The most vagile host as the main determinant of population connectivity in marine macroparasites

Marine Ecology Progress Series

Volumn 520, Issue , 2015, Pages 85-99

  Feis, Marieke E ^a,b,g   Thieltges, David W ^a   Olsen, Jeanine L ^b   De Montaudouin, Xavier ^c   Jensen, K Thomas ^d   Bazaïri, Hocein ^e   Culloty, Sarah C ^f   Luttikhuizen, Pieternella C ^a  

^a ROYAL NETHERLANDS INSTITUTE FOR SEA RESEARCH   (Netherlands)

^b UNIVERSITY OF GRONINGEN   (Netherlands)

^c UNIVERSITÉ DE BORDEAUX   (France)

^d AARHUS UNIVERSITY   (Denmark)

^e FACULTÉ DES SCIENCES   (Morocco)

^f UNIVERSITY COLLEGE CORK   (Ireland)

^g ALFRED WEGENER INSTITUTE FOR POLAR AND MARINE RESEARCH   (Germany)

Author keywords

Bucephalus minimus; Gymnophallus choledochus; Host parasite dynamics; Invertebrates; Marine ecology; Parasite; Population genetics; Trematode

Indexed keywords

BIRD; COLONIZATION; DISPERSAL; GENE EXPRESSION; HOST-PARASITE INTERACTION; MARINE ECOSYSTEM; PARASITE; POPULATION GENETICS; POPULATION STRUCTURE;

ATLANTIC COAST [AFRICA]; ATLANTIC COAST [EUROPE];

AVES; BUCEPHALUS; GYMNOPHALLUS CHOLEDOCHUS; INVERTEBRATA; TREMATODA;

EID: 84922326711     PISSN: 01718630     EISSN: 16161599     Source Type: Journal    
DOI: 10.3354/meps11096     Document Type: Article

References (82)

1. LITERATURE CITED Alarcon JA, Magoulas A, Georgakopoulos T, Zouros E, Alvarez MC (2004) Genetic comparison of wild and cultivated European populations of the gilthead sea bream (Sparus aurata). Aquaculture 230: 65-80
2. Aurelle D, Ledoux JB, Rocher C, Borsa P, Chenuil A, Féral JP (2011) Phylogeography of red coral (Corallium rubrum): inferences on the evolutionary history of a temperate gorgonian. Genetica 139: 855-869
3. Avise JC (2000) Phylogeography: the history and formation of species. Harvard University Press, Cambridge, MA
4. Bahri-Sfar L, Lemaire C, Ben Hassine OK, Bonhomme F (2000) Fragmentation of sea bass populations in the western and eastern Mediterranean as revealed by microsatellite polymorphism. Proc R Soc Lond B 267: 929-935
5. Ballard JWO, Whitlock MC (2004) The incomplete natural history of mitochondria. Mol Ecol 13: 729-744
6. Bartoli P, Gibson DI (2007) Synopsis of the life cycles of Digenea (Platyhelminthes) from lagoons of the northern coast of the western Mediterranean. J Nat Hist 41: 1553-1570
7. Begg GA, Waldman JR (1999) An holistic approach to fish stock identification. Fish Res 43: 35-44
8. Blasco-Costa I, Poulin R (2013) Host traits explain the genetic structure of parasites: a meta-analysis. Parasitology 140: 1316-1322
9. Blasco-Costa I, Waters JM, Poulin R (2012) Swimming against the current: genetic structure, host mobility and the drift paradox in trematode parasites. Mol Ecol 21: 207-217
10. Blouin MS, Yowell CA, Courtney CH, Dame JB (1995) Host movement and the genetic structure of populations of parasitic nematodes. Genetics 141: 1007-1014
11. Camphuysen CJ, Vercruijsse HJP, Spaans AL (2011) Colony-and age-specific seasonal dispersal of Herring Gulls Larus argentatus breeding in The Netherlands. J Ornithol 152: 849-868
12. Chandarana J, Reish DJ, Johnson RL (2013) Genetic structure of the polychaete Nereis grubei in the context of current patterns and life history. Mar Ecol Prog Ser 473: 215-224
13. Chenuil A, Hoareau TB, Egea E, Penant G and others (2010) An efficient method to find potentially universal population genetic markers, applied to metazoans. BMC Evol Biol 10: 276
14. Chevolot M, Hoarau G, Rijnsdorp AD, Stam WT, Olsen JL (2006) Phylogeography and population structure of thornback rays (Raja clavata L. , Rajidae). Mol Ecol 15: 3693-3705
15. Clarke LM, Munch SB, Thorrold SR, Conover DO (2010) High connectivity among locally adapted populations of a marine fish (Menidia menidia). Ecology 91: 3526-3537
16. Cowen RK, Lwiza KMM, Sponaugle S, Paris CB, Olson DB (2000) Connectivity of marine populations: open or closed? Science 287: 857-859
17. Criscione CD (2008) Parasite co-structure: broad and local scale approaches. Parasite 15: 439-443
18. Criscione CD, Blouin MS (2004) Life cycles shape parasite evolution: comparative population genetics of salmon trematodes. Evolution 58:198-202
19. Criscione CD, Poulin R, BlouinMS (2005) Molecular ecology of parasites: elucidating ecological and microevolutionary processes. Mol Ecol 14: 2247-2257
20. Criscione CD, Vilas R, Paniagua E, Blouin MS (2011) More than meets the eye: detecting cryptic microgeographic population structure in a parasite with a complex life cycle. Mol Ecol 20: 2510-2524
21. Cuveliers EL, Larmuseau MHD, Hellemans B, Verherstraeten S, Volckaert FAM, Maes GE (2012) Multimarker estimate of genetic connectivity of sole (Solea solea) in the North-East Atlantic Ocean. Mar Biol 159: 1239-1253
22. de Montaudouin X, Thieltges DW, Gam M, Krakau M and others (2009) Trematode species in the cockle Cerastoderma edule: identification key and distribution along the North-East Atlantic shoreline. J Mar Biol Assoc UK 89: 543-556
23. Di Franco A, Gillanders BM, De Benedetto G, Pennetta A, De Leo GA, Guidetti P (2012) Dispersal patterns of coastal fish: implications for designing networks of marine protected areas. PLoS ONE 7: e31681
24. Dowling DK, Friberg U, Lindell J (2008) Evolutionary implications of non-neutral mitochondrial genetic variation. Trends Ecol Evol 23: 546-554
25. Drummond AJ, Rambaut A (2007) BEAST: Bayesian evolutionary analysis by sampling trees. BMC Evol Biol 7: 214
26. Drummond AJ, Rambaut A, Shapiro B, Pybus OG (2005) Bayesian coalescent inference of past population dynamics from molecular sequences. Mol Biol Evol 22: 1185-1192
27. El-Darsh HEM, Whitfield PJ (1999) Digenean metacercariae (Timoniella spp. , Labratrema minimus and Cryptocotyle concava) from the flounder, Platichthys flesus, in the tidal Thames. J Helminthol 73: 103-113
28. Esch GW, Kennedy CR, Bush AO, Aho JM (1988) Patterns in helminth communities in freshwater fish in Great Britain: alternative strategies for colonization. Parasitology 96: 519-532
29. 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
30. Faliex E, Biagianti S (1987) Metacercarial infection of marine fish by Labratrema minimus (Digenea, Bucephalidae): histo-cytological analysis of host-parasite relationship. Aquaculture 67: 229-232
31. Frade PR, Reyes-Nivia MC, Faria J, Kaandorp JA, Luttik-huizen PC, Bak RPM (2010) Semi-permeable species boundaries in the coral genus Madracis: introgression in a brooding coral system. Mol Phylogenet Evol 57: 1072-1090
32. Frank B (1969) Der bemerkenswerte Lebenszyklus des marinen Vogeltrematoden Gymnophallus choledochus. J Ornithol 110: 471-474
33. Gostel MR, Weeks A (2014) Development of novel, exonprimed intron-crossing (EPIC) markers from EST databases and evaluation of their phylogenetic utility in Commiphora (Burseraceae). Appl Plant Sci 2: apps. 130009
34. Greischar MA, Koskella B (2007) A synthesis of experimental work on parasite local adaptation. Ecol Lett 10: 418-434
35. Hall TA (1999) BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucleic Acids Symp Ser 41: 95-98
36. Hayward A (2010) Cryptic diversity and patterns of host specificity in trematode flatworms. Mol Ecol 19: 2602-2604
37. Heled J, Drummond AJ (2008) Bayesian inference of population size history from multiple loci. BMC Evol Biol 8: 289
38. Jannotti-Passos LK, Souza CP, Parra JC (2001) Biparental mitochondrial DNA inheritance in the parasitic trematode Schistosoma mansoni. J Parasitol 87: 79-82
39. Kear J (2005) Ducks, geese and swans, Vol 1: general chapters; species accounts (Anhima to Salvadorina). Oxford University Press, Oxford
40. Keeney DB, Waters J, Poulin R (2007) Diversity of trematode genetic clones within amphipods and the timing of sameclone infections. Int J Parasitol 37: 351-357
41. Keeney DB, Bryan-Walker K, King TM, Poulin R (2008) Local variation of within-host clonal diversity coupled with genetic homogeneity in a marine trematode. Mar Biol 154: 183-190
42. Keeney DB, King TM, Rowe DL, Poulin R (2009) Contrasting mtDNA diversity and population structure in a directdeveloping marine gastropod and its trematode parasites. Mol Ecol 18: 4591-4603
43. Kesaniemi JE, Bostrom C, Knott KE (2012) New genetic markers reveal population genetic structure at different spatial scales in the opportunistic polychaete Pygospio elegans. Hydrobiologia 691: 213-223
44. Krakau M, Jacobsen S, Jensen KT, Reise K (2012) The cockle Cerastoderma edule at Northeast Atlantic shores: genetic signatures of glacial refugia. Mar Biol 159: 221-230
45. Lemaire C, Versini JJ, Bonhomme F (2005) Maintenance of genetic differentiation across a transition zone in the sea: discordance between nuclear and cytoplasmic markers. J Evol Biol 18: 70-80
46. Lenormand T (2002) Gene flow and the limits to natural selection. Trends Ecol Evol 17: 183-189
47. Leung TLF, Keeney DB, Poulin R (2009) Cryptic species complexes in manipulative echinostomatid trematodes: when two become six. Parasitology 136: 241-252
48. Loos-Frank B (1969) Studies on Gymnophallid trematodes of North Sea. I. Alternative life cycles of Gymnophallus choledochus Odhner 1900. Z Parasitenkd 32: 135-156
49. Lopes RJ, Hortas F, Wennerberg L (2008) Geographical segregation in Dunlin Calidris alpina populations wintering along the East Atlantic migratory flyway-evidence from mitochondrial DNA analysis. Divers Distrib 14: 732-741
50. Luttikhuizen PC, Drent J, Van Delden W, Piersma T (2003) Spatially structured genetic variation in a broadcastspawning bivalve: quantitative versus molecular traits. J Evol Biol 16: 260-272
51. MacKenzie K (2002) Parasites as biological tags in population studies of marine organisms: an update. Parasitology 124: S153-S163
52. MacKenzie K, Abounza P (1998) Parasites as biological tags for stock discrimination of marine fish: a guide to procedures and methods. Fish Res 38: 45-56
53. Maillard C (1975) Labratrema lamirandi (Carrère, 1937) (Trematoda, Bucephalidae) parasite de Dicentrarchus labrax (L. , 1758). Création du genre Labratrema. Cycle évolutif. Bull Mus Natl Hist Nat 3 193: 69-80
54. Maillard C (1976) Distomatoses de poissons en milieu lagunaire. University of Montpellier, Montpellier
55. Martinez L, Mendez J, Insua A, Arias-Perez A, Freire R (2013) Genetic diversity and population differentiation in the cockle Cerastoderma edule estimated by microsatellite markers. Helgol Mar Res 67: 179-189
56. McPeek MA, Holt RD (1992) The evolution of dispersal in spatially and temporally varying environments. Am Nat 140: 1010-1027
57. Miura O, Kuris AM, Torchin ME, Hechinger RF, Dunhum EJ, Chiba S (2005) Molecular-genetic analyses reveal cryptic species of trematodes in the intertidal gastropod, Batillaria cumingi (Crosse). Int J Parasitol 35: 793-801
58. Moszczynska A, Locke SA, McLaughlin JD, Marcogliese DJ, Crease TJ (2009) Development of primers for the mitochondrial cytochrome c oxidase I gene in digenetic trematodes (Platyhelminthes) illustrates the challenge of barcoding parasitic helminths. Mol Ecol Resour 9: 75-82
59. Naciri M, Lemaire C, Borsa P, Bonhomme F (1999) Genetic study of the Atlantic/Mediterranean transition in sea bass (Dicentrarchus labrax). J Hered 90: 591-596
60. Olson MA, Zajac RN, Russello MA (2009) Estuarine-scale genetic variation in the polychaete Hobsonia florida (Ampharetidae; Annelida) in Long Island Sound and relationships to Pleistocene glaciations. Biol Bull 217: 86-94
61. Pawson MG, Pickett GD, Leballeur J, Brown M, Fritsch M (2007a) Migrations, fishery interactions, and management units of sea bass (Dicentrarchus labrax) in Northwest Europe. ICES J Mar Sci 64: 332-345
62. Pawson MG, Kupschus S, Pickett GD (2007b) The status of sea bass (Dicentrarchus labrax) stocks around England and Wales, derived using a separable catch-at-age model, and implications for fisheries management. ICES J Mar Sci 64: 346-356
63. Pickett GD, Pawson MG (1994) Sea bass: Biology, exploitation and conservation. Chapman & Hall, London
64. Pina S, Barandela T, Santos MJ, Russell-Pinto F, Rodrigues P (2009) Identification and description of Bucephalus minimus (Digenea: Bucephalidae) life cycle in Portugal: morphological, histopathological, and molecular data. J Parasitol 95: 353-359
65. Poulin R (2007) Evolutionary ecology of parasites, 2nd edn. Princeton University Press, Princeton, NJ
66. Poulin R (2011) Uneven distribution of cryptic diversity among higher taxa of parasitic worms. Biol Lett 7: 241-244
67. Prugnolle F, Liu H, de Meeus T, Balloux F (2005) Population genetics of complex life-cycle parasites: an illustration with trematodes. Int J Parasitol 35: 255-263
68. Quéré N, Guinand B, Kuhl H, Reinhardt R, Bonhomme F, Desmarais E (2010) Genomic sequences and genetic differentiation at associated tandem repeat markers in growth hormone, somatolactin and insulin-like growth factor-1 genes of the sea bass, Dicentrarchus labrax. Aquat Living Resour 23: 285-296
69. Rambaut A, Drummond AJ (2007) Tracer v1. 4, available at http: //beast. bio. ed. ac. uk/Tracer Rauch G, Kalbe M, Reusch TBH (2005) How a complex life cycle can improve a parasite's sex life. J Evol Biol 18: 1069-1075
70. Rogers AR, Harpending H (1992) Population growth makes waves in the distribution of pairwise genetic differences. Mol Biol Evol 9: 552-569
71. Rozen S, Skaletsky H (2000) Primer3 on the WWW for general users and for biologist programmers. Methods Mol Biol 132: 365-386
72. Tamura K, Peterson D, Peterson N, Stecher G, Nei M, Kumar S (2011) MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol Biol Evol 28: 2731-2739
73. Thieltges DW, Ferguson MAD, Jones CS, Krakau M and others (2009) Distance decay of similarity among parasite communities of three marine invertebrate hosts. Oecologia 160: 163-173
74. Thieltges DW, Marcogliese DJ, Blanar CA, Poulin R (2013) Trematode prevalence-occupancy relationships on re-gional and continental spatial scales in marine gastropod hosts. Mar Ecol Prog Ser 490: 147-154
75. Tiedemann R, Paulus KB, Scheer M, Von Kistowski KG, Skirnisson K, Bloch D, DamM(2004) Mitochondrial DNA and microsatellite variation in the eider duck (Somateria mollissima) indicate stepwise postglacial colonization of Europe and limited current long-distance dispersal. Mol Ecol 13: 1481-1494
76. Varela AI, Ritchie PA, Smith PJ (2013) Global genetic population structure in the commercially exploited deep-sea teleost orange roughy (Hoplostethus atlanticus) based on microsatellite DNA analyses. Fish Res 140: 83-90
77. Vilas R, SanmartínML, Paniagua E (2004) Genetic variability of natural populations of trematodes of the genus Lecithochirium parasites of eels. Parasitology 129: 191-201
78. Vilas R, Criscione CD, Blouin MS (2005) A comparison between mitochondrial DNA and the ribosomal internal transcribed regions in prospecting for cryptic species of platyhelminth parasites. Parasitology 131: 839-846
79. Walther GR, Post E, Convey P, Menzel A and others (2002) Ecological responses to recent climate change. Nature 416: 389-395
80. Webb SD, Keeling MJ, Boots M (2013) The role of spatial population structure on the evolution of parasites with acquired immunity and demography. J Theor Biol 324: 21-31
81. Whitfield AK, Panfili J, Durand JD (2012) A global review of the cosmopolitan flathead mullet Mugil cephalus Linnaeus 1758 (Teleostei: Mugilidae), with emphasis on the biology, genetics, ecology and fisheries aspects of this apparent species complex. Rev Fish Biol Fish 22: 641-681
82. Zakas C, Wares JP (2012) Consequences of a poecilogonous life history for genetic structure in coastal populations of the polychaete Streblospio benedicti. Mol Ecol 21: 5447-5460