Genomic analyses suggest strong population connectivity over large spatial scales of the commercially important baitworm, Australonuphis teres (Onuphidae)
Amanda Padovan
A B I , Rowan C. Chick C , Victoria J. Cole C , Ludovic Dutoit D , Patricia A. Hutchings E F , Cameron Jack G and Ceridwen I. Fraser A H
+ Author Affiliations
- Author Affiliations
A Fenner School of Environment and Society, Building 44, Australian National University, Canberra, ACT 2601, Australia.
B CSIRO, Black Mountain Science and Innovation Park, Clunies Ross Street, Canberra, ACT 2601, Australia.
C New South Wales Department of Primary Industries, Port Stephens Fisheries Institute, Taylors Beach, NSW 2316, Australia.
D Department of Zoology, University of Otago, 340 Great King Street, Dunedin, 9016, New Zealand.
E Australian Museum Research Institute, Australian Museum, 1 William Street, Sydney, NSW 2010, Australia.
F Department of Biological Sciences, Macquarie University, North Ryde, NSW 2109, Australia.
G ANU Bioinformatics Consultancy, John Curtin School of Medical Research, Australian National University, Acton, ACT 2601, Australia.
H Department of Marine Science, University of Otago, PO Box 56, Dunedin, 9054, New Zealand.
I Corresponding author. Email: amanda.padovan@csiro.au
Marine and Freshwater Research 71(11) 1549-1556 https://doi.org/10.1071/MF20044
Submitted: 11 February 2020 Accepted: 27 April 2020 Published: 21 May 2020
Journal Compilation © CSIRO 2020 Open Access CC BY
Abstract
Barriers to dispersal can disrupt gene flow between populations, resulting in genetically distinct populations. Although many marine animals have potential for long-distance dispersal via a planktonic stage, gene flow among populations separated by large geographic distances is not always evident. Polychaetes are ecologically important and have been used as biological surrogates for marine biodiversity. Some polychaete species are used as bait for recreational fisheries, with this demand supporting commercial fisheries for polychaetes to service the retail bait market. However, despite their ecological and economic importance, very little is known about the life history or population dynamics of polychaetes, and few studies have used genetic or genomic approaches to understand polychaete population connectivity. Here, we investigate the population structure of one commonly collected beachworm species used for bait on the eastern coast of Australia, namely, Australonuphis teres, by using genome-wide single-nucleotide polymorphism data. We sampled A. teres from hierarchical nested spatial scales along 900 km of the coast in New South Wales. We identified six genetic groups, but there was no clear geographic pattern of distribution. Our results suggest that there is considerable gene flow among the sampled populations. These high-resolution genomic data support the findings of previous studies, and we infer that oceanographic processes promote genetic exchange among polychaete populations in south-eastern Australia.
Additional keywords: admixture, fisheries, genotype-by-sequencing, management, polychaete, population structure, SNP.
References
Andrews, S. (2010). FASTQC. A quality control tool for high throughput sequence data. Available at https://www.bioinformatics.babraham.ac.uk/projects/fastqc/ [verified 5 May 2020].Bellgrove, A., van Rooyen, A., Weeks, A. R., Clark, J. S., Doblin, M. A., and Miller, A. D. (2017). New resource for population genetics studies on the Australasian intertidal brown alga, Hormosira banksii: isolation and characterization of 15 polymorphic microsatellite loci through next generation DNA sequencing. Journal of Applied Phycology 29, 1721–1727.
| New resource for population genetics studies on the Australasian intertidal brown alga, Hormosira banksii: isolation and characterization of 15 polymorphic microsatellite loci through next generation DNA sequencing.Crossref | GoogleScholarGoogle Scholar |
Bougeard, S., and Dray, S. (2018). Supervised multiblock analysis in R with the ade4 package. Journal of Statistical Software 86, 1–17.
| Supervised multiblock analysis in R with the ade4 package.Crossref | GoogleScholarGoogle Scholar |
Bristow, G. A., and Vadas, R. L. (1991). Genetic variability in blood worm (Glycera dibranchiata) populations in the Gulf of Maine. Marine Biology 109, 311–319.
| Genetic variability in blood worm (Glycera dibranchiata) populations in the Gulf of Maine.Crossref | GoogleScholarGoogle Scholar |
Catchen, J., Hohenlohe, P. A., Bassham, S., Amores, A., and Cresko, W. A. (2013). Stacks: an analysis tool set for population genomics. Molecular Ecology 22, 3124–3140.
| Stacks: an analysis tool set for population genomics.Crossref | GoogleScholarGoogle Scholar | 23701397PubMed |
Chan, K. Y. K., Sewell, M. A., and Byrne, M. (2018). Revisiting the larval dispersal black box in the Anthropocene. ICES Journal of Marine Science 75, 1841–1848.
| Revisiting the larval dispersal black box in the Anthropocene.Crossref | GoogleScholarGoogle Scholar |
Chatzigeorgiou, G., Sarropoulou, E., Vasileiadou, K., Brown, C., Faulwetter, S., Kotoulas, G., and Arvanitidis, C. (2015) Potential links between polychaete community structure and population genetics (Hermodice carunculatasmith) patterns in the shallow hard substrates. In ‘11th Panhellenic Symposium on Oceanography and Fisheries’. Mytilene, Lesvos island, Greece. pp. 577–580.
Chessel, D., Dufour, A.-B., and Thioulouse, J. (2004). The {ade4} Package – {I}: one-table methods. R News 4, 5–10.
Cole, V. J., Chapman, M. G., and Underwood, A. J. (2007). Landscapes and life-histories influence colonisation of polychaetes to intertidal biogenic habitats. Journal of Experimental Marine Biology and Ecology 348, 191–199.
| Landscapes and life-histories influence colonisation of polychaetes to intertidal biogenic habitats.Crossref | GoogleScholarGoogle Scholar |
Cole, V. J., Hutchings, P. A., and Ross, P. M. (2017). Predicting biodiversity changes due to loss of bioengineers from an intertidal landscape, a case study from Sydney Harbour. Australian Zoologist 39, 194–206.
| Predicting biodiversity changes due to loss of bioengineers from an intertidal landscape, a case study from Sydney Harbour.Crossref | GoogleScholarGoogle Scholar |
Cole, V. J., Chick, R. C., and Hutchings, P. A. (2018). A review of global fisheries for polychaete worms as a resource for recreational fishers: diversity, sustainability and research needs. Reviews in Fish Biology and Fisheries 28, 543–565.
| A review of global fisheries for polychaete worms as a resource for recreational fishers: diversity, sustainability and research needs.Crossref | GoogleScholarGoogle Scholar |
Coleman, M. A., Roughan, M., Macdonald, H. S., Connell, S. D., Gillanders, B. M., Kelaher, B. P., and Steinberg, P. D. (2011). Variation in the strength of continental boundary currents determines continent-wide connectivity in kelp. Journal of Ecology 99, 1026–1032.
| Variation in the strength of continental boundary currents determines continent-wide connectivity in kelp.Crossref | GoogleScholarGoogle Scholar |
Coleman, M. A., Feng, M., Roughan, M., Cetina-Heredia, P., and Connell, S. D. (2013). Temperate shelf water dispersal by Australian boundary currents: implications for population connectivity. Limnology and Oceanography: Fluids and Environments 3, 295–309.
Cowen, R. K., and Sponaugle, S. (2009). Larval dispersal and marine population connectivity. Annual Review of Marine Science 1, 443–466.
| Larval dispersal and marine population connectivity.Crossref | GoogleScholarGoogle Scholar | 21141044PubMed |
Cowen, R. K., Gawarkiewicz, G., Pineda, J., Thorrold, S. R., and Werner, F. E. (2007). Population connectivity in marine systems: an overview. Oceanography 20, 14–21.
| Population connectivity in marine systems: an overview.Crossref | GoogleScholarGoogle Scholar |
Danecek, P., Auton, A., Abecasis, G., Albers, C. A., Banks, E., DePristo, M. A., Handsaker, R. E., Lunter, G., Marth, G. T., Sherry, S. T., McVean, G., and Durbin, R. (2011). The variant call format and VCFtools. Bioinformatics 27, 2156–2158.
| The variant call format and VCFtools.Crossref | GoogleScholarGoogle Scholar | 21653522PubMed |
David, A. A., Matthee, C. A., Loveday, B. R., and Simon, C. A. (2016). Predicting the dispersal potential of an invasive polychaete pest along a complex coastal biome. Integrative and Comparative Biology 56, 600–610.
| Predicting the dispersal potential of an invasive polychaete pest along a complex coastal biome.Crossref | GoogleScholarGoogle Scholar | 27126982PubMed |
Dennis, A. B., and Hellberg, M. E. (2010). Ecological partitioning among parapatric cryptic species. Molecular Ecology 19, 3206–3225.
| Ecological partitioning among parapatric cryptic species.Crossref | GoogleScholarGoogle Scholar | 20618906PubMed |
Dibacco, C., Levin, L. A., and Sala E. (2006). Connectivity in marine ecosystems: the importance of larval and spore dispersal. In ‘Connectivity Conservation’. (Eds K. Crooks and M. Sanjayan.) pp. 184–212. (Cambridge University Press: Cambridge, UK.)
Dray, S., and Dufour, A. B. (2007). The ade4 package: implementing the duality diagram for ecologists. Journal of Statistical Software 22, 1–20.
| The ade4 package: implementing the duality diagram for ecologists.Crossref | GoogleScholarGoogle Scholar |
Elshire, R. J., Glaubitz, J. C., Sun, Q., Poland, J. A., Kawamoto, K., Buckler, E. S., and Mitchell, S. E. (2011). A robust, simple genotyping-by-sequencing (GBS) approach for high diversity species. PLoS One 6, e19379.
| A robust, simple genotyping-by-sequencing (GBS) approach for high diversity species.Crossref | GoogleScholarGoogle Scholar | 21573248PubMed |
Excoffier, L., Smouse, P. E., and Quattro, J. M. (1992). Analysis of molecular variance inferred from metric distances among DNA haplotypes: application to human mitochondrial DNA restriction data. Genetics 131, 479–491.
| 1644282PubMed |
Falush, D., Stephens, M., and Pritchard, J. K. (2003). Inference of population structure using multilocus genotype data: linked loci and correlated allele frequencies. Genetics 164, 1567–1587.
| 12930761PubMed |
Falush, D., Stephens, M., and Pritchard, J. K. (2007). Inference of population structure using multilocus genotype data: dominant markers and null alleles. Molecular Ecology Notes 7, 574–578.
| Inference of population structure using multilocus genotype data: dominant markers and null alleles.Crossref | GoogleScholarGoogle Scholar | 18784791PubMed |
Fauchald, K., and Jumars, P. A. (1979). The diet of worms: a study of polychaete feeding guilds. Oceanography and Marine Biology - An Annual Review 17, 193–284.
Fogarty, M. J., and Botsford, L. W. (2007). Population connectivity and spatial management of marine fisheries. Oceanography 20, 112–123.
| Population connectivity and spatial management of marine fisheries.Crossref | GoogleScholarGoogle Scholar |
Foll, M., and Gaggiotti, O. (2008). A genome-scan method to identify selected loci appropriate for both dominant and codominant markers: a Bayesian perspective. Genetics 180, 977–993.
| A genome-scan method to identify selected loci appropriate for both dominant and codominant markers: a Bayesian perspective.Crossref | GoogleScholarGoogle Scholar | 18780740PubMed |
Fraser, C. I., Morrison, A. K., Hogg, A. M. C., Macaya, E. C., van Sebille, E., Ryan, P. G., Padovan, A., Jack, C., Valdivia, N., and Waters, J. M. (2018a). Antarctica’s ecological isolation will be broken by storm-driven dispersal and warming. Nature Climate Change 8, 704–708.
| Antarctica’s ecological isolation will be broken by storm-driven dispersal and warming.Crossref | GoogleScholarGoogle Scholar |
Fraser, C. I., Davies, I. D., Bryant, D., and Waters, J. M. (2018b). How disturbance and dispersal influence intraspecific structure. Journal of Ecology 106, 1298–1306.
| How disturbance and dispersal influence intraspecific structure.Crossref | GoogleScholarGoogle Scholar |
Froukh, T., and Kochzius, M. (2007). Genetic population structure of the endemic fourline wrasse (Larabicus quadrilineatus) suggests limited larval dispersal distances in the Red Sea. Molecular Ecology 16, 1359–1367.
| Genetic population structure of the endemic fourline wrasse (Larabicus quadrilineatus) suggests limited larval dispersal distances in the Red Sea.Crossref | GoogleScholarGoogle Scholar | 17391261PubMed |
Giangrande, A., Licciano, M., and Musco, L. (2005). Polychaetes as environmental indicators revisited. Marine Pollution Bulletin 50, 1153–1162.
| Polychaetes as environmental indicators revisited.Crossref | GoogleScholarGoogle Scholar | 16197965PubMed |
Gogarten, S., Zheng, X., and Stilp, A. (2019). SeqVarTools: tools for variant data. R package version 1.25.0. https://github.com/smgogarten/SeqVarTools [verified 5 May 2020].
Gosselin, T. (2019). radiator: RADseq data exploration, manipulation and visualization using R. https://github.com/smgogarten/SeqVarTools [verified 5 May 2020].
Goudet, J. (2005). hierfstat, a package for R to compute and test hierarchical F‐statistics. Molecular Ecology Notes 5, 184–186.
| hierfstat, a package for R to compute and test hierarchical F‐statistics.Crossref | GoogleScholarGoogle Scholar |
Hsieh, H. L. (1994). Larval development and substrate preference at settlement in Pseudopolydora diopatra (Polychaeta: Spionidae). Invertebrate Reproduction & Development 25, 205–214.
| Larval development and substrate preference at settlement in Pseudopolydora diopatra (Polychaeta: Spionidae).Crossref | GoogleScholarGoogle Scholar |
Hubisz, M. J., Falush, D., Stephens, M., and Pritchard, J. K. (2009). Inferring weak population structure with the assistance of sample group information. Molecular Ecology Resources 9, 1322–1332.
| Inferring weak population structure with the assistance of sample group information.Crossref | GoogleScholarGoogle Scholar | 21564903PubMed |
Iacchei, M., Ben-Horin, T., Selkoe, K. A., Bird, C. E., García-Rodríguez, F. J., and Toonen, R. J. (2013). Combined analyses of kinship and FST suggest potential drivers of chaotic genetic patchiness in high gene-flow populations. Molecular Ecology 22, 3476–3494.
| Combined analyses of kinship and FST suggest potential drivers of chaotic genetic patchiness in high gene-flow populations.Crossref | GoogleScholarGoogle Scholar | 23802550PubMed |
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 | 18397895PubMed |
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 | 21926124PubMed |
Jumars, P. A., Dorgan, K. M., and Lindsay, S. M. (2015). Diet of worms emended: an update of polychaete feeding guilds. Annual Review of Marine Science 7, 497–520.
| Diet of worms emended: an update of polychaete feeding guilds.Crossref | GoogleScholarGoogle Scholar | 25251269PubMed |
Kamvar, Z. N., Tabima, J. F., and Grünwald, N. J. (2014). Poppr: an R package for genetic analysis of populations with clonal, partially clonal, and/or sexual reproduction. PeerJ 2, e281.
| Poppr: an R package for genetic analysis of populations with clonal, partially clonal, and/or sexual reproduction.Crossref | GoogleScholarGoogle Scholar | 24688859PubMed |
Kamvar, Z. N., Brooks, J. C., and Grünwald, N. J. (2015). Novel R tools for analysis of genome-wide population genetic data with emphasis on clonality. Frontiers in Genetics 6, 1–10.
| Novel R tools for analysis of genome-wide population genetic data with emphasis on clonality.Crossref | GoogleScholarGoogle Scholar |
Karsenti, E., Acinas, S. G., Bork, P., Bowler, C., de Vargas, C., Raes, J., Sullivan, M., Arendt, D., Benzoni, F., Claverie, J. M., Follows, M., Gorsky, G., Hingamp, P., Iudicone, D., Jaillon, O., Kandels-Lewis, S., Krzic, U., Not, F., Ogata, H., Pesant, S., Reynaud, E. G., Sardet, C., Sieracki, M. E., Speich, S., Velayoudon, D., Weissenbach, J., Wincker, P., Abergel, C., Arslan, D., Audic, S., Aury, J. M., Babic, N., Beaufort, L., Bittner, L., Boss, E., Boutte, C., Brum, J., Carmichael, M., Casotti, R., Chambouvet, A., Chang, P., Chica, C., Clerissi, C., Colin, S., Cornejo-Castillo, F. M., Da Silva, C., De Monte, S., Decelle, J., Desdevises, Y., Dimier, C., Dolan, J., Duhaime, M., Durrieu de Madron, X., d’Ortenzio, F., d’Ovidio, F., Ferrera, I., Garczarek, L., Garet-Delmas, M. J., Gasmi, S., Gasol, J. M., Grimsley, N., Heilig, R., Ignacio-Espinoza, J., Jamet, J. L., Karp-Boss, L., Katinka, M., Khalili, H., Kolber, Z., Le Bescot, N., Le Gofff, H., Lima-Mendez, G., Mahé, F., Mazzocchi, M. G., Montresor, M., Morin, P., Noel, B., Pedro’s-Alió, C., Pelletier, E., Perez, Y., Picheral, M., Piganeau, G., Poirot, O., Poulain, J., Poulton, N., Prejger, F., Prihoda, J., Probert, I., Rampal, J., Reverdin, G., Romac, S., Romagnan, J. B., Roullier, F., Rouviere, C., Samson, G., Santini, S., Sarmento, H., Sciandra, A., Solonenko, S., Stemmann, L., Subirana, L., Sunagawa, S., Tanaka, A., Testor, P., Thompson, A., Tichanné-Seltzer, V., Tirichine, L., Toulza, E., Tozzi, S., Veluchamy, A., and Zingone, A. (2011). A holistic approach to marine eco-systems biology. PLoS Biology 9, e1001177.
| A holistic approach to marine eco-systems biology.Crossref | GoogleScholarGoogle Scholar | 22028628PubMed |
Keane, J. P., and Neira, F. J. (2008). Larval fish assemblages along the south-eastern Australian shelf: linking mesoscale non-depth-discriminate structure and water masses. Fisheries Oceanography 17, 263–280.
| Larval fish assemblages along the south-eastern Australian shelf: linking mesoscale non-depth-discriminate structure and water masses.Crossref | GoogleScholarGoogle Scholar |
Kesäniemi, J. E., Geuverink, E., and Knott, K. E. (2012). Polymorphism in developmental mode and its effect on population genetic structure of a spionid polychaete, Pygospio elegans. Integrative and Comparative Biology 52, 181–196.
| Polymorphism in developmental mode and its effect on population genetic structure of a spionid polychaete, Pygospio elegans.Crossref | GoogleScholarGoogle Scholar | 22576815PubMed |
Kinlan, B. P., and Gaines, S. D. (2003). Propagule dispersal in marine and terrestrial environments: a community perspective. Ecology 84, 2007–2020.
| Propagule dispersal in marine and terrestrial environments: a community perspective.Crossref | GoogleScholarGoogle Scholar |
Knaus, B. J., and Grünwald, N. J. (2017). vcfr: a package to manipulate and visualize variant call format data in R. Molecular Ecology Resources 17, 44–53.
| vcfr: a package to manipulate and visualize variant call format data in R.Crossref | GoogleScholarGoogle Scholar | 27401132PubMed |
Levin, L. A. (2006). Recent progress in understanding larval dispersal: new directions and digressions. Integrative and Comparative Biology 46, 282–297.
| Recent progress in understanding larval dispersal: new directions and digressions.Crossref | GoogleScholarGoogle Scholar | 21672742PubMed |
Marko, P. B., Rogers-Bennett, L., and Dennis, A. B. (2007). MtDNA population structure and gene flow in lingcod (Ophiodon elongatus): limited connectivity despite long-lived pelagic larvae. Marine Biology 150, 1301–1311.
| MtDNA population structure and gene flow in lingcod (Ophiodon elongatus): limited connectivity despite long-lived pelagic larvae.Crossref | GoogleScholarGoogle Scholar |
McGaughran, A., Terauds, A., Convey, P., and Fraser, C. I. (2019). Genome-wide SNP data reveal improved evidence for Antarctic glacial refugia and dispersal of terrestrial invertebrates. Molecular Ecology 28, 4941–4957.
| Genome-wide SNP data reveal improved evidence for Antarctic glacial refugia and dispersal of terrestrial invertebrates.Crossref | GoogleScholarGoogle Scholar | 31596994PubMed |
Miller, K. J., Maynard, B. T., and Mundy, C. N. (2009). Genetic diversity and gene flow in collapsed and healthy abalone fisheries. Molecular Ecology 18, 200–211.
| Genetic diversity and gene flow in collapsed and healthy abalone fisheries.Crossref | GoogleScholarGoogle Scholar | 19076275PubMed |
Miller, K. J., Mundy, C. N., and Mayfield, S. (2014). Molecular genetics to inform spatial management in benthic invertebrate fisheries: a case study using the Australian greenlip abalone. Molecular Ecology 23, 4958–4975.
| Molecular genetics to inform spatial management in benthic invertebrate fisheries: a case study using the Australian greenlip abalone.Crossref | GoogleScholarGoogle Scholar | 25211183PubMed |
Montgomery, S. S. (1990). Movements of juvenile eastern king prawns, Penaeus plebejus, and identification of stock along the east coast of Australia. Fisheries Research 9, 189–208.
| Movements of juvenile eastern king prawns, Penaeus plebejus, and identification of stock along the east coast of Australia.Crossref | GoogleScholarGoogle Scholar |
Morris, G. P., Grabowski, P. P., and Borevitz, J. O. (2011). Genomic diversity in switchgrass (Panicum virgatum): from the continental scale to a dune landscape. Molecular Ecology 20, 4938–4952.
| Genomic diversity in switchgrass (Panicum virgatum): from the continental scale to a dune landscape.Crossref | GoogleScholarGoogle Scholar | 22060816PubMed |
Nei, M. (1987). ‘Molecular evolutionary genetics.’ (Columbia University Press: New York, USA.)
Nunes, F. L. D., Van Wormhoudt, A., Faroni-Perez, L., and Fournier, J. (2017). Phylogeography of the reef-building polychaetes of the genus Phragmatopoma in the western Atlantic Region. Journal of Biogeography 44, 1612–1625.
| Phylogeography of the reef-building polychaetes of the genus Phragmatopoma in the western Atlantic Region.Crossref | GoogleScholarGoogle Scholar |
Olsgard, F., and Somerfield, P. J. (2000). Surrogates in marine benthic investigations: which taxonomic unit to target? Journal of Aquatic Ecosystem Stress and Recovery 7, 25–42.
| Surrogates in marine benthic investigations: which taxonomic unit to target?Crossref | GoogleScholarGoogle Scholar |
Olsgard, F., Brattegard, T., and Holthe, T. (2003). Polychaetes as surrogates for marine biodiversity: lower taxonomic resolution and indicator groups. Biodiversity and Conservation 12, 1033–1049.
| Polychaetes as surrogates for marine biodiversity: lower taxonomic resolution and indicator groups.Crossref | GoogleScholarGoogle Scholar |
Paradis, E. (2010). pegas: an R package for population genetics with an integrated–modular approach. Bioinformatics 26, 419–420.
| pegas: an R package for population genetics with an integrated–modular approach.Crossref | GoogleScholarGoogle Scholar | 20080509PubMed |
Paxton, H. (1979). Taxonomy and aspects of the life history of Australian beachworms (Polychaeta: Onuphidae). Marine and Freshwater Research 30, 265–294.
| Taxonomy and aspects of the life history of Australian beachworms (Polychaeta: Onuphidae).Crossref | GoogleScholarGoogle Scholar |
Paxton, H. (1986). Generic revision and relationships of the family Onuphidae (Annelida: Polychaeta). Records of the Australian Museum 38, 1–74.
| Generic revision and relationships of the family Onuphidae (Annelida: Polychaeta).Crossref | GoogleScholarGoogle Scholar |
Pritchard, J. K., Stephens, M., and Donnelly, P. (2000). Inference of population structure using multilocus genotype data. Genetics 155, 945–959.
| 10835412PubMed |
Purcell, J. F. H., Cowen, R. K., Hughes, C. R., and Williams, D. A. (2006). Weak genetic structure indicates strong dispersal limits: a tale of two coral reef fish. Proceedings. Biological Sciences 273, 1483–1490.
| Weak genetic structure indicates strong dispersal limits: a tale of two coral reef fish.Crossref | GoogleScholarGoogle Scholar |
Riginos, C., Douglas, K. E., Jin, Y., Shanahan, D. F., and Treml, E. A. (2011). Effects of geography and life history traits on genetic differentiation in benthic marine fishes. Ecography 34, 566–575.
| Effects of geography and life history traits on genetic differentiation in benthic marine fishes.Crossref | GoogleScholarGoogle Scholar |
Roberts, C. M. (1997). Connectivity and management of Caribbean coral reefs. Science 278, 1454–1457.
| Connectivity and management of Caribbean coral reefs.Crossref | GoogleScholarGoogle Scholar | 9367956PubMed |
Ruello, N. V. (1975). Geographical distribution, growth and breeding migration of the eastern Australian king prawn Penaus plebejus Hess. Australian Journal of Marine and Freshwater Research 26, 343–354.
| Geographical distribution, growth and breeding migration of the eastern Australian king prawn Penaus plebejus Hess.Crossref | GoogleScholarGoogle Scholar |
Seixas, V. C., Paiva, P. C., and Russo, C. A de M. (2018). Comparative population genetics and demographic history of two polychaete species suggest that coastal lagoon populations evolve under alternate regimes of gene flow. Marine Biology 165, 179.
| Comparative population genetics and demographic history of two polychaete species suggest that coastal lagoon populations evolve under alternate regimes of gene flow.Crossref | GoogleScholarGoogle Scholar |
Shen, P. P., and Gu, J. D. (2015). Genetic population structure of polychaeta Neanthes glandicincta (Nereididae) of the Mai Po Inner Deep Bay Ramsar Site, Hong Kong. Ecotoxicology 24, 1557–1565.
| Genetic population structure of polychaeta Neanthes glandicincta (Nereididae) of the Mai Po Inner Deep Bay Ramsar Site, Hong Kong.Crossref | GoogleScholarGoogle Scholar | 25967938PubMed |
Shokri, M. R., Gladstone, W., and Kepert, A. (2009). Annelids, arthropods or molluscs are suitable as surrogate taxa for selecting conservation reserves in estuaries. Biodiversity and Conservation 18, 1117–1130.
Shulman, M. J., and Bermingham, E. (1995). Early life histories, ocean currents, and the population genetics of Caribbean reef fishes. Evolution 49, 897–910.
| Early life histories, ocean currents, and the population genetics of Caribbean reef fishes.Crossref | GoogleScholarGoogle Scholar | 28564869PubMed |
Smith, L. M., Hutchings, P., and Fraser, C. I. (2015). Molecular evidence supports coastal dispersal among estuaries for two benthic marine worm (Nephtyidae) species in southeastern Australia. Marine Biology 162, 1319–1327.
| Molecular evidence supports coastal dispersal among estuaries for two benthic marine worm (Nephtyidae) species in southeastern Australia.Crossref | GoogleScholarGoogle Scholar |
Sun, Y., Wong, E., Ahyong, S. T., Williamson, J. E., Pat, A., and Kupriyanova, E. K. (2018). Barcoding and multi-locus phylogeography of the globally distributed calcareous tubeworm genus Hydroides Gunnerus, 1768 (Annelida, Polychaeta, Serpulidae). Molecular Phylogenetics and Evolution 127, 732–745.
| Barcoding and multi-locus phylogeography of the globally distributed calcareous tubeworm genus Hydroides Gunnerus, 1768 (Annelida, Polychaeta, Serpulidae).Crossref | GoogleScholarGoogle Scholar | 29906604PubMed |
Temby, N., Miller, K., and Mundy, C. (2007). Evidence of genetic subdivision among populations of blacklip abalone (Haliotis rubra Leach) in Tasmania. Marine and Freshwater Research 58, 733–742.
| Evidence of genetic subdivision among populations of blacklip abalone (Haliotis rubra Leach) in Tasmania.Crossref | GoogleScholarGoogle Scholar |
Thiel, M., and Gutow, L. (2005a). The ecology of rafting in the marine environment. I. the floating substrata. Oceanography and Marine Biology - An Annual Review 42, 181–263.
| The ecology of rafting in the marine environment. I. the floating substrata.Crossref | GoogleScholarGoogle Scholar |
Thiel, M., and Gutow, L. (2005b). The ecology of rafting in the marine environment. II. the rafting organisms and community. Oceanography and Marine Biology - An Annual Review 43, 279–418.
| The ecology of rafting in the marine environment. II. the rafting organisms and community.Crossref | GoogleScholarGoogle Scholar |
Thorrold, S. R. (2006). Ocean ecology: don’t fence me in. Current Biology 16, R638–R640.
| Ocean ecology: don’t fence me in.Crossref | GoogleScholarGoogle Scholar | 16920611PubMed |
Waples, R., and Punt, A. (2008). Integrating genetic data into management of marine resources: how can we do it better? Fish and Fisheries 9, 423–449.
| Integrating genetic data into management of marine resources: how can we do it better?Crossref | GoogleScholarGoogle Scholar |
Waters, J. M., Fraser, C. I., and Hewitt, G. M. (2013). Founder takes all: density-dependent processes structure biodiversity. Trends in Ecology & Evolution 28, 78–85.
| Founder takes all: density-dependent processes structure biodiversity.Crossref | GoogleScholarGoogle Scholar |
Weir, B. S., and Cockerham, C. C. (1984). Estimating F‐statistics for the analysis of population structure. Evolution 38, 1358–1370.
| 28563791PubMed |
Wickham, H. (2016). ‘ggplot2: dlegant graphics for data analysis.’ (Springer-Verlag: New York, USA.)
Wickham, H., Hester, J., and Chang, W. (2019). Package ‘devtools’. https://github.com/r-lib/devtools [verified 5 May 2020].
Wilson, P. B., Streich, J. C., Murray, K. D., Eichten, S. R., Cheng, R., Aitken, N. C., Spokas, K., Warthmann, N., Gordon, S. P., Vogel, J. P., Borevitz, J. O., Liu, S., Bradford, K., Ezrati, S., Budak, H., Lopez, D., Catalan, P., Garvin, D., Vogel, J., Gordon, S., Hazen, S., and Mur, L. (2019). Global diversity of the Brachypodium species complex as a resource for genome-wide association studies demonstrated for agronomic traits in response to climate. Genetics 211, 317–331.
| Global diversity of the Brachypodium species complex as a resource for genome-wide association studies demonstrated for agronomic traits in response to climate.Crossref | GoogleScholarGoogle Scholar | 30446522PubMed |
Xuereb, A., Benestan, L., Normandeau, E., Curtis, J. M. R., Bernatchez, L., and Fortin, M.-J. (2018). Asymmetric oceanographic processes mediate connectivity and population genetic structure, as revealed by RADseq, in a highly dispersive marine invertebrate (Parastichopus californicus). Molecular Ecology 27, 2347–2364.
| Asymmetric oceanographic processes mediate connectivity and population genetic structure, as revealed by RADseq, in a highly dispersive marine invertebrate (Parastichopus californicus).Crossref | GoogleScholarGoogle Scholar | 29654703PubMed |
Zaâbi, S., Metais, I., Gillet, P., Afli, A., and Boumaiza, M. (2015). Preliminary study of population genetic diversity of Hyalinoecia tubicola (Polychaeta: Onuphidae) from the north east coast of Tunisia (western Mediterranean) using random amplified polymorphic DNA markers. Journal of Coastal Zone Management 18, 1–6.
| Preliminary study of population genetic diversity of Hyalinoecia tubicola (Polychaeta: Onuphidae) from the north east coast of Tunisia (western Mediterranean) using random amplified polymorphic DNA markers.Crossref | GoogleScholarGoogle Scholar |
