Influence of the larval phase on connectivity: Strong differences in the genetic structure of brooders and broadcasters in the Ophioderma longicauda species complex

Molecular Ecology

Volumn 24, Issue 24, 2015, Pages 6080-6094

  Weber, A A T ^a,b   Merigot B ^c   Valiere S ^d   Chenuil, A ^a  

^a AIX MARSEILLE UNIVERSITY   (France)

^b UNIVERSITY OF BASEL   (Switzerland)

^c UNIV MONTPELLIER   (France)

^d Institut National de la Recherche Agronomique   (France)

Author keywords

DNA barcoding; echinoderms; life history evolution; phylogeography; population genetics empirical

Indexed keywords

GENETIC MARKER; MITOCHONDRIAL DNA; TRANSCRIPTOME;

ANIMAL; ANIMAL DISPERSAL; DNA SEQUENCE; ECHINODERM; EVOLUTION; GENETIC MARKER; GENETIC VARIATION; GENETICS; GENOTYPE; GREECE; INTRON; LARVA; MEDITERRANEAN SEA; PHYLOGEOGRAPHY; POPULATION GENETICS; REPRODUCTION;

ANIMAL DISTRIBUTION; ANIMALS; BIOLOGICAL EVOLUTION; DNA, MITOCHONDRIAL; ECHINODERMATA; GENETIC MARKERS; GENETIC VARIATION; GENETICS, POPULATION; GENOTYPE; GREECE; INTRONS; LARVA; MEDITERRANEAN SEA; PHYLOGEOGRAPHY; REPRODUCTION; SEQUENCE ANALYSIS, DNA; TRANSCRIPTOME;

EID: 84955279622     PISSN: 09621083     EISSN: 1365294X     Source Type: Journal    
DOI: 10.1111/mec.13456     Document Type: Article

References (91)

1. Arndt A, Smith MJ, (1998) Genetic diversity and population structure in two species of sea cucumber: differing patterns according to mode of development. Molecular Ecology, 7, 1053-1064.
2. Ayre DJ, Hughes TP, (2000) Genotypic diversity and gene flow in brooding and spawning corals along the Great Barrier Reef, Australia. Evolution, 54, 1590-1605.
3. Ayre DJ, Minchinton TE, Perrin C, (2009) Does life history predict past and current connectivity for rocky intertidal invertebrates across a marine biogeographic barrier? Molecular Ecology, 18, 1887-1903.
4. Bandelt HJ, Forster P, Röhl A, (1999) Median-joining networks for inferring intraspecific phylogenies. Molecular Biology and Evolution, 16, 37-48.
5. Barbosa SS, Klanten SO, Puritz JB, Toonen RJ, Byrne M, (2013) Very fine-scale population genetic structure of sympatric asterinid sea stars with benthic and pelagic larvae: influence of mating system and dispersal potential. Biological Journal of the Linnean Society, 108, 821-833.
6. Baus E, Darrock DJ, Bruford MW, (2005) Gene-flow patterns in Atlantic and Mediterranean populations of the Lusitanian sea star Asterina gibbosa. Molecular Ecology, 14, 3373-3382.
7. Beerli P, Felsenstein J, (2001) Maximum likelihood estimation of a migration matrix and effective population sizes in n subpopulations by using a coalescent approach. Proceedings of the National Academy of Sciences, USA, 98, 4563-4568.
8. Belkhir K, Borsa P, Chikhi L, Raufaste N, Bonhomme F, (2004) GENETIX 4.05, Population Genetics Software for Windows TM. Université de Montpellier II, Montpellier.
9. Berger EM, (1973) Gene-enzyme variation in three sympatric species of Littorina. The Biological Bulletin, 145, 83-90.
10. Bohonak AJ, (1999) Dispersal, gene flow, and population structure. The Quarterly Review of Biology, 74, 21-45.
11. Boissin E, Stöhr S, Chenuil A, (2011) Did vicariance and adaptation drive cryptic speciation and evolution of brooding in Ophioderma longicauda (Echinodermata: Ophiuroidea), a common Atlanto-Mediterranean ophiuroid? Molecular Ecology, 20, 4737-4755.
12. Chenuil A, (2012) How to infer reliable diploid genotypes from NGS or traditional sequence data: from basic probability to experimental optimization. Journal of Evolutionary Biology, 25, 949-960.
13. Chenuil A, Egea E, Rocher C, Touzet H, Féral J-P, (2008) Does hybridization increase evolutionary rate? Data from the 28S-rDNA D8 domain in Echinoderms. Journal of Molecular Evolution, 67, 539-550.
14. Collin R, (2001) The effects of mode of development on phylogeography and population structure of North Atlantic Crepidula (Gastropoda: Calyptraeidae). Molecular Ecology, 10, 2249-2262.
15. Crandall ED, Frey MA, Grosberg RK, Barber PH, (2008) Contrasting demographic history and phylogeographical patterns in two Indo-Pacific gastropods. Molecular Ecology, 17, 611-626.
16. Crooks KR, Sanjayan M, (2006) Connectivity conservation: maintaining connections for nature. In: Connectivity Conservation (eds., Crooks KR, Sanjayan M,), pp. 1-19. Cambridge University Press, Cambridge, UK.
17. Dawson MN, (2012) Parallel phylogeographic structure in ecologically similar sympatric sister taxa. Molecular Ecology, 21, 987-1004.
18. Dawson MN, (2014a) Natural experiments and meta-analyses in comparative phylogeography. Journal of Biogeography, 41, 52-65.
19. Dawson MN, (2014b) Biogeography and complex traits: dispersal syndromes, in the sea. Frontiers of Biogeography, 6, 11-15.
20. Dawson MN, Louie KD, Barlow M, Jacobs DK, Swift CC, (2002) Comparative phylogeography of sympatric sister species, Clevelandia ios and Eucyclogobius newberryi (Teleostei, Gobiidae), across the California Transition Zone. Molecular Ecology, 11, 1065-1075.
21. Dawson MN, Hays CG, Grosberg RK, Raimondi PT, (2014) Dispersal potential and population genetic structure in the marine intertidal of the eastern North Pacific. Ecological Monographs, 84, 435-456.
22. Deschuyteneer M, Jangoux M, (1978) Comportement alimentaire et structures digestives d'Ophioderma longicauda (Retzius) (Echinodermata, Ophiuroidea). Annales de L'Institut Océanographique, 54, 127-138.
23. DeWit P, Pespeni MH, Ladner JT, et al,. (2012) The simple fool's guide to population genomics via RNA-Seq: an introduction to high-throughput sequencing data analysis. Molecular Ecology Resources, 12, 1058-1067.
24. DeWit P, Pespeni MH, Palumbi SR, (2015) SNP genotyping and population genomics from expressed sequences-current advances and future possibilities. Molecular Ecology, 24, 2310-2323.
25. Duffy JE, (1993) Genetic population structure in two tropical sponge-dwelling shrimps that differ in dispersal potential. Marine Biology, 116, 459-470.
26. Edgar RC, (2004) MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Research, 32, 1792-1797.
27. Edmands S, (2001) Phylogeography of the intertidal copepod Tigriopus californicus reveals substantially reduced population differentiation at northern latitudes. Molecular Ecology, 10, 1743-1750.
28. Emlet RB, (1995) Developmental mode and species geographic range in regular sea urchins (Echinodermata: Echinoidea). Evolution, 49, 476-489.
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. Molecular Ecology Resources, 10, 564-567.
30. Excoffier L, Smouse PE, Quattro JM, (1992) Analysis of molecular variance inferred from metric distances among DNA haplotypes: application to human mitochondrial DNA restriction data. Genetics, 131, 479-491.
31. Fenaux L, (1969) Le développement larvaire chez Ophioderma longicauda (Retzius). Cahiers de Biologie Marine, 10, 59-62.
32. Fenaux L, (1972) Evolution saisonnière des gonades chez l'Ophiure Ophioderma longicauda (RETZIUS), Ophiuroidea. Internationale Revue der Gesamten Hydrobiologie und Hydrographie, 57, 257-262.
33. Foltz DW, (2003) Invertebrate species with nonpelagic larvae have elevated levels of nonsynonymous substitutions and reduced nucleotide diversities. Journal of Molecular Evolution, 57, 607-612.
34. Foltz DW, Hrincevich AW, Rocha-Olivares A, (2004) Apparent selection intensity for the cytochrome oxidase subunit I gene varies with mode of reproduction in Echinoderms. Genetica, 122, 115-125.
35. Fu Y-X, (1997) Statistical tests of neutrality of mutations against population growth, hitchhiking and background selection. Genetics, 147, 915-925.
36. Fu YX, Li WH, (1993) Statistical tests of neutrality of mutations. Genetics, 133, 693-709.
37. Gouy M, Guindon S, Gascuel O, (2010) SeaView Version 4: a multiplatform graphical user interface for sequence alignment and phylogenetic tree building. Molecular Biology and Evolution, 27, 221-224.
38. Hart MW, Marko PB, (2010) It's about time: divergence, demography, and the evolution of developmental modes in marine invertebrates. Integrative and Comparative Biology, 50, 643-661.
39. Haye PA, Segovia NI, Muñoz-Herrera NC, et al,. (2014) Phylogeographic structure in benthic marine invertebrates of the southeast Pacific coast of Chile with differing dispersal potential. PLoS ONE, 9, e88613.
40. Hedgecock D, Pudovkin AI, (2011) Sweepstakes reproductive success in highly fecund marine fish and shellfish: a review and commentary. Bulletin of Marine Science, 87, 971-1002.
41. Hedrick P, (2005) Large variance in reproductive success and the Ne/N ratio. Evolution, 59, 1596-1599.
42. Hellberg ME, (1996) Dependence of gene flow on geographic distance in two solitary corals with different larval dispersal capabilities. Evolution, 50, 1167-1175.
43. Hellberg ME, (2009) Gene flow and isolation among populations of marine animals. Annual Review of Ecology, Evolution, and Systematics, 40, 291-310.
44. Hellberg ME, Burton RS, Neigel JE, Palumbi SR, (2002) Genetic assessment of connectivity among marine populations. Bulletin of Marine Science, 70, 273-290.
45. Hey J, (2010) Isolation with migration models for more than two populations. Molecular Biology and Evolution, 27, 905-920.
46. Hoareau TB, Boissin E, Paulay G, Bruggemann JH, (2013) The Southwestern Indian Ocean as a potential marine evolutionary hotspot: perspectives from comparative phylogeography of reef brittle-stars. Journal of Biogeography, 40, 2167-2179.
47. Hoffman JI, Clarke A, Linse K, Peck LS, (2011) Effects of brooding and broadcasting reproductive modes on the population genetic structure of two Antarctic gastropod molluscs. Marine Biology, 158, 287-296.
48. Hoskin MG, (1997) Effects of contrasting modes of larval development on the genetic structures of populations of three species of prosobranch gastropods. Marine Biology, 127, 647-656.
49. Hunt A, (1993) Effects of contrasting patterns of larval dispersal on the genetic connectedness of local populations of two intertidal starfish, Patiriella calcar and P. exigua. Marine Ecology Progress Series, 92, 179-186.
50. Keever CC, Sunday J, Puritz JB, et al,. (2009) Discordant distribution of populations and genetic variation in a sea star with high dispersal potential. Evolution, 63, 3214-3227.
51. Kimura M, (1969) The number of heterozygous nucleotide sites maintained in a finite population due to steady flux of mutations. Genetics, 61, 893-903.
52. Knowlton N, Jackson JB, (1993) Inbreeding and outbreeding in marine invertebrates. In: The Natural History of Inbreeding and Outbreeding (ed., Thornhill NW,), pp. 200-249. University of Chicago Press, Chicago, Illinois.
53. Kyle CJ, Boulding EG, (2000) Comparative population genetic structure of marine gastropods (Littorina spp.) with and without pelagic larval dispersal. Marine Biology, 137, 835-845.
54. Laine A-L, (2005) Spatial scale of local adaptation in a plant-pathogen metapopulation. Journal of Evolutionary Biology, 18, 930-938.
55. Ledoux J-B, Tarnowska K, Gérard K, et al,. (2012) Fine-scale spatial genetic structure in the brooding sea urchin Abatus cordatus suggests vulnerability of the Southern Ocean marine invertebrates facing global change. Polar Biology, 35, 611-623.
56. Lee HJ, Boulding EG, (2009) Spatial and temporal population genetic structure of four northeastern Pacific littorinid gastropods: the effect of mode of larval development on variation at one mitochondrial and two nuclear DNA markers. Molecular Ecology, 18, 2165-2184.
57. Librado P, Rozas J, (2009) DnaSP v5: a software for comprehensive analysis of DNA polymorphism data. Bioinformatics, 25, 1451-1452.
58. Lischer HEL, Excoffier L, (2012) PGDSpider: an automated data conversion tool for connecting population genetics and genomics programs. Bioinformatics, 28, 298-299.
59. Luiz OJ, Allen AP, Robertson DR, et al,. (2013) Adult and larval traits as determinants of geographic range size among tropical reef fishes. Proceedings of the National Academy of Sciences, USA, 110, 16498-16502.
60. Marko PB, (2004) 'What's larvae got to do with it?' Disparate patterns of post-glacial population structure in two benthic marine gastropods with identical dispersal potential. Molecular Ecology, 13, 597-611.
61. Marko PB, Hart MW, (2011) The complex analytical landscape of gene flow inference. Trends in Ecology & Evolution, 26, 448-456.
62. McMillan WO, Raff RA, Palumbi SR, (1992) Population genetic consequences of developmental evolution in sea urchins (genus Heliocidaris). Evolution, 46, 1299-1312.
63. Palmer AR, Strathmann RR, (1981) Scale of dispersal in varying environments and its implications for life histories of marine invertebrates. Oecologia, 48, 308-318.
64. Palumbi SR, (2003) Population genetics, demographic connectivity, and the design of marine reserves. Ecological Applications, 13, 146-158.
65. Pechenik JA, (1999) On the advantages and disadvantages of larval stages in benthic marine invertebrate life cycles. Marine Ecology Progress Series, 177, 269-297.
66. Poulin E, Feral J-P, (1996) Why are there so many species of brooding antarctic Echinoids? Evolution, 50, 820-830.
67. Puritz JB, Keever CC, Addison JA, et al,. (2012) Extraordinarily rapid life-history divergence between Cryptasterina sea star species. Proceedings of the Royal Society B: Biological Sciences, 279, 3914-3922.
68. Rabinowitz A, Zeller KA, (2010) A range-wide model of landscape connectivity and conservation for the jaguar, Panthera onca. Biological Conservation, 143, 939-945.
69. Riginos C, Douglas KE, Jin Y, Shanahan DF, Treml EA, (2011) Effects of geography and life history traits on genetic differentiation in benthic marine fishes. Ecography, 34, 566-575.
70. Riginos C, Buckley YM, Blomberg SP, Treml EA, (2014) Dispersal capacity predicts both population genetic structure and species richness in reef fishes. The American Naturalist, 184, 52-64.
71. Romiguier J, Gayral P, Ballenghien M, et al,. (2014) Comparative population genomics in animals uncovers the determinants of genetic diversity. Nature, 515, 261-263.
72. Sanford E, Kelly MW, (2011) Local adaptation in marine invertebrates. Annual Review of Marine Science, 3, 509-535.
73. Schloss PD, Westcott SL, Ryabin T, et al,. (2009) Introducing mothur: open-source, platform-independent, community-supported software for describing and comparing microbial communities. Applied and Environmental Microbiology, 75, 7537-7541.
74. Selkoe KA, Toonen RJ, (2011) Marine connectivity: a new look at pelagic larval duration and genetic metrics of dispersal. Marine Ecology Progress Series, 436, 291-305.
75. Shanks AL, (2009) Pelagic larval duration and dispersal distance revisited. The Biological Bulletin, 216, 373-385.
76. Shanks AL, Grantham BA, Carr MH, (2003) Propagule dispersal distance and the size and spacing of marine reserves. Ecological Applications, 13, 159-169.
77. Sherman CDH, Hunt A, Ayre DJ, (2008) Is life history a barrier to dispersal? Contrasting patterns of genetic differentiation along an oceanographically complex coast. Biological Journal of the Linnean Society, 95, 106-116.
78. Siegel DA, Kinlan BP, Gaylord B, Gaines SD, (2003) Lagrangian descriptions of marine larval dispersion. Marine Ecology Progress Series, 260, 83-96.
79. Steele CA, Baumsteiger J, Storfer A, (2009) Influence of life-history variation on the genetic structure of two sympatric salamander taxa. Molecular Ecology, 18, 1629-1639.
80. Stöhr S, Boissin E, Chenuil A, (2009) Potential cryptic speciation in Mediterranean populations of Ophioderma (Echinodermata: Ophiuroidea). Zootaxa, 2071, 1-20.
81. Strathmann RR, (1985) Feeding and nonfeeding larval development and life-history evolution in marine invertebrates. Annual Review of Ecology and Systematics, 16, 339-361.
82. Tajima F, (1989) Statistical method for testing the neutral mutation hypothesis by DNA polymorphism. Genetics, 123, 585-595.
83. Tarnowska K, Krakau M, Jacobsen S, et al,. (2012) Comparative phylogeography of two sister (congeneric) species of cardiid bivalve: strong influence of habitat, life history and post-glacial history. Estuarine, Coastal and Shelf Science, 107, 150-158.
84. Teske PR, Papadopoulos I, Zardi GI, et al,. (2007) Implications of life history for genetic structure and migration rates of southern African coastal invertebrates: planktonic, abbreviated and direct development. Marine Biology, 152, 697-711.
85. Tortonese E, (1983) Remarks on the morphology and taxonomy of Ophioderma longicaudum (Retz.) from the Mediterranean. Atti Della Societa Italiana di Scienze Naturali e del Museo Civico di Storia Naturale in Milano, 124, 21-28.
86. Warner RR, Palumbi SR, (2003) Larvae retention: genes or oceanography? Response. Science, 300, 1658.
87. Weber AA-T, (2015) Etude Écologique et Génétique du Complexe D'espèces Cryptiques Ophioderma Longicauda (Ophiuroidea: Echinodermata): Comparaison Entre Lignées Incubantes et Lignées Produisant des Larves Planctoniques. Aix-Marseille Université, Marseille.
88. Weber AA-T, Dupont S, Chenuil A, (2013) Thermotolerance and regeneration in the brittle star species complex Ophioderma longicauda: a preliminary study comparing lineages and Mediterranean basins. Comptes Rendus Biologies, 336, 572-581.
89. Weber AA-T, Stöhr S, Chenuil A, (2014) Genetic data, reproduction season and reproductive strategy data support the existence of biological species in Ophioderma longicauda. Comptes Rendus Biologies, 337, 553-560.
90. Webster MS, Marra PP, Haig SM, Bensch S, Holmes RT, (2002) Links between worlds: unraveling migratory connectivity. Trends in Ecology & Evolution, 17, 76-83.
91. Weersing K, Toonen RJ, (2009) Population genetics, larval dispersal, and connectivity in marine systems. Marine Ecology Progress Series, 393, 1-12.