Changes in parasite species distributions could be driven by host range expansions: the case of hybridisation between two Australian reptile ticks
Bridgette Barnden A , Amy L. Slender![https://orcid.org/0000-0002-2851-253X](/media/client/orcid_16x16.png)
![https://orcid.org/0000-0002-8629-354X](/media/client/orcid_16x16.png)
A College of Science and Engineering, Flinders University, GPO Box 2100, Adelaide, SA 5001, Australia.
B Evolutionary Biology Unit, South Australian Museum, North Terrace, Adelaide, SA 5000, Australia.
Australian Journal of Zoology 70(5) 153-163 https://doi.org/10.1071/ZO23010
Submitted: 15 March 2023 Accepted: 24 April 2023 Published: 24 May 2023
© 2022 The Author(s) (or their employer(s)). Published by CSIRO Publishing. This is an open access article distributed under the Creative Commons Attribution-NonCommercial-NoDerivatives 4.0 International License (CC BY-NC-ND)
Abstract
Anthropogenic stressors such as climate change and diminishing habitats cause widespread disturbances in species distributions for a variety of taxa. Range shifts and hybridisation following secondary contact become of particular importance when it comes to parasites such as ticks, as they are dependent on their host distributions and can carry numerous harmful pathogens. We aimed to determine if two parapatric reptile tick species, Amblyomma albolimbatum and A. limbatum, hybridise at their parapatric boundary by comparing morphological and genomic variation using single nucleotide polymorphisms. Our results show that both tick species were genomically distinct, but hybridisation has occurred. We found a hybrid and an A. limbatum outside of their previously known range, suggesting there could have been a shift in tick distribution. What were thought to be hybrids due to intermediate morphological traits were not hybrids but morphological variants of the parental species. This information suggests more distinctive morphological features are needed for identifying these tick species and that novel environmental conditions and a broadening of tick niche due to hybridisation could increase host exposure to different pathogens.
Keywords: climate change, Egerniinae (Tiliquini), genomics, hybridisation, parapatry, SNPs, Squamata, ticks.
References
Abbott, RJ, Barton, NH, and Good, JM (2016). Genomics of hybridization and its evolutionary consequences. Molecular Ecology 25, 2325–2332.| Genomics of hybridization and its evolutionary consequences.Crossref | GoogleScholarGoogle Scholar |
Alkishe, A, Raghavan, RK, and Peterson, AT (2021). Likely geographic distributional shifts among medically important tick species and tick-associated diseases under climate change in North America: a review. Insects 12, 225.
| Likely geographic distributional shifts among medically important tick species and tick-associated diseases under climate change in North America: a review.Crossref | GoogleScholarGoogle Scholar |
Anderson, EC, and Thompson, EA (2002). A model-based method for identifying species hybrids using multilocus genetic data. Genetics 160, 1217–1229.
| A model-based method for identifying species hybrids using multilocus genetic data.Crossref | GoogleScholarGoogle Scholar |
Andrews, RH, Petney, TN, and Bull, CM (1982). Reproductive interference between three parapatric species of reptile tick. Oecologia 52, 281–286.
| Reproductive interference between three parapatric species of reptile tick.Crossref | GoogleScholarGoogle Scholar |
Barton, NH, and Hewitt, GM (1985). Analysis of hybrid zones. Annual Review of Ecology and Systematics 16, 113–148.
| Analysis of hybrid zones.Crossref | GoogleScholarGoogle Scholar |
Beever, EA, O’Leary, J, Mengelt, C, West, JM, Julius, S, Green, N, Magness, D, Petes, L, Stein, B, Nicotra, AB, Hellmann, JJ, Robertson, AL, Staudinger, MD, Rosenberg, AA, Babij, E, Brennan, J, Schuurman, GW, and Hofmann, GE (2016). Improving conservation outcomes with a new paradigm for understanding species’ fundamental and realized adaptive capacity. Conservation Letters 9, 131–137.
| Improving conservation outcomes with a new paradigm for understanding species’ fundamental and realized adaptive capacity.Crossref | GoogleScholarGoogle Scholar |
Bournez, L, Cangi, N, Lancelot, R, Pleydell, DRJ, Stachurski, F, Bouyer, J, Martinez, D, Lefrancois, T, Neves, L, and Pradel, J (2015). Parapatric distribution and sexual competition between two tick species, Amblyomma variegatum and A. hebraeum (Acari, Ixodidae), in Mozambique. Parasites & Vectors 8, 504.
| Parapatric distribution and sexual competition between two tick species, Amblyomma variegatum and A. hebraeum (Acari, Ixodidae), in Mozambique.Crossref | GoogleScholarGoogle Scholar |
Brauer, CJ, Sandoval-Castillo, J, Gates, K, Hammer, MP, Unmack, PJ, Bernatchez, L, and Beheregaray, LB (2023). Natural hybridization reduces vulnerability to climate change. Nature Climate Change 13, 282–289.
| Natural hybridization reduces vulnerability to climate change.Crossref | GoogleScholarGoogle Scholar |
Bull, CM (1991). Ecology of parapatric distributions. Annual Review of Ecology and Systematics 22, 19–36.
| Ecology of parapatric distributions.Crossref | GoogleScholarGoogle Scholar |
Bull, CM, and Burzacott, D (2001). Temporal and spatial dynamics of a parapatric boundary between two Australian reptile ticks. Molecular Ecology 10, 639–648.
| Temporal and spatial dynamics of a parapatric boundary between two Australian reptile ticks.Crossref | GoogleScholarGoogle Scholar |
Bull, CM, and Freake, MJ (1999). Home-range fidelity in the Australian sleepy lizard, Tiliqua rugosa. Australian Journal of Zoology 47, 125–132.
| Home-range fidelity in the Australian sleepy lizard, Tiliqua rugosa.Crossref | GoogleScholarGoogle Scholar |
Carlson, CJ, Burgio, KR, Dougherty, ER, Phillips, AJ, Bueno, VM, Clements, CF, Castaldo, G, Dallas, TA, Cizauskas, CA, Cumming, GS, Doña, J, Harris, NC, Jovani, R, Mironov, S, Muellerklein, OC, Proctor, HC, and Getz, WM (2017). Parasite biodiversity faces extinction and redistribution in a changing climate. Science Advances 3, e1602422.
| Parasite biodiversity faces extinction and redistribution in a changing climate.Crossref | GoogleScholarGoogle Scholar |
Currat, M, Ruedi, M, Petit, RJ, and Excoffier, L (2008). The hidden side of invasions: massive introgression by local genes. Evolution 62, 1908–1920.
| The hidden side of invasions: massive introgression by local genes.Crossref | GoogleScholarGoogle Scholar |
Dantas-Torres, F (2018). Species concepts: what about ticks? Trends in Parasitology 34, 1017–1026.
| Species concepts: what about ticks?Crossref | GoogleScholarGoogle Scholar |
Dehhaghi, M, Kazemi Shariat Panahi, H, Holmes, EC, Hudson, BJ, Schloeffel, R, and Guillemin, GJ (2019). Human tick-borne diseases in Australia. Frontiers in Cellular and Infection Microbiology 9, 3.
| Human tick-borne diseases in Australia.Crossref | GoogleScholarGoogle Scholar |
Earl, DA, and vonHoldt, BM (2012). STRUCTURE HARVESTER: a website and program for visualizing STRUCTURE output and implementing the Evanno method. Conservation Genetics Resources 4, 359–361.
| STRUCTURE HARVESTER: a website and program for visualizing STRUCTURE output and implementing the Evanno method.Crossref | GoogleScholarGoogle Scholar |
Engler, JO, Rödder, D, Elle, O, Hochkirch, A, and Secondi, J (2013). Species distribution models contribute to determine the effect of climate and interspecific interactions in moving hybrid zones. Journal of Evolutionary Biology 26, 2487–2496.
| Species distribution models contribute to determine the effect of climate and interspecific interactions in moving hybrid zones.Crossref | GoogleScholarGoogle Scholar |
Estrada-Peña, A, Ayllón, N, and De La Fuente, J (2012). Impact of climate trends on tick-borne pathogen transmission. Frontiers in Physiology 3, 64.
Godfrey, SS, and Gardner, MG (2017). Lizards, ticks and contributions to Australian parasitology: C. Michael Bull (1947–2016). International Journal for Parasitology: Parasites and Wildlife 6, 295–298.
Gruber, B, Unmack, PJ, Berry, OF, and Georges, A (2018). dartr: an r package to facilitate analysis of SNP data generated from reduced representation genome sequencing. Molecular Ecology Resources 18, 691–699.
| dartr: an r package to facilitate analysis of SNP data generated from reduced representation genome sequencing.Crossref | GoogleScholarGoogle Scholar |
Harper, FM, and Hart, MW (2007). Morphological and phylogenetic evidence for hybridization and introgression in a sea star secondary contact zone. Invertebrate Biology 126, 373–384.
| Morphological and phylogenetic evidence for hybridization and introgression in a sea star secondary contact zone.Crossref | GoogleScholarGoogle Scholar |
Harr, B, and Price, T (2014). Climate change: a hybrid zone moves north. Current Biology 24, R230–R232.
| Climate change: a hybrid zone moves north.Crossref | GoogleScholarGoogle Scholar |
Harvell, CD, Mitchell, CE, Ward, JR, Altizer, S, Dobson, AP, Ostfeld, RS, and Samuel, MD (2002). Climate warming and disease risks for terrestrial and marine biota. Science 296, 2158–2162.
| Climate warming and disease risks for terrestrial and marine biota.Crossref | GoogleScholarGoogle Scholar |
Hasselman, DJ, Argo, EE, McBride, MC, Bentzen, P, Schultz, TF, Perez-Umphrey, AA, and Palkovacs, EP (2014). Human disturbance causes the formation of a hybrid swarm between two naturally sympatric fish species. Molecular Ecology 23, 1137–1152.
| Human disturbance causes the formation of a hybrid swarm between two naturally sympatric fish species.Crossref | GoogleScholarGoogle Scholar |
Hermes, C, Keller, K, Nicholas, RE, Segelbacher, G, and Schaefer, HM (2018). Projected impacts of climate change on habitat availability for an endangered parakeet. PLoS ONE 13, e0191773.
| Projected impacts of climate change on habitat availability for an endangered parakeet.Crossref | GoogleScholarGoogle Scholar |
Hunter, EA, Matocq, MD, Murphy, PJ, and Shoemaker, KT (2017). Differential effects of climate on survival rates drive hybrid zone movement. Current Biology 27, 3898–3903.e4.
| Differential effects of climate on survival rates drive hybrid zone movement.Crossref | GoogleScholarGoogle Scholar |
Jakobsson, M, and Rosenberg, NA (2007). CLUMPP: a cluster matching and permutation program for dealing with label switching and multimodality in analysis of population structure. Bioinformatics 23, 1801–1806.
| CLUMPP: a cluster matching and permutation program for dealing with label switching and multimodality in analysis of population structure.Crossref | GoogleScholarGoogle Scholar |
Jombart, T (2008). adegenet: a R package for the multivariate analysis of genetic markers. Bioinformatics 24, 1403–1405.
| adegenet: a R package for the multivariate analysis of genetic markers.Crossref | GoogleScholarGoogle Scholar |
Jombart, T, and Ahmed, I (2011). adegenet 1.3-1: new tools for the analysis of genome-wide SNP data. Bioinformatics 27, 3070–3071.
| adegenet 1.3-1: new tools for the analysis of genome-wide SNP data.Crossref | GoogleScholarGoogle Scholar |
Jones, W, Kulma, K, Bensch, S, Cichoń, M, Kerimov, A, Krist, M, Laaksonen, T, Moreno, J, Munclinger, P, Slater, FM, Szöllősi, E, Visser, ME, and Qvarnström, A (2018). Interspecific transfer of parasites following a range-shift in Ficedula flycatchers. Ecology and Evolution 8, 12183–12192.
| Interspecific transfer of parasites following a range-shift in Ficedula flycatchers.Crossref | GoogleScholarGoogle Scholar |
Kilian A, Wenzl P, Huttner E, Carling J, Xia L, Blois H, Caig V, Heller-Uszynska K, Jaccoud D, Hopper C, Aschenbrenner-Kilian M, Evers M, Peng K, Cayla C, Hok P, Uszynski G (2012) Diversity arrays technology: a generic genome profiling technology on open platforms. In ‘Data production and analysis in population genomics’. (Eds F Pompanon, A Bonin) pp. 67–89. (Humana Press)
King, KC, Stelkens, RB, Webster, JP, Smith, DF, and Brockhurst, MA (2015). Hybridization in parasites: consequences for adaptive evolution, pathogenesis, and public health in a changing world. PLoS Pathogens 11, e1005098.
| Hybridization in parasites: consequences for adaptive evolution, pathogenesis, and public health in a changing world.Crossref | GoogleScholarGoogle Scholar |
Kovalev, SY, Golovljova, IV, and Mukhacheva, TA (2016). Natural hybridization between Ixodes ricinus and Ixodes persulcatus ticks evidenced by molecular genetics methods. Ticks and Tick-borne Diseases 7, 113–118.
| Natural hybridization between Ixodes ricinus and Ixodes persulcatus ticks evidenced by molecular genetics methods.Crossref | GoogleScholarGoogle Scholar |
Léger, E, Vourc’h, G, Vial, L, Chevillon, C, and McCoy, KD (2013). Changing distributions of ticks: causes and consequences. Experimental and Applied Acarology 59, 219–244.
| Changing distributions of ticks: causes and consequences.Crossref | GoogleScholarGoogle Scholar |
Lopes, PC, Kanno, RH, Sourassou, NF, and Moraes, GJ (2018). Effect of temperature and diet on the morphology of Euseius concordis (Acari: Phytoseiidae). Systematic and Applied Acarology 23, 1322–1332.
| Effect of temperature and diet on the morphology of Euseius concordis (Acari: Phytoseiidae).Crossref | GoogleScholarGoogle Scholar |
Lynen, G, Zeman, P, Bakuname, C, Di Giulio, G, Mtui, P, Sanka, P, and Jongejan, F (2008). Shifts in the distributional ranges of Boophilus ticks in Tanzania: evidence that a parapatric boundary between Boophilus microplus and B. decoloratus follows climate gradients. Experimental and Applied Acarology 44, 147–164.
| Shifts in the distributional ranges of Boophilus ticks in Tanzania: evidence that a parapatric boundary between Boophilus microplus and B. decoloratus follows climate gradients.Crossref | GoogleScholarGoogle Scholar |
Mayr E (1963) ‘Animals, species and evolution.’ (Harvard University Press: Cambridge, Massachusetts)
Mayr E (1970) ‘Populations, species, and evolution: an abridgment of animal species and evolution.’ (Belknap Press of Harvard University Press)
McQuillan, MA, and Rice, AM (2015). Differential effects of climate and species interactions on range limits at a hybrid zone: potential direct and indirect impacts of climate change. Ecology and Evolution 5, 5120–5137.
| Differential effects of climate and species interactions on range limits at a hybrid zone: potential direct and indirect impacts of climate change.Crossref | GoogleScholarGoogle Scholar |
Ogston, G, Beatty, SJ, Morgan, DL, Pusey, BJ, and Lymbery, AJ (2016). Living on burrowed time: aestivating fishes in south-western Australia face extinction due to climate change. Biological Conservation 195, 235–244.
| Living on burrowed time: aestivating fishes in south-western Australia face extinction due to climate change.Crossref | GoogleScholarGoogle Scholar |
Oliveira, SVd, Romero-Alvarez, D, Martins, TF, Santos, JPd, Labruna, MB, Gazeta, GS, Escobar, LE, and Gurgel-Gonçalves, R (2017). Amblyomma ticks and future climate: range contraction due to climate warming. Acta Tropica 176, 340–348.
| Amblyomma ticks and future climate: range contraction due to climate warming.Crossref | GoogleScholarGoogle Scholar |
Oliver, JH, Wilkinson, PR, and Kohls, GM (1972). Observations on hybridization of three species of North American dermacentor ticks. The Journal of Parasitology 58, 380–384.
| Observations on hybridization of three species of North American dermacentor ticks.Crossref | GoogleScholarGoogle Scholar |
Ostfeld, RS, and Brunner, JL (2015). Climate change and Ixodes tick-borne diseases of humans. Philosophical Transactions of the Royal Society B: Biological Sciences 370, 20140051.
| Climate change and Ixodes tick-borne diseases of humans.Crossref | GoogleScholarGoogle Scholar |
Peterson, BK, Weber, JN, Kay, EH, Fisher, HS, and Hoekstra, HE (2012). Double digest RADseq: an inexpensive method for de novo SNP discovery and genotyping in model and non-model species. PLoS ONE 7, e37135.
| Double digest RADseq: an inexpensive method for de novo SNP discovery and genotyping in model and non-model species.Crossref | GoogleScholarGoogle Scholar |
Pfäffle, M, Černá Bolfíková, B, Hulva, P, and Petney, T (2014). Different parasite faunas in sympatric populations of sister hedgehog species in a secondary contact zone. PLoS ONE 9, e114030.
| Different parasite faunas in sympatric populations of sister hedgehog species in a secondary contact zone.Crossref | GoogleScholarGoogle Scholar |
Pritchard, JK, Stephens, M, and Donnelly, P (2000). Inference of population structure using multilocus genotype data. Genetics 155, 945–959.
| Inference of population structure using multilocus genotype data.Crossref | GoogleScholarGoogle Scholar |
Roberts FHS (1970) Australian ticks. CSIRO Publishing, Melbourne.
Rosenberg, NA (2004). DISTRUCT: a program for the graphical display of population structure. Molecular Ecology Notes 4, 137–138.
| DISTRUCT: a program for the graphical display of population structure.Crossref | GoogleScholarGoogle Scholar |
Sansaloni, C, Petroli, C, Jaccoud, D, Carling, J, Detering, F, Grattapaglia, D, and Kilian, A (2011). Diversity Arrays Technology (DArT) and next-generation sequencing combined: genome-wide, high throughput, highly informative genotyping for molecular breeding of Eucalyptus. BMC Proceedings 5, P54.
| Diversity Arrays Technology (DArT) and next-generation sequencing combined: genome-wide, high throughput, highly informative genotyping for molecular breeding of Eucalyptus.Crossref | GoogleScholarGoogle Scholar |
Sharrad RD (1979) Studies of factors which determine the distributions of three species of South Australian reptile ticks. PhD thesis, University of Adelaide, Adelaide.
Siebentritt M, Halsey N, Stafford-Smith M (2014) Regional climate change adaptation plan for the Eyre Peninsula. Prepared for the Eyre Peninsula Integrated Climate Change Agreement Committee. Seed Consulting Services.
Smyth, M (1973). The distribution of three species of reptile ticks, Aponomma hydrosauri (Denny), Amblyomma albolimbatum Neumann, and Amb. limbatum Neumann I. Distribution and hosts. Australian Journal of Zoology 21, 91–101.
| The distribution of three species of reptile ticks, Aponomma hydrosauri (Denny), Amblyomma albolimbatum Neumann, and Amb. limbatum Neumann I. Distribution and hosts.Crossref | GoogleScholarGoogle Scholar |
Sonenshine, DE (2018). Range expansion of tick disease vectors in North America: implications for spread of tick-borne disease. International Journal of Environmental Research and Public Health 15, 478.
| Range expansion of tick disease vectors in North America: implications for spread of tick-borne disease.Crossref | GoogleScholarGoogle Scholar |
Sungirai, M, Madder, M, Moyo, DZ, De Clercq, P, and Abatih, EN (2015). An update on the ecological distribution of the Ixodidae ticks in Zimbabwe. Experimental and Applied Acarology 66, 269–280.
| An update on the ecological distribution of the Ixodidae ticks in Zimbabwe.Crossref | GoogleScholarGoogle Scholar |
Sungirai, M, Abatih, EN, Moyo, DZ, Clercq, PD, and Madder, M (2017). Shifts in the distribution of ixodid ticks parasitizing cattle in Zimbabwe. Medical and Veterinary Entomology 31, 78–87.
| Shifts in the distribution of ixodid ticks parasitizing cattle in Zimbabwe.Crossref | GoogleScholarGoogle Scholar |
Sutherst, RW (1987). The dynamics of hybrid zones between tick (Acari) species. International Journal for Parasitology 17, 921–926.
| The dynamics of hybrid zones between tick (Acari) species.Crossref | GoogleScholarGoogle Scholar |
Taylor, SA, Larson, EL, and Harrison, RG (2015). Hybrid zones: windows on climate change. Trends in Ecology & Evolution 30, 398–406.
| Hybrid zones: windows on climate change.Crossref | GoogleScholarGoogle Scholar |
Theodosopoulos, AN, Hund, AK, and Taylor, SA (2019). Parasites and host species barriers in animal hybrid zones. Trends in Ecology & Evolution 34, 19–30.
| Parasites and host species barriers in animal hybrid zones.Crossref | GoogleScholarGoogle Scholar |
Wielstra, B, Burke, T, Butlin, RK, Avcı, A, Üzüm, N, Bozkurt, E, Olgun, K, and Arntzen, JW (2017). A genomic footprint of hybrid zone movement in crested newts. Evolution Letters 1, 93–101.
| A genomic footprint of hybrid zone movement in crested newts.Crossref | GoogleScholarGoogle Scholar |
Wringe, BF, Stanley, RRE, Jeffery, NW, Anderson, EC, and Bradbury, IR (2017). parallelnewhybrid: an R package for the parallelization of hybrid detection using newhybrids. Molecular Ecology Resources 17, 91–95.
| parallelnewhybrid: an R package for the parallelization of hybrid detection using newhybrids.Crossref | GoogleScholarGoogle Scholar |
Zivkovic, D, Pegram, RG, Jongejan, F, and Mwase, ET (1986). Biology of Rhipicephalus appendiculatus and R. zambeziensis and production of a fertile hybrid under laboratory conditions. Experimental & Applied Acarology 2, 285–298.
| Biology of Rhipicephalus appendiculatus and R. zambeziensis and production of a fertile hybrid under laboratory conditions.Crossref | GoogleScholarGoogle Scholar |