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The comparative phylogeography of shore crabs and their acanthocephalan parasites

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Abstract

Comparing the genetic structure of host populations with that of their parasites can shed light on the efficiency and independence of their respective dispersal mechanisms. The degree of congruence between host and parasite genetic structure should reflect to what extent they share dispersal mechanisms. Here, we contrast the genetic structure of the acanthocephalan parasite Profilicollis novaezelandensis with that of its intermediate host, the hairy-handed shore crab Hemigrapsus crenulatus, along the east coast of New Zealand’s South Island. We expected no congruence in their phylogeographic patterns because of the very different modes of dispersal used by the crabs (planktonic drift) and the acanthocephalans (bird-mediated dispersal). Based on analysis of cytochrome oxidase subunit I gene sequences, we found no significant genetic structure among isolated populations of the crab and those of their parasite, along a roughly 600 km stretch of coastline. Surprisingly, based on a distance-based co-evolutionary analysis statistical tool (PACo), we observed an overall significant level of congruence between host and parasite population-level phylogenies. The most parsimonious interpretation is that statistical significance does not translate into biological significance, with the result likely due to chance, possibly because bird movements that disperse parasites coincidentally match patterns of crab dispersal by ocean currents in parts of our study area. In this system, the connectivity among different localities and the apparent genetic mixing among populations may have implications for host–parasite co-evolution.

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References

  • Balbuena JA, Miguez-Lozano R, Blasco-Costa I (2013) PACo: a novel procrustes application to cophylogenetic analysis. PLoS One 8:e61048

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Blasco-Costa I, Poulin R (2013) Host traits explain the genetic structure of parasites: a meta-analysis. Parasitology 140:1316–1322

    Article  PubMed  Google Scholar 

  • Brockerhoff AM, Smales LR (2002) Profilicollis novaezelandensis n. sp (Polymorphidae) and two other acanthocephalan parasites from shore birds (Haematopodidae and Scolopacidae) in New Zealand, with records of two species in intertidal crabs (Decapoda: Grapsidae and Ocypodidae). Syst Parasitol 52:55–65

    Article  CAS  PubMed  Google Scholar 

  • Bryan-Walker K, Leung TLF, Poulin R (2007) Local adaptation of immunity against a trematode parasite in marine amphipod populations. Mar Biol 152:687–695

    Article  Google Scholar 

  • Clement M, Posada D, Crandall KA (2000) TCS: a computer program to estimate gene genealogies. Mol Ecol 9:1657–1659

    Article  CAS  PubMed  Google Scholar 

  • Cornet S, Biard C, Moret Y (2009) Variation in immune defence among populations of Gammarus pulex (Crustacea: Amphipoda). Oecologia 159:257–269

    Article  PubMed  Google Scholar 

  • Criscione CD, Blouin MS (2004) Life cycles shape parasite evolution: comparative population genetics of salmon trematodes. Evolution 58:198–202

    Article  PubMed  Google Scholar 

  • de Vienne DM, Aguileta G, Ollier S (2011) Euclidean nature of phylogenetic distance matrices. Syst Biol 60:826–832

    Article  PubMed  Google Scholar 

  • Devlin CM, Diamond AW, Saunders GW (2004) Sexing arctic terns in the field and laboratory. Waterbirds 27:314–320

    Article  Google Scholar 

  • Drummond AJ, Rambaut A (2007) BEAST: Bayesian evolutionary analysis by sampling trees. BMC Evol Biol 7:214

    Article  PubMed  PubMed Central  Google Scholar 

  • Dybdahl M, Lively CM (1996) The geography of coevolution: comparative population structures for a snail and its trematode parasite. Evolution 50:2264–2275

    Article  PubMed  Google Scholar 

  • Excoffier L, Lischer HEL (2010) Arlequin suite ver 3.5: a new series of programs to perform population genetics analyses under Linux and Windows. Mol Ecol Resour 10:564–567

    Article  PubMed  Google Scholar 

  • Fordham R (1968) Dispersion and dispersal of the Dominican gull in Wellington, New Zealand. Proc N Z Ecol Soc 15:40–50

    Google Scholar 

  • Garcia-Varela M, Pérez-Ponce de Léon G, Aznar FJ, Nadler SA (2013) Phylogenetic relationship among genera of Polymorphidae (Acanthocephala), inferred from nuclear and mitochondrial gene sequences. Mol Phylogenet Evol 68:176–184

    Article  PubMed  Google Scholar 

  • Geller J, Meyer C, Parker M, Hawk H (2013) Redesign of PCR primers for mitochondrial cytochrome c oxidase subunit I for marine invertebrates and application in all-taxa biotic surveys. Mol Ecol Resour 13:851–861

    Article  CAS  PubMed  Google Scholar 

  • Gilg MR, Hilbish TJ (2003) The geography of marine larval dispersal: coupling genetics with fine-scale physical oceanography. Ecology 84:2989–2998

    Article  Google Scholar 

  • Goulding TC, Cohen CS (2014) Phylogeography of a marine acanthocephalan: lack of cryptic diversity in a cosmopolitan parasite of mole crabs. J Biogeogr 41:965–976

    Article  Google Scholar 

  • Groner ML, Maynard J, Breyta R et al (2016) Managing marine disease emergencies in an era of rapid change. Phil Trans R Soc B 371:20150364

    Article  PubMed  PubMed Central  Google Scholar 

  • Guindon S, Dufayard JF, Lefort V, Anisimova M, Hordijk W, Gascuel O (2010) New algorithms and methods to estimate maximum-likelihood phylogenies: assessing the performance of PhyML 3.0. Syst Biol 59:307–321

    Article  CAS  PubMed  Google Scholar 

  • Harper JT, Saunders GW (2001) The application of sequences of the ribosomal cistron to the systematics and classification of the florideophyte red algae (Florideophyceae, Rhodophyta). Cah Biol Mar 42:25–38

    Google Scholar 

  • Jombart T (2008) adegenet: a R package for the multivariate analysis of genetic markers. Bioinformatics 24:1403–1405

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  PubMed  PubMed Central  Google Scholar 

  • Katoh K, Standley DM (2013) MAFFT multiple sequence alignment software version 7: improvements in performance and usability. Mol Biol Evol 30:772–780

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kearse M et al (2012) Geneious basic: an integrated and extendable desktop software platform for the organization and analysis of sequence data. Bioinform 28:1647–1649

    Article  Google Scholar 

  • Keeney DB, King TM, Rowe DL, Poulin R (2009) Contrasting mtDNA diversity and population structure in a direct-developing marine gastropod and its trematode parasites. Mol Ecol 18:4591–4603

    Article  PubMed  Google Scholar 

  • Kumar S, Stecher G, Tamura K (2016) MEGA7: molecular evolutionary genetics analysis version 7.0 for bigger datasets. Mol Biol Evol 33:1870–1874

    Article  CAS  PubMed  Google Scholar 

  • Lagrue C, Joannes A, Poulin R, Blasco-Costa I (2016) Genetic structure and host–parasite co-divergence: evidence for trait-specific local adaptation. Biol J Linn Soc 118:344–358

    Article  Google Scholar 

  • Lanfear R, Calcott B, Ho SYW, Guindon S (2012) PartitionFinder: combined selection of partitioning schemes and substitution models for phylogenetic analyses. Mol Biol Evol 29:1695–1701

    Article  CAS  PubMed  Google Scholar 

  • Lanfear R, Frandsen PB, Wright AM, Senfeld T, Calcott B (2016) PartitionFinder 2: new methods for selecting partitioned models of evolution for molecular and morphological phylogenetic analyses. Mol Biol Evol 34:772–773

    Google Scholar 

  • Latham ADM, Poulin R (2002a) Field evidence of the impact of two acanthocephalan parasites on the mortality of three species of New Zealand shore crabs (Brachyura). Mar Biol 141:1131–1139

    Article  Google Scholar 

  • Latham ADM, Poulin R (2002b) Effect of acanthocephalan parasites on hiding behaviour in two species of shore crabs. J Helminthol 76:323–326

    Article  CAS  PubMed  Google Scholar 

  • Latham ADM, Poulin R (2003) Spatiotemporal heterogeneity in recruitment of larval parasites to shore crab intermediate hosts: the influence of shorebird definitive hosts. Can J Zool 81:1282–1291

    Article  Google Scholar 

  • Leigh JW, Bryant D (2015) POPART: full-feature software for haplotype network construction. Methods Ecol Evol 6:1110–1116

    Article  Google Scholar 

  • Martinez-Aquino A, Reyna-Fabian ME, Rosas-Valdez R, Razo-Mendivil U, Pérez-Ponce de León G, Garcia-Varela M (2009) Detecting a complex of cryptic species within Neoechinorhynchus golvani (Acanthocephala: Neoechinorhynchidae) inferred from ITSs and LSU rDNA gene sequences. J Parasitol 95:1040–1047

    Article  CAS  PubMed  Google Scholar 

  • Mazé-Guilmo E, Blanchet S, McCoy KD, Loot G (2016) Host dispersal as the driver of parasite genetic structure: a paradigm lost? Ecol Lett 19:336–347

    Article  PubMed  Google Scholar 

  • McLay CL (1988) Brachyura and crab-like Anomura of New Zealand. University of Auckland Marine Laboratory, Auckland

    Google Scholar 

  • Miller MA, Pfeiffer W, Schwartz T (2010) Creating the CIPRES science gateway for inference of large phylogenetic trees. In: Proceedings of the gateway computing environments workshop, New Orleans, LA, pp 1–8

  • Morjan CL, Rieseberg LH (2004) How species evolve collectively: implications of gene flow and selection for the spread of advantageous alleles. Mol Ecol 13:1341–1356

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Paradis E, Claude J, Strimmer K (2004) APE: analyses of phylogenetics and evolution in R language. Bioinform 20:289–290

    Article  CAS  Google Scholar 

  • Prugnolle F, Théron A, Pointier JP, Jabbour-Zahab R, Jarne P, Durand P, de Meeûs T (2005) Dispersal in a parasitic worm and its two hosts: consequences for local adaptation. Evolution 59:296–303

    Article  PubMed  Google Scholar 

  • Rodriguez SM, D’Elia G (2017) Pan-American marine coastal distribution of the acanthocephalan Profilicollis altmani based on morphometric and phylogenetic analyses of cystacanths from the mole crab Emerita brasiliensis. J Helminthol 91:371–375

    Article  CAS  PubMed  Google Scholar 

  • Ronquist F, Huelsenbeck JP (2003) MRBAYES 3: Bayesian phylogenetic inference under mixed models. Bioinform 19:1572–1574

    Article  CAS  Google Scholar 

  • Ross PM, Hogg ID, Pilditch CA, Lundquist CJ (2009) Phylogeography of New Zealand’s coastal benthos. N Z J Mar Freshw Res 43:1009–1027

    Article  Google Scholar 

  • Rowe L (2013) Dispersal of southern black-backed gulls (Larus dominicanus dominicanus) banded in Canterbury, New Zealand, 1959–1993. Notornis 60:134–142

    Google Scholar 

  • Steinauer ML, Nickol BB, Orti G (2007) Cryptic speciation and patterns of phenotypic variation of a highly variable acanthocephalan parasite. Mol Ecol 16:4097–4109

    Article  CAS  PubMed  Google Scholar 

  • Sutton PJH (2003) The Southland current: a subantarctic current. N Z J Mar Freshw Res 37:645–652

    Article  Google Scholar 

  • Tamura K, Nei M (1993) Estimation of the number of nucleotide substitutions in the control region of mitochondrial-DNA in humans and chimpanzees. Mol Biol Evol 10:512–526

    CAS  PubMed  Google Scholar 

  • Tobias ZJC, Jorge F, Poulin R (2017) Life at the beach: comparative phylogeography of a sandhopper and its nematode parasite reveals extreme lack of parasite mtDNA variation. Biol J Linn Soc 122:113–132

    Article  Google Scholar 

  • Wallis GP, Trewick SA (2009) New Zealand phylogeography: evolution on a small continent. Mol Ecol 18:3548–3580

    Article  PubMed  Google Scholar 

  • Ward JR, Lafferty KD (2004) The elusive baseline of marine disease: are diseases in ocean ecosystems increasing? PLoS Biol 2:e120

    Article  PubMed  PubMed Central  Google Scholar 

  • Wear RG (1970) Life-history studies on New Zealand Brachyura. N Z J Mar Freshw Res 4:3–35

    Article  Google Scholar 

  • Zhang Z, Schwartz S, Wagner L, Miller W (2000) A greedy algorithm for aligning DNA sequences. J Comput Biol 7:203–214

    Article  CAS  PubMed  Google Scholar 

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Acknowledgements

We thank Lynda Hay, Lance Hay, Jahmaine Hay and Kirby McKenzie for assistance with crab collection in the field, and Dr. Bronwen Presswell for providing an adult acanthocephalan specimen.

Funding

This research was funded internally by the Department of Zoology, University of Otago, and received no external funding from commercial or non-profit sectors.

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Authors and Affiliations

  1. Department of Zoology, University of Otago, PO Box 56, Dunedin, 9054, New Zealand

    Eleanor Hay, Fátima Jorge & Robert Poulin

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  1. Eleanor Hay
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  2. Fátima Jorge
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Correspondence to Eleanor Hay.

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The authors declare having no conflict of interest.

Ethical statement

Collection and euthanasia of crabs were approved by the Otago University Animal Ethics Committee (Application no. ET 2/17).

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Responsible Editor: T. Reusch.

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Hay, E., Jorge, F. & Poulin, R. The comparative phylogeography of shore crabs and their acanthocephalan parasites. Mar Biol 165, 69 (2018). https://doi.org/10.1007/s00227-018-3326-y

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