interactions (Acari: Ixodidae): Implications for Parasite Transmission, Journal of Medical Entomology, Volume 36 (1999) no. 6, pp. 741-748 | DOI

[50] Rottler, A.-M.; Schulz, S.; Ayasse, M. Wax Lipids Signal Nest Identity in Bumblebee Colonies, Journal of Chemical Ecology, Volume 39 (2013) no. 1, pp. 67-75 | DOI

[51] Schlamp, K. K. Contact pheromone components and diel periodicity of sexual communication in peach twig borers, Anarsia lineatella (Lepidoptera: Gelechiidae) (PhD Thesis), Biological Sciences Department-Simon Fraser University (2005)

[52] Schöni, R.; Hess, E.; Blum, W.; Ramstein, K. The aggregation-attachment pheromone of the tropical bont tick Amblyomma variegatum Fabricius (Acari, Ixodidae): Isolation, identification and action of its components, Journal of Insect Physiology, Volume 30 (1984) no. 8, pp. 613-618 | DOI

[53] Shimshoni, J. A.; Erster, O.; Rot, A.; Cuneah, O.; Soback, S.; Shkap, V. Cuticular fatty acid profile analysis of three Rhipicephalus tick species (Acari: Ixodidae), Experimental and Applied Acarology, Volume 61 (2013) no. 4, pp. 481-489 | DOI

[54] Simmons, L. W.; Thomas, M. L.; Gray, B.; Zuk, M. Replicated evolutionary divergence in the cuticular hydrocarbon profile of male crickets associated with the loss of song in the Hawaiian archipelago, Journal of Evolutionary Biology, Volume 27 (2014) no. 10, pp. 2249-2257 | DOI

[55] Singer, T. L.; Espelie, K. E. Nest surface hydrocarbons facilitate nestmate recognition for the social wasp,Polistes metricus Say (Hymenoptera: Vespidae), Journal of Insect Behavior, Volume 9 (1996) no. 6, pp. 857-870 | DOI

[56] Sonenshine, D. E. Pheromones and other semiochemicals of ticks and their use in tick control, Parasitology, Volume 129 (2004) no. S1 | DOI

[57] Sonenshine, D.; Roe, R.; (Eds.) Biology of ticks, 2nd ed., Oxford University Press, 2014

[58] Sonenshine, D. E.; Silverstein, R. M.; Brossut, R.; Davis, E. E.; Taylor, D.; Carson, K. A.; Homsher, P. J.; Wang, V. B. Genital sex pheromones of ixodid ticks: 1. Evidence of occurrence in anterior reproductive tract of American dog tick, Dermacentor variabilis (Say) (Acari: Ixodidae), Journal of Chemical Ecology, Volume 11 (1985) no. 12, pp. 1669-1694 | DOI

[59] Tkachev, A. V.; Dobrotvorsky, A. K.; Vjalkov, A. I.; Morozov, S. V. Chemical composition of lipophylic compounds from the body surface of unfed adult Ixodes persulcatus ticks (Acari: Ixodidae), Experimental and Applied Acarology, Volume 24 (2000) no. 2, pp. 145-158 | DOI

[60] Uebel, E. C.; Schwarz, M.; Sonnet, P. E.; Miller, R. W.; Menzer, R. E. Evaluation of the Mating Stimulant Pheromones of Fannia canicularis, F. pusio, and F. femoralis as Attractants, The Florida Entomologist, Volume 61 (1978) no. 3, pp. 139-143 | DOI

[61] Uebel, E. C.; Sonnet, P. E.; Bierl, B. A.; Miller, R. W. Sex pheromone of the stable flyl: Isolation and preliminary identification of compounds that induce mating strike behavior, Journal of Chemical Ecology, Volume 1 (1975) no. 3, pp. 377-385 | DOI

[62] van Zweden, J. S.; d'Ettorre, P. Insect Hydrocarbons In: In Insect Hydrocarbons: Biology, Biochemistry, and chemical Ecology , Cambridge University Press (2010), pp. 222-243 | DOI

[63] Wyatt, T. D. Pheromones and signature mixtures: defining species-wide signals and variable cues for identity in both invertebrates and vertebrates, Journal of Comparative Physiology A, Volume 196 (2010) no. 10, pp. 685-700 | DOI

[64] Yoder, J. A.; Domingus, J. L. Identification of hydrocarbons that protect ticks (Acari: Ixodidae) against fire ants (Hymenoptera: Formicidae), but not lizards (Squamata: Polychrotidae), in an allomonal defense secretion, International Journal of Acarology, Volume 29 (2003) no. 1, pp. 87-91 | DOI

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