in

Highly restricted dispersal in habitat-forming seaweed may impede natural recovery of disturbed populations

  • 1.

    Wernberg, T. & Filbee-Dexter, K. Missing the marine forest for the trees. Mar. Ecol. Prog. Ser. 612, 209–215 (2019).

    ADS 
    Article 

    Google Scholar 

  • 2.

    Thompson, R. C., Wilson, B. J., Tobin, M. L., Hill, A. S. & Hawkins, S. J. Biologically generated habitat provision and diversity of rocky shore organisms at a hierarchy of spatial scales. J. Exp. Mar. Biol. Ecol. 202, 73–84 (1996).

    Article 

    Google Scholar 

  • 3.

    Christie, H., Jørgensen, N. M. & Norderhaug, K. M. Bushy or smooth, high or low; importance of habitat architecture and vertical position for distribution of fauna on kelp. J. Sea Res. 58, 198–208 (2007).

    ADS 
    Article 

    Google Scholar 

  • 4.

    Steneck, R. S. et al. Kelp forest ecosystems: Biodiversity, stability, resilience and future. Environ. Conserv. 29, 436–459 (2002).

    Article 

    Google Scholar 

  • 5.

    Strain, E. M. A., Thomson, R. J., Micheli, F., Mancuso, F. P. & Airoldi, L. Identifying the interacting roles of stressors in driving the global loss of canopy-forming to mat-forming algae in marine ecosystems. Glob. Change Biol. 20, 3300–3312 (2014).

    ADS 
    Article 

    Google Scholar 

  • 6.

    Mineur, F. et al. European seaweeds under pressure: Consequences for communities and ecosystem functioning. J. Sea Res. 98, 91–108 (2015).

    ADS 
    Article 

    Google Scholar 

  • 7.

    Krumhansl, K. A. et al. Global patterns of kelp forest change over the past half-century. PNAS 113, 13785–13790 (2016).

    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 

  • 8.

    Straub, S. C. et al. Resistance, extinction, and everything in between—The diverse responses of seaweeds to marine heatwaves. Front. Mar. Sci. 6, 763 (2019).

    Article 

    Google Scholar 

  • 9.

    Cheminée, A. et al. Nursery value of Cystoseira forests for Mediterranean rocky reef fishes. J. Exp. Mar. Biol. Ecol. 442, 70–79 (2013).

    Article 

    Google Scholar 

  • 10.

    Piazzi, L. et al. Biodiversity in canopy-forming algae: Structure and spatial variability of the Mediterranean Cystoseira assemblages. Estuar. Coast. Shelf Sci. 207, 132–141 (2018).

    ADS 
    Article 

    Google Scholar 

  • 11.

    Thibaut, T., Pinedo, S., Torras, X. & Ballesteros, E. Long-term decline of the populations of Fucales (Cystoseira spp. and Sargassum spp.) in the Albères coast (France, North-western Mediterranean). Mar. Pollut. Bull. 50, 1472–1489 (2005).

    CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 

  • 12.

    Gianni, F. et al. Conservation and restoration of marine forests in the Mediterranean Sea and the potential role of marine protected areas. Adv. Oceanogr. Limnol. 4, 83–101 (2013).

    Article 

    Google Scholar 

  • 13.

    Blanfuné, A., Boudouresque, C. F., Verlaque, M. & Thibaut, T. The fate of Cystoseira crinita, a forest-forming Fucale (Phaeophyceae, Stramenopiles), in France (North Western Mediterranean Sea). Estuar. Coast. Shelf Sci. 181, 196–208 (2016).

    ADS 
    Article 

    Google Scholar 

  • 14.

    Gubbay, S. et al. European Red List of Habitats. Part 1. Marine habitats. Luxembourg: Publications Office of the European Union (2016).

  • 15.

    Perkol-Finkel, S., Ferrario, F., Nicotera, V. & Airoldi, L. Conservation challenges in urban seascapes: Promoting the growth of threatened species on coastal infrastructures. J. Appl. Ecol. 49, 1457–1466 (2012).

    Article 

    Google Scholar 

  • 16.

    Falace, A., Kaleb, S., Fuente, G. D. L., Asnaghi, V. & Chiantore, M. Ex situ cultivation protocol for Cystoseira amentacea var. stricta (Fucales, Phaeophyceae) from a restoration perspective. PLoS ONE 13, e0193011 (2018).

    PubMed 
    PubMed Central 
    Article 
    CAS 

    Google Scholar 

  • 17.

    Gianni, F., Bartolini, F., Airoldi, L. & Mangialajo, L. Reduction of herbivorous fish pressure can facilitate focal algal species forestation on artificial structures. Mar. Environ. Res. 138, 102–109 (2018).

    CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 

  • 18.

    Gianni, F. et al. Optimizing canopy-forming algae conservation and restoration with a new herbivorous fish deterrent device. Restor. Ecol. 28, 750–756 (2020).

    Article 

    Google Scholar 

  • 19.

    Verdura, J., Sales, M., Ballesteros, E., Cefalì, M. E. & Cebrian, E. Restoration of a canopy-forming alga based on recruitment enhancement: Methods and long-term success assessment. Front. Plant Sci. 9, 1832 (2018).

    PubMed 
    PubMed Central 
    Article 

    Google Scholar 

  • 20.

    Fuente, G. D. L., Chiantore, M., Asnaghi, V., Kaleb, S. & Falace, A. First ex situ outplanting of the habitat-forming seaweed Cystoseira amentacea var. stricta from a restoration perspective. PeerJ 7, e7290 (2019).

    Article 

    Google Scholar 

  • 21.

    Tamburello, L. et al. Are we ready for scaling up restoration actions? An insight from Mediterranean macroalgal canopies. PLoS ONE 14, e0224477 (2019).

    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 

  • 22.

    Medrano, A. et al. From marine deserts to algal beds: Treptacantha elegans revegetation to reverse stable degraded ecosystems inside and outside a No-Take marine reserve. Restor. Ecol. 28, 632–644 (2020).

    Article 

    Google Scholar 

  • 23.

    Chryssovergis, F. & Panayotidis, P. Évolution des peuplements macrophytobenthiques le long d’un gradient d’eutrophisation. Oceanol. Acta 18, 649–658 (1995).

    Google Scholar 

  • 24.

    Sales, M., Cebrian, E., Tomas, F. & Ballesteros, E. Pollution impacts and recovery potential in three species of the genus Cystoseira (Fucales, Heterokontophyta). Estuar. Coast. Shelf Sci. 92, 347–357 (2011).

    ADS 
    CAS 
    Article 

    Google Scholar 

  • 25.

    Díez, I., Santolaria, A., Secilla, A. & Gorostiaga, J. M. Recovery stages over long-term monitoring of the intertidal vegetation in the ‘Abra de Bilbao’ area and on the adjacent coast (N. Spain). Eur. J. Phycol. 44, 1–14 (2009).

    Article 

    Google Scholar 

  • 26.

    Bringloe, T. T. et al. Phylogeny and evolution of the brown algae. Crit. Rev. Plant Sci. 39, 281–321 (2020).

    CAS 
    Article 

    Google Scholar 

  • 27.

    Guern, M. Embryologie de quelques espèces du genre Cystoseira Agardh 1821 (FUCALES). Vie et Milieu 649–680 (1962).

  • 28.

    Dudgeon, S., Kübler, J. E., Wright, W. A., Vadas, R. L. & Petraitis, P. S. Natural variability in zygote dispersal of Ascophyllum nodosum at small spatial scales. Funct. Ecol. 15, 595–604 (2001).

    Article 

    Google Scholar 

  • 29.

    Mangialajo, L. et al. Zonation patterns and interspecific relationships of fucoids in microtidal environments. J. Exp. Mar. Biol. Ecol. 412, 72–80 (2012).

    Article 

    Google Scholar 

  • 30.

    Capdevila, P. et al. Recruitment patterns in the Mediterranean deep-water alga Cystoseira zosteroides. Mar. Biol. 162, 1165–1174 (2015).

    CAS 
    Article 

    Google Scholar 

  • 31.

    Assis, J. et al. A fine-tuned global distribution dataset of marine forests. Sci. Data 7, 119 (2020).

    PubMed 
    PubMed Central 
    Article 

    Google Scholar 

  • 32.

    Fabbrizzi, E. et al. Modeling macroalgal forest distribution at Mediterranean scale: Present status, drivers of changes and insights for conservation and management. Front. Mar. Sci. 7, 20 (2020).

    Article 

    Google Scholar 

  • 33.

    Benedetti-Cecchi, L., Tamburello, L., Maggi, E. & Bulleri, F. Experimental perturbations modify the performance of early warning indicators of regime shift. Curr. Biol. 25, 1867–1872 (2015).

    CAS 
    PubMed 
    Article 

    Google Scholar 

  • 34.

    Bulleri, F., Benedetti-Cecchi, L., Ceccherelli, G. & Tamburello, L. A few is enough: A low cover of a non-native seaweed reduces the resilience of Mediterranean macroalgal stands to disturbances of varying extent. Biolical Invasions 19, 2291–2305 (2017).

    Article 

    Google Scholar 

  • 35.

    Rindi, L., Bello, M. D., Dai, L., Gore, J. & Benedetti-Cecchi, L. Direct observation of increasing recovery length before collapse of a marine benthic ecosystem. Nat. Ecol. Evol. 1, 1–7 (2017).

    Article 

    Google Scholar 

  • 36.

    Draisma, S. G. A., Ballesteros, E., Rousseau, F. & Thibaut, T. DNA sequence data demonstrate the polyphyly of the genus Cystoseira and other Sargassaceae genera (Phaeophyceae). J. Phycol. 46, 1329–1345 (2010).

    Article 

    Google Scholar 

  • 37.

    Bruno de Sousa, C. et al. Improved phylogeny of brown algae Cystoseira (Fucales) from the Atlantic-Mediterranean region based on mitochondrial sequences. PLoS ONE 14, e0210143 (2019).

    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 

  • 38.

    Jódar-Pérez, A. B., Terradas-Fernández, M., López-Moya, F., Asensio-Berbegal, L. & López-Llorca, L. V. Multidisciplinary analysis of Cystoseira sensu lato (SE Spain) suggest a complex colonization of the Mediterranean. J. Mar. Sci. Eng. 8, 961 (2020).

    Article 

    Google Scholar 

  • 39.

    Hughes, A. R. & Stachowicz, J. J. Genetic diversity enhances the resistance of a seagrass ecosystem to disturbance. PNAS 101, 8998–9002 (2004).

    ADS 
    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 

  • 40.

    Reusch, T. B. H. & Hughes, A. R. The emerging role of genetic diversity for ecosystem functioning: Estuarine macrophytes as models. Estuaries and Coasts J ERF 29, 159–164 (2006).

    Article 

    Google Scholar 

  • 41.

    Reusch, T. B. H., Ehlers, A., Hämmerli, A. & Worm, B. Ecosystem recovery after climatic extremes enhanced by genotypic diversity. PNAS 102, 2826–2831 (2005).

    ADS 
    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 

  • 42.

    Ehlers, A., Worm, B. & Reusch, T. B. H. Importance of genetic diversity in eelgrass Zostera marina for its resilience to global warming. Mar. Ecol. Prog. Ser. 355, 1–7 (2008).

    ADS 
    Article 

    Google Scholar 

  • 43.

    Hughes, A. R., Inouye, B. D., Johnson, M. T. J., Underwood, N. & Vellend, M. Ecological consequences of genetic diversity. Ecol. Lett. 11, 609–623 (2008).

    PubMed 
    Article 

    Google Scholar 

  • 44.

    Frankham, R., Ballou, J. D. & Briscoe, D. A. Introduction to Conservation Genetics (Cambridge University Press, 2002) https://doi.org/10.1017/CBO9780511808999
    .

    Book 

    Google Scholar 

  • 45.

    Cowen, R., Gawarkiewicz, G., Pineda, J., Thorrold, S. & Werner, F. Population connectivity in marine systems: An overview. Oceanography 20, 14–21 (2007).

    Article 

    Google Scholar 

  • 46.

    Mayr, E. Animal Species and Evolution. Animal Species and Evolution (Harvard University Press, 2013).

    Google Scholar 

  • 47.

    Kimura, M. The Neutral Theory of Molecular Evolution (Cambridge University Press, 1983) https://doi.org/10.1017/CBO9780511623486
    .

    Book 

    Google Scholar 

  • 48.

    Frankham, R. Conservation genetics. Annu. Rev. Genet. 29, 305–327 (1995).

    CAS 
    PubMed 
    Article 

    Google Scholar 

  • 49.

    Lacy, R. C. Loss of genetic diversity from managed populations: Interacting effects of drift, mutation, immigration, selection, and population subdivision. Conserv. Biol. 1, 143–158 (1987).

    Article 

    Google Scholar 

  • 50.

    Frankham, R. et al. Genetic Management of Fragmented Animal and Plant Populations (Oxford University Press, 2017).

    Book 

    Google Scholar 

  • 51.

    Planes, S., Jones, G. P. & Thorrold, S. R. Larval dispersal connects fish populations in a network of marine protected areas. PNAS https://doi.org/10.1073/pnas.0808007106 (2009).

    Article 
    PubMed 
    PubMed Central 

    Google Scholar 

  • 52.

    Pineda, J., Hare, J. A. & Sponaugle, S. Larval transport and dispersal in the coastal ocean and consequences for population connectivity. Oceanography 20, 22–39 (2007).

    Article 

    Google Scholar 

  • 53.

    Caughley, G. Directions in conservation biology. J. Anim. Ecol. 63, 215–244 (1994).

    Article 

    Google Scholar 

  • 54.

    Buonomo, R. et al. Predicted extinction of unique genetic diversity in marine forests of Cystoseira spp. Mar. Environ. Res. 138, 119–128 (2018).

    CAS 
    PubMed 
    Article 

    Google Scholar 

  • 55.

    Buonomo, R. et al. Habitat continuity and stepping-stone oceanographic distances explain population genetic connectivity of the brown alga Cystoseira amentacea. Mol. Ecol. 26, 766–780 (2017).

    PubMed 
    Article 

    Google Scholar 

  • 56.

    Bermejo, R. et al. Marine forests of the Mediterranean-Atlantic Cystoseira tamariscifolia complex show a southern Iberian genetic hotspot and no reproductive isolation in parapatry. Sci. Rep. 8, 10427 (2018).

    ADS 
    PubMed 
    PubMed Central 
    Article 
    CAS 

    Google Scholar 

  • 57.

    Engelen, A. H. et al. A population genetics toolbox for the threatened canopy-forming brown seaweeds Cystoseira tamariscifolia and C. amentacea (Fucales, Sargassaceae). J. Appl. Phycol. 29, 627–629 (2017).

    Article 

    Google Scholar 

  • 58.

    Thibaut, T. et al. Connectivity of populations of the seaweed Cystoseira amentacea within the Bay of Marseille (Mediterranean Sea): Genetic structure and hydrodynamic connections. crya 37, 233–255 (2016).

    Article 

    Google Scholar 

  • 59.

    Guiry, M.D. & Guiry, G.M. AlgaeBase. World-wide electronic publication (National University of Ireland, 2021) http://www.algaebase.org (Accessed 21 Jan 2021).

  • 60.

    Sales, M. & Ballesteros, E. Shallow Cystoseira (Fucales: Ochrophyta) assemblages thriving in sheltered areas from Menorca (NW Mediterranean): Relationships with environmental factors and anthropogenic pressures. Estuar. Coast. Shelf Sci. 84, 476–482 (2009).

    ADS 
    CAS 
    Article 

    Google Scholar 

  • 61.

    Robvieux, P. et al. First characterization of eight polymorphic microsatellites for Cystoseira amentacea var. stricta (Fucales, Sargassaceae). Conserv. Genet. Resour. 4, 923–925 (2012).

    Article 

    Google Scholar 

  • 62.

    Sadogurska, S. S., Neiva, J., Falace, A., Serrão, E. A. & Israel, Á. The genus Cystoseira s.l. (Ochrophyta, Fucales, Sargassaceae) in the Black Sea: Morphological variability and molecular taxonomy of Gongolaria barbata and endemic Ericaria crinita f. bosphorica comb. nov. Phytotaxa 480, 1–21 (2021).

    Article 

    Google Scholar 

  • 63.

    Bologa, A. S. & Sava, D. Progressive decline and present trend of Romanian Black Sea macroalgal flora. Cercetari Mar. 36, 31–60 (2006).

    Google Scholar 

  • 64.

    Irving, A. D., Balata, D., Colosio, F., Ferrando, G. A. & Airoldi, L. Light, sediment, temperature, and the early life-history of the habitat-forming alga Cystoseira barbata. Mar. Biol. 156, 1223–1231 (2009).

    Article 

    Google Scholar 

  • 65.

    Allendorf, F. W. Genetics and the conservation of natural populations: Allozymes to genomes. Mol. Ecol. 26, 420–430 (2017).

    CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 

  • 66.

    Ellegren, H. Microsatellites: Simple sequences with complex evolution. Nat. Rev. Genet. 5, 435–445 (2004).

    CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 

  • 67.

    De Meeûs, T. et al. Deceptive combined effects of short allele dominance and stuttering: An example with Ixodes scapularis, the main vector of Lyme disease in the USA. bioRxiv https://doi.org/10.1101/622373 (2019).

    Article 

    Google Scholar 

  • 68.

    De Meeûs, T. Revisiting FIS, FST, Wahlund effects, and null alleles. J. Hered. 109, 446–456 (2018).

    PubMed 
    Article 
    PubMed Central 

    Google Scholar 

  • 69.

    Evanno, G., Regnaut, S. & Goudet, J. Detecting the number of clusters of individuals using the software STRUCTURE: A simulation study. Mol. Ecol. 14, 2611–2620 (2005).

    CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 

  • 70.

    Selkoe, K. A. & Toonen, R. J. Microsatellites for ecologists: A practical guide to using and evaluating microsatellite markers. Ecol. Lett. 9, 615–629 (2006).

    PubMed 
    Article 
    PubMed Central 

    Google Scholar 

  • 71.

    Manangwa, O. et al. Detecting Wahlund effects together with amplification problems: Cryptic species, null alleles and short allele dominance in Glossina pallidipes populations from Tanzania. Mol. Ecol. Resour. 19, 757–772 (2019).

    PubMed 
    Article 
    PubMed Central 

    Google Scholar 

  • 72.

    Chapuis, M.-P. & Estoup, A. Microsatellite null alleles and estimation of population differentiation. Mol. Biol. Evol. 24, 621–631 (2007).

    CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 

  • 73.

    Engel, C. R., Brawley, S. H., Edwards, K. J. & Serrão, E. Isolation and cross-species amplification of microsatellite loci from the fucoid seaweeds Fucus vesiculosus, F. serratus and Ascophyllum nodosum (Heterokontophyta, Fucaceae). Mol. Ecol. Notes 3, 180–182 (2003).

    CAS 
    Article 

    Google Scholar 

  • 74.

    Paulino, C. et al. Characterization of 12 polymorphic microsatellite markers in the sugar kelp Saccharina latissima. J. Appl. Phycol. 28, 3071–3074 (2016).

    Article 

    Google Scholar 

  • 75.

    Coleman, M. A., Dolman, G., Kelaher, B. P. & Steinberg, P. D. Characterisation of microsatellite loci in the subtidal habitat-forming alga, Phyllospora comosa (Phaeophyceae, Fucales). Conserv. Genet. 9, 1015–1017 (2008).

    CAS 
    Article 

    Google Scholar 

  • 76.

    Coleman, M. A. & Brawley, S. H. Are life history characteristics good predictors of genetic diversity and structure? A case study of the intertidal alga Fucus spiralis (heterokontophyta; Phaeophyceae). J. Phycol. 41, 753–762 (2005).

    Article 

    Google Scholar 

  • 77.

    Coleman, M. A. & Brawley, S. H. Spatial and temporal variability in dispersal and population genetic structure of a rockpool alga. Mar. Ecol. Prog. Ser. 300, 63–77 (2005).

    ADS 
    Article 

    Google Scholar 

  • 78.

    Engel, C. R., Daguin, C. & Serrão, E. A. Genetic entities and mating system in hermaphroditic Fucus spiralis and its close dioecious relative F. vesiculosus (Fucaceae, Phaeophyceae). Mol. Ecol. 14, 2033–2046 (2005).

    CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 

  • 79.

    Medrano, A. et al. Ecological traits, genetic diversity and regional distribution of the macroalga Treptacantha elegans along the Catalan coast (NW Mediterranean Sea). Sci. Rep. 10, 19219 (2020).

    ADS 
    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 

  • 80.

    Engelen, A. H. et al. Periodicity of propagule expulsion and settlement in the competing native and invasive brown seaweeds, Cystoseira humilis and Sargassum muticum (Phaeophyta). Eur. J. Phycol. 43, 275–282 (2008).

    Article 

    Google Scholar 

  • 81.

    Assis, J., Serrão, E. A., Claro, B., Perrin, C. & Pearson, G. A. Climate-driven range shifts explain the distribution of extant gene pools and predict future loss of unique lineages in a marine brown alga. Mol. Ecol. 23, 2797–2810 (2014).

    CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 

  • 82.

    Neiva, J. et al. Genes left behind: Climate change threatens cryptic genetic diversity in the canopy-forming seaweed Bifurcaria bifurcata. PLoS ONE 10, e0131530 (2015).

    PubMed 
    PubMed Central 
    Article 
    CAS 

    Google Scholar 

  • 83.

    Coleman, M. A. & Kelaher, B. P. Connectivity among fragmented populations of a habitat-forming alga, Phyllospora comosa (Phaeophyceae, Fucales) on an urbanised coast. Mar. Ecol. Prog. Ser. 381, 63–70 (2009).

    ADS 
    Article 

    Google Scholar 

  • 84.

    Boissin, E. et al. Chaotic genetic structure and past demographic expansion of the invasive gastropod Tritia neritea in its native range, the Mediterranean Sea. Sci. Rep. 10, 21624 (2020).

    ADS 
    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 

  • 85.

    Olsen, J. L. et al. North Atlantic phylogeography and large-scale population differentiation of the seagrass Zostera marina L. Mol. Ecol. 13, 1923–1941 (2004).

    CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 

  • 86.

    Peijnenburg, K. T. C. A., Breeuwer, J. A. J., Pierrot-Bults, A. C. & Menken, S. B. J. Phylogeography of the planktonic chaetognath Sagitta setosa reveals isolation in European Seas. Evolution 58, 1472–1487 (2004).

    PubMed 
    Article 
    PubMed Central 

    Google Scholar 

  • 87.

    Luttikhuizen, P. C., Campos, J., van Bleijswijk, J., Peijnenburg, K. T. C. A. & van der Veer, H. W. Phylogeography of the common shrimp, Crangon crangon (L.) across its distribution range. Mol. Phylogenet. Evol. 46, 1015–1030 (2008).

    CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 

  • 88.

    Wilson, A. B. & Eigenmann Veraguth, I. The impact of Pleistocene glaciation across the range of a widespread European coastal species. Mol. Ecol. 19, 4535–4553 (2010).

    CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 

  • 89.

    Riquet, F. et al. Parallel pattern of differentiation at a genomic island shared between clinal and mosaic hybrid zones in a complex of cryptic seahorse lineages. Evolution 73, 817–835 (2019).

    PubMed 
    Article 
    PubMed Central 

    Google Scholar 

  • 90.

    Hewitt, G. M. Hybrid zones-natural laboratories for evolutionary studies. Trends Ecol. Evol. 3, 158–167 (1988).

    CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 

  • 91.

    Johannesson, K., Le Moan, A., Perini, S. & André, C. A Darwinian laboratory of multiple contact zones. Trends Ecol. Evol. https://doi.org/10.1016/j.tree.2020.07.015 (2020).

    Article 
    PubMed 
    PubMed Central 

    Google Scholar 

  • 92.

    McCoy, S. J., Krueger-Hadfield, S. A. & Mieszkowska, N. Evolutionary phycology: Toward a macroalgal species conceptual framework. J. Phycol. 56, 1404–1413 (2020).

    PubMed 
    PubMed Central 
    Article 

    Google Scholar 

  • 93.

    Neiva, J., Pearson, G. A., Valero, M. & Serrão, E. A. Fine-scale genetic breaks driven by historical range dynamics and ongoing density-barrier effects in the estuarine seaweed Fucus ceranoides L. BMC Evol. Biol. 12, 78 (2012).

    PubMed 
    PubMed Central 
    Article 

    Google Scholar 

  • 94.

    Whitlock, M. C. & McCauley, D. E. Indirect measures of gene flow and migration: FST ≠1/(4 Nm + 1). Heredity 82, 117–125 (1999).

    PubMed 
    Article 
    PubMed Central 

    Google Scholar 

  • 95.

    Lowe, W. H. & Allendorf, F. W. What can genetics tell us about population connectivity?. Mol. Ecol. 19, 3038–3051 (2010).

    PubMed 
    Article 
    PubMed Central 

    Google Scholar 

  • 96.

    Durrant, H. M. S. et al. Implications of macroalgal isolation by distance for networks of marine protected areas. Conserv. Biol. 28, 438–445 (2014).

    PubMed 
    Article 
    PubMed Central 

    Google Scholar 

  • 97.

    Engelen, A., Olsen, J., Breeman, A. & Stam, W. Genetic differentiation in Sargassum polyceratium (Fucales: Phaeophyceae) around the island of Curaçao (Netherlands Antilles). Mar. Biol. 139, 267–277 (2001).

    CAS 
    Article 

    Google Scholar 

  • 98.

    Billot, C., Engel, C. R., Rousvoal, S., Kloareg, B. & Valero, M. Current patterns, habitat discontinuities and population genetic structure: The case of the kelp Laminaria digitata in the English Channel. Mar. Ecol. Prog. Ser. 253, 111–121 (2003).

    ADS 
    Article 

    Google Scholar 

  • 99.

    Tatarenkov, A., Jönsson, R. B., Kautsky, L. & Johannesson, K. Genetic structure in populations of Fucus vesiculosus (phaeophyceae) over spatial scales from 10 m to 800 km. J. Phycol. 43, 675–685 (2007).

    CAS 
    Article 

    Google Scholar 

  • 100.

    Susini, M.-L., Thibaut, T., Meinesz, A. & Forcioli, D. A preliminary study of genetic diversity in Cystoseira amentacea (C. Agardh) Bory var. stricta Montagne (Fucales, Phaeophyceae) using random amplified polymorphic DNA. Phycologia 46, 605–611 (2007).

    Article 

    Google Scholar 

  • 101.

    Korotenko, K., Bowman, M. & Dietrich, D. High-resolution numerical model for predicting the transport and dispersal of oil spilled in the Black Sea. Terrest. Atmos. Oceanic Sci. J. 21, 123–136 (2010).

    Article 

    Google Scholar 

  • 102.

    Barale, V., Schiller, C., Tacchi, R. & Marechal, C. Trends and interactions of physical and bio-geo-chemical features in the Adriatic Sea as derived from satellite observations. Sci. Total Environ. 353, 68–81 (2005).

    ADS 
    CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 

  • 103.

    Hauser, L. & Carvalho, G. R. Paradigm shifts in marine fisheries genetics: Ugly hypotheses slain by beautiful facts. Fish Fish. 9, 333–362 (2008).

    Article 

    Google Scholar 

  • 104.

    Orellana, S., Hernández, M. & Sansón, M. Diversity of Cystoseira sensu lato (Fucales, Phaeophyceae) in the eastern Atlantic and Mediterranean based on morphological and DNA evidence, including Carpodesmia gen. emend. and Treptacantha gen. emend. Eur. J. Phycol. 54, 447–465 (2019).

    CAS 
    Article 

    Google Scholar 

  • 105.

    Richard, B., A. & Wilks, A., R. Maps in S. AT&T Bell Laboratories Statistics Research Report [93.2] (1993).

  • 106.

    Richard, B., A. & Wilks, A., R. Constructing a Geographical Database. AT&T Bell Lab-oratories Statistics Research Report [95.2] (1995).

  • 107.

    R Core Team. R: A Language and Environment for Statistical Computing https://www.R-project.org/ (R Foundation for Statistical Computing, 2017).

  • 108.

    Holleley, C. E. & Geerts, P. G. Multiplex Manager 1.0: A cross-platform computer program that plans and optimizes multiplex PCR. Biotechniques 46, 511–517 (2009).

    CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 

  • 109.

    Peakall, R. & Smouse, P. E. genalex 6: Genetic analysis in Excel. Population genetic software for teaching and research. Mol. Ecol. Notes 6, 288–295 (2006).

    Article 

    Google Scholar 

  • 110.

    Goudet, J. Fstat (Version 1.2): A computer program to calculate F-Statistics. J. Hered. 86, 485–486 (1995).

    Article 

    Google Scholar 

  • 111.

    De Meeûs, T., Guégan, J.-F. & Teriokhin, A. T. MultiTest V.1.2, a program to binomially combine independent tests and performance comparison with other related methods on proportional data. BMC Bioinform. 10, 443 (2009).

    Article 
    CAS 

    Google Scholar 

  • 112.

    Benjamini, Y. & Hochberg, Y. Controlling the False Discovery Rate: A practical and powerful approach to multiple testing. J. R. Stat. Soc. Ser. B Methodol. 57, 289–300 (1995).

    MathSciNet 
    MATH 

    Google Scholar 

  • 113.

    Oosterhout, C. V., Weetman, D. & Hutchinson, W. F. Estimation and adjustment of microsatellite null alleles in nonequilibrium populations. Mol. Ecol. Notes 6, 255–256 (2006).

    Article 

    Google Scholar 

  • 114.

    Petit, R. J., Mousadik, A. E. & Pons, O. Identifying populations for conservation on the basis of genetic markers. Conserv. Biol. 12, 844–855 (1998).

    Article 

    Google Scholar 

  • 115.

    El Mousadik, A. & Petit, R. J. High level of genetic differentiation for allelic richness among populations of the argan tree [Argania spinosa (L.) Skeels] endemic to Morocco. Theor. Appl. Genet. 92, 832–839 (1996).

    PubMed 
    Article 
    PubMed Central 

    Google Scholar 

  • 116.

    Raymond, M. & Rousset, F. GENEPOP (Version 1.2): Population genetics Software for exact tests and ecumenicism. J. Hered. 86, 248–249 (1995).

    Article 

    Google Scholar 

  • 117.

    Szulkin, M., Bierne, N. & David, P. Heterozygosity-fitness correlations: A time for reappraisal. Evolution 64, 1202–1217 (2010).

    PubMed 
    PubMed Central 

    Google Scholar 

  • 118.

    David, P., Pujol, B., Viard, F., Castella, V. & Goudet, J. Reliable selfing rate estimates from imperfect population genetic data. Mol. Ecol. 16, 2474–2487 (2007).

    CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 

  • 119.

    Wright, S. The interpretation of population structure by F-statistics with special regard to systems of mating. Evolution 19, 395–420 (1965).

    Article 

    Google Scholar 

  • 120.

    Weir, B. S. & Cockerham, C. C. Estimating F-statistics for the analysis of population structure. Evolution 38, 1358–1370 (1984).

    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • 121.

    Pritchard, J. K., Stephens, M. & Donnelly, P. Inference of population structure using multilocus genotype data. Genetics 155, 945–959 (2000).

    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 

  • 122.

    Falush, D., Stephens, M. & Pritchard, J. K. Inference of population structure using multilocus genotype data: Linked loci and correlated allele frequencies. Genetics 164, 1567–1587 (2003).

    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 

  • 123.

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

    CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 

  • 124.

    Jakobsson, M. & Rosenberg, N. A. Clumpp: A cluster matching and permutation program for dealing with label switching and multimodality in analysis of population structure. Bioinformatics 23, 1801–1806 (2007).

    CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 

  • 125.

    Goudet, J. hierfstat, a package for r to compute and test hierarchical F-statistics. Mol. Ecol. Notes 5, 184–186 (2005).

    Article 

    Google Scholar 

  • 126.

    Séré, M., Thévenon, S., Belem, A. M. G. & De Meeûs, T. Comparison of different genetic distances to test isolation by distance between populations. Heredity 119, 55–63 (2017).

    PubMed 
    PubMed Central 
    Article 

    Google Scholar 

  • 127.

    Rousset, F. & Raymond, M. Statistical analyses of population genetic data: New tools, old concepts. Trends Ecol. Evol. 12, 313–317 (1997).

    CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 

  • 128.

    Hijmans, R. J. Geosphere: Spherical Trigonometry. https://CRAN.R-project.org/package=geosphere. R package version 1.5–5. (2016).

  • 129.

    Korotenko, K. A. Effects of mesoscale eddies on behavior of an oil spill resulting from an accidental deepwater blowout in the Black Sea: An assessment of the environmental impacts. PeerJ 6, e5448 (2018).

    PubMed 
    PubMed Central 
    Article 
    CAS 

    Google Scholar 

  • 130.

    López-Márquez, V. et al. Seascape genetics and connectivity modelling for an endangered Mediterranean coral in the northern Ionian and Adriatic seas. Landsc. Ecol. 34, 2649–2668 (2019).

    Article 

    Google Scholar 

  • 131.

    Rousset, F. Genetic differentiation and estimation of gene flow from F-statistics under isolation by distance. Genetics 145, 1219–1228 (1997).

    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 

  • 132.

    Watts, P. C. et al. Compatible genetic and ecological estimates of dispersal rates in insect (Coenagrion mercuriale: Odonata: Zygoptera) populations: Analysis of ‘neighbourhood size’ using a more precise estimator. Mol. Ecol. 16, 737–751 (2007).

    PubMed 
    Article 
    PubMed Central 

    Google Scholar 

  • 133.

    Hill, W. G. Estimation of effective population size from data on linkage disequilibrium. Genet. Res. 38, 209–216 (1981).

    Article 

    Google Scholar 

  • 134.

    Waples, R. S. Seed banks, salmon, and sleeping genes: Effective population size in semelparous, age-structured species with fluctuating abundance. Am. Nat. 167, 118–135 (2006).

    PubMed 
    Article 
    PubMed Central 

    Google Scholar 

  • 135.

    Waples, R. S. & Do, C. ldne: A program for estimating effective population size from data on linkage disequilibrium. Mol. Ecol. Resour. 8, 753–756 (2008).

    PubMed 
    Article 

    Google Scholar 

  • 136.

    Do, C. et al. NeEstimator v2: Re-implementation of software for the estimation of contemporary effective population size (Ne) from genetic data. Mol. Ecol. Resour. 14, 209–214 (2014).

    CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 

  • 137.

    Cavalli-Sforza, L. L., & Edwards, A. W. F. Phylogenetic analysis: Model and estimation procedures. Am. J. Hum. Genet. 19, 233–257 (1967).

    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 


  • Source: Ecology - nature.com

    Smarter regulation of global shipping emissions could improve air quality and health outcomes

    Resource–diversity relationships in bacterial communities reflect the network structure of microbial metabolism