Comparative population genetics of congeneric limpets across a biogeographic transition zone reveals common patterns of genetic structure and demographic history.
Scurria
Chile
RADseq
Southeastern Pacific
intertidal
rocky shores
Journal
Molecular ecology
ISSN: 1365-294X
Titre abrégé: Mol Ecol
Pays: England
ID NLM: 9214478
Informations de publication
Date de publication:
07 2023
07 2023
Historique:
revised:
21
04
2023
received:
30
12
2022
accepted:
26
04
2023
medline:
11
7
2023
pubmed:
10
5
2023
entrez:
10
5
2023
Statut:
ppublish
Résumé
The distribution of genetic diversity is often heterogeneous in space, and it usually correlates with environmental transitions or historical processes that affect demography. The coast of Chile encompasses two biogeographic provinces and spans a broad environmental gradient together with oceanographic processes linked to coastal topography that can affect species' genetic diversity. Here, we evaluated the genetic connectivity and historical demography of four Scurria limpets, S. scurra, S. variabilis, S. ceciliana and S. araucana, between ca. 19° S and 53° S in the Chilean coast using genome-wide SNPs markers. Genetic structure varied among species which was evidenced by species-specific breaks together with two shared breaks. One of the shared breaks was located at 22-25° S and was observed in S. araucana and S. variabilis, while the second break around 31-34° S was shared by three Scurria species. Interestingly, the identified genetic breaks are also shared with other low-disperser invertebrates. Demographic histories show bottlenecks in S. scurra and S. araucana populations and recent population expansion in all species. The shared genetic breaks can be linked to oceanographic features acting as soft barriers to dispersal and also to historical climate, evidencing the utility of comparing multiple and sympatric species to understand the influence of a particular seascape on genetic diversity.
Banques de données
Dryad
['10.5061/dryad.k98sf7mbs']
Types de publication
Journal Article
Research Support, Non-U.S. Gov't
Langues
eng
Sous-ensembles de citation
IM
Pagination
3812-3825Informations de copyright
© 2023 John Wiley & Sons Ltd.
Références
Aguirre, C., Pizarro, Ó., Strub, P. T., Garreaud, R., & Barth, J. A. (2012). Seasonal dynamics of the near-surface alongshore flow off Central Chile. Journal of Geophysical Research: Oceans, 117(1), 1-17.
Alcala, N., & Vuilleumier, S. (2014). Turnover and accumulation of genetic diversity across large time-scale cycles of isolation and connection of populations. Proceedings of the Royal Society B: Biological Sciences, 281(1794), 20141369.
Allio, R., Donega, S., Galtier, N., & Nabholz, B. (2017). Large variation in the ratio of mitochondrial to nuclear mutation rate across animals: Implications for genetic diversity and the use of mitochondrial DNA as a molecular marker. Molecular Biology and Evolution, 34(11), 2762-2772.
Asorey, C. M. (2017). Diversificación y coexistencia de Lottidae (Mollusca: Patellogastropoda) en la costa del Pacífico Suroriental. [PhD thesis, Facultad de Ciencias del Mar, Universidad Católica].
Barahona, M., Broitman, B. R., Faugeron, S., Jaugeon, L., Ospina-Alvarez, A., Véliz, D., & Navarrete, S. A. (2019). Environmental and demographical factors influence the spatial genetic structure of an intertidal barnacle in Central-Northern Chile. Marine Ecology Progress Series, 612, 151-165.
Bird, C. E., Holland, B. S., Bowen, B. W., & Toonen, R. J. (2007). Contrasting phylogeography in three endemic Hawaiian limpets (Cellana spp.) with similar life histories. Molecular Ecology, 16(15), 3173-3186.
Bowen, B. W., Gaither, M. R., DiBattista, J. D., Iacchei, M., Andrews, K. R., Grant, W. S., Toonen, R. J., & Briggs, J. C. (2016). Comparative phylogeography of the ocean planet. Proceedings of the National Academy of Sciences of the United States of America, 113(29), 7962-7969.
Brattström, H., & Johanssen, A. (1983). Ecological and regional zoogeography of the marine benthic fauna of Chile. Sarsia, 68(4), 289-339.
Broitman, B., Navarrete, S., Smith, F., & Gaines, S. (2001). Geographic variation of southeastern pacific intertidal communities. Marine Ecology Progress Series, 224, 21-34.
Broitman, B. R., Blanchette, C. A., Menge, B. A., Lubchenco, J., Krenz, C., Foley, M., Raimondi, P. T., Lohse, D., & Gaines, S. D. (2008). Spatial and temporal patterns of invertebrate recruitment along the west coast of the United States. Ecological Monographs, 78(3), 403-421.
Broitman, B. R., Lagos, N. A., Opitz, T., Figueroa, D., Maldonado, K., Ricote, N., & Lardies, M. A. (2021). Phenotypic plasticity is not a cline: Thermal physiology of an intertidal barnacle over 20° of latitude. Journal of Animal Ecology, 90(8), 1961-1972.
Camus, P. A. (2001). Biogeografía marina de Chile continental. Revista Chilena de Historia Natural, 74(3), 587-617.
Cárdenas, L., Castilla, J. C., & Viard, F. (2009). A phylogeographical analysis across three biogeographical provinces of the South-Eastern Pacific: The case of the marine gastropod Concholepas concholepas. Journal of Biogeography, 36(5), 969-981.
Catchen, J., Hohenlohe, P. A., Bassham, S., Amores, A., & Cresko, W. A. (2013). Stacks: An analysis tool set for population genomics. Molecular Ecology, 22(11), 3124-3140.
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., Durbin, R., & 1000 Genomes Project Analysis Group. (2011). The variant call format and VCFtools. Bioinformatics, 27(15), 2156-2158.
Dawson, M. N., Hays, C. G., Grosberg, R. K., & Raimondi, P. T. (2014). Dispersal potential and population genetic structure in the marine intertidal of the eastern North Pacific. Ecological Monographs, 84(3), 435-456.
Dray, S., & Dufour, A. (2007). The ade4 package: Implementing the duality diagram for ecologists. Journal of Statistical Software, 22(4), 1-20.
Espoz, C. (2002). Relaciones ecológicas y evolutivas entre los patelogastrópodos intermareales endémicos a la costa rocosa de Perú y Chile: Distribución, abundancia y filogenia. [PhD thesis, Pontificia Universidad Catolica de Chile, Chile, 253 p].
Espoz, C., Lindberg, D. R., Castilla, J. C., & Simison, W. B. (2004). Los patelogastrópodos intermareales de Chile y Perú. Revista Chilena de Historia Natural, 77(2), 257-283.
Ewers-Saucedo, C., Pringle, J. M., Sepúlveda, H. H., Byers, J. E., Navarrete, S. A., & Wares, J. P. (2016). The oceanic concordance of phylogeography and biogeography: A case study in Notochthamalus. Ecology and Evolution, 6(13), 4403-4420.
Foll, M., & Gaggiotti, O. E. (2008). A genome scan method to identify selected loci appropriate for both dominant and codominant markers: A Bayesian perspective. Genetics, 180, 977-993.
Fraser, C. I., Morrison, A. K., Hogg, A. M., Macaya, E. C., van Sebille, E., Ryan, P. G., Padovan, A., Jack, C., Valdivia, N., & Waters, J. M. (2018). Antarctica's ecological isolation will be broken by storm-driven dispersal and warming. Nature Climate Change, 8, 704-708.
Fraser, C. I., Nikula, R., & Waters, J. M. (2011). Oceanic rafting by a coastal community. Proceedings of the Royal Society B, 278, 649-655.
Fraser, C. I., Velásquez, M., Nelson, W. A., Macaya, E. C., & Hay, C. H. (2020). The biogeographic importance of buoyancy in macroalgae: A case study of the southern bull-kelp genus Durvillaea (Phaeophyceae), including descriptions of two new species. Journal of Phycology, 56(1), 23-36.
Frichot, E., & François, O. (2015). LEA: An R package for landscape and ecological association studies. Methods in Ecology and Evolution, 6(8), 925-929.
Gilbertson, C. R., & Wyatt, J. D. (2016). Evaluation of euthanasia techniques for an invertebrate species, land snails (Succinea putris). Journal of the American Association for Laboratory Animal Science, 55(5), 577-581.
Goldstien, S. J., Schiel, D. R., & Gemmell, N. J. (2006). Comparative phylogeography of coastal limpets across a marine disjunction in New Zealand. Molecular Ecology, 15(11), 3259-3268.
González, A., Beltrán, J., Hiriart-Bertrand, L., Flores, V., de Reviers, B., Correa, J. A., & Santelices, B. (2012). Identification of cryptic species in the lessonia nigrescens complex (phaeophyceae, laminariales). Journal of Phycology, 48(5), 1153-1165.
Goudet, J., & Jombart, T. (2021). hierfstat: Estimation and tests of hierarchical F-statistics. R package version 0.5-10. https://CRAN.R-project.org/package=hierfstat
Gray, J. E. (1847). A list of the genera of recent Mollusca, their synonyma and types. Proceedings of the Zoological Society of London, 15, 129-219.
Guiñez, R., Pita, A., Pérez, M., Briones, C., Navarrete, S. A., Toro, J., & Presa, P. (2016). Present-day connectivity of historical stocks of the ecosystem engineer Perumytilus purpuratus along 4500 km of the Chilean coast. Fisheries Research, 179, 322-332.
Gutenkunst, R., Hernandez, R., Williamson, S., & Bustamante, C. (2010). Diffusion approximations for demographic inference: DaDi. Nature Precedings, 5, 1.
Haye, P. A., Segovia, N. I., Muñoz-Herrera, N. C., Gálvez, F. E., Martínez, A., Meynard, A., Pardo-Gandarillas, M. C., Poulin, E., & Faugeron, S. (2014). Phylogeographic structure in benthic marine invertebrates of the southeast pacific coast of Chile with differing dispersal potential. PLoS One, 9(2), 1-15.
Haye, P. A., Segovia, N. I., Varela, A. I., Rojas, R., Rivadeneira, M. M., & Thiel, M. (2019). Genetic and morphological divergence at a biogeographic break in the beach-dwelling brooder Excirolana hirsuticauda Menzies (Crustacea, Peracarida). BMC Evolutionary Biology, 19(1), 118.
Hettinger, A., Sanford, E., Hill, T. M., Lenz, E. A., Russell, A. D., & Gaylord, B. (2013). Larval carry-over effects from ocean acidification persist in the natural environment. Global Change Biology, 19, 3317-3326.
Hijmans, R. J. (2021). geosphere: Spherical trigonometry. R package version 1.5-14. https://CRAN.R-project.org/package=geosphere
Hoang, D. T., Vinh, L. S., Flouri, T., Stamatakis, A., von Haeseler, A., & Minh, B. Q. (2018). MPBoot: Fast phylogenetic maximum parsimony tree inference and bootstrap approximation. BMC Evolutionary Biology, 18(1), 1-11.
Hormazabal, S., Shaffer, G., & Leth, O. K. (2004). Coastal transition zone off Chile. Journal of Geophysical Research, 109(C1), C01021.
Jombart, T., & Ahmed, I. (2011). Adegenet 1.3-1: New tools for the analysis of genome-wide SNP data. Bioinformatics, 27(21), 3070-3071.
Jouganous, J., Long, W., Ragsdale, A. P., & Gravel, S. (2017). Inferring the joint demographic history of multiple populations: Beyond the diffusion approximation. Genetics, 206(3), 1549-1567.
Kaiser, J., Lamy, F., & Hebbeln, D. (2005). A 70-kyr sea surface temperature record off southern Chile (Ocean Drilling Program Site 1233). Paleoceanography, 20(4), 1-15.
Kalyaanamoorthy, S., Minh, B. Q., Wong, T. K., Von Haeseler, A., & Jermiin, L. S. (2017). Model Finder: Fast model selection for accurate phylogenetic estimates. Nature Methods, 14(6), 587-589.
Kamvar, Z. N., Tabima, J. F., & Grünwald, N. J. (2014). Poppr: An R package for genetic analysis of populations with clonal, partially clonal, and/or sexual reproduction. PeerJ, 2, e281.
Kay, M. C., & Emlet, R. B. (2002). Laboratory spawning, larval development, and metamorphosis of the limpets Lottia digitalis. Invertebrate Biology, 121(1), 11-24.
Kolbin, K. G., & Kulikova, V. A. (2011). Reproduction and larval development of the limpet Lottia persona (Rathke, 1833) (Gastropoda: Lottiidae). Russian Journal of Marine Biology, 37(3), 239-242.
Kuo, E. S. L., & Sanford, E. (2013). Northern distribution of the seaweed limpet Lottia insessa (Mollusca: Gastropoda) along the Pacific coast. Pacific Science, 67(2), 303-313.
Langmead, B., & Salzberg, S. (2012). Fast gapped-read alignment with Bowtie 2. Nature Methods, 9, 357-359.
Lara, C., Saldías, G. S., Cazelles, B., Rivadeneira, M. M., Haye, P. A., & Broitman, B. R. (2019). Coastal biophysical processes and the biogeography of rocky intertidal species along the South-Eastern Pacific. Journal of Biogeography, 46(2), 420-431.
Lardies, M. A., Caballero, P., Duarte, C., & Poupin, M. J. (2021). Geographical variation in phenotypic plasticity of intertidal sister Limpet's species under ocean acidification scenarios. Frontiers in Marine Science, 8, 1-13.
Largier, J. L. (2020). Upwelling bays: How coastal upwelling controls circulation, habitat, and productivity in bays. Annual Review of Marine Science, 12, 415-447.
Lesson, R. P. (1830). Voyage autour du monde, sur la Corvette la Coquille, pendant les années 1822-1825. Voyage Coquille, Zoölogie 2.
Letelier, J., Soto-Mardones, L., Salinas, S., Vincenti, L., Pavez, R., & Arriagada, M. (2012). Influencia de la península de mejillones en la variabilidad oceanográfica anual e interanual frente al norte de Chile. Revista de Biología Marina y Oceanografía, 47(3), 513-526.
López, B. A., Macaya, E. C., Jeldres, R., Valdivia, N., Bonta, C. C., Tala, F., & Thiel, M. (2018). Spatio-temporal variability of strandings of the southern bull kelp Durvillaea Antarctica (Fucales, Phaeophyceae) on beaches along the coast of Chile linked to local storms. Journal of Applied Phycology, 31(3), 2159-2173.
Manel, S., Guerin, P. E., Mouillot, D., Blanchet, S., Velez, L., Albouy, C., & Pellissier, L. (2020). Global determinants of freshwater and marine fish genetic diversity. Nature Communications, 11, 692.
McGaughran, A., Liggins, L., Marske, K. A., Dawson, M. N., Schiebelhut, L. M., Lavery, S., Knowles, L., Moritz, C., & Riginos, C. (2022). Comparative Phylogeography in the genomic age: Opportunities and challenges. Journal of Biogeography, 49, 2130-2144.
Navarrete, S. A., Broitman, B. R., & Menge, B. A. (2008). Interhemispheric comparison of recruitment to intertidal communities: Pattern persistence and scales of variation. Ecology, 89(5), 1308-1322.
Navarrete, S. A., Wieters, E. A., Broitman, B. R. R., & Castilla, J. C. (2005). Scales of benthic-pelagic coupling and the intensity of species interactions: From recruitment limitation to top-down control. Proceedings of the National Academy of Sciences of the United States of America, 102(50), 18046-18051.
Nguyen, L. T., Schmidt, H. A., Von Haeseler, A., & Minh, B. Q. (2015). IQ-TREE: A fast and effective stochastic algorithm for estimating maximum-likelihood phylogenies. Molecular Biology and Evolution, 32(1), 268-274.
Noskova, E., Ulyantsev, V., Koepfli, K. P., O'Brien, S. J., & Dobrynin, P. (2020). GADMA: Genetic algorithm for inferring demographic history of multiple populations from allele frequency spectrum data. GigaScience, 9(3), giaa005.
Oksanen, J., Blanchet, F. G., Friendly, M., Kindt, R., Legendre, P., McGlinn, D., Minchin, P. R., O'Hara, R. B., Simpson, G. L., Solymos, P., Stevens, M. H., Szoecs, E., & Wagner, H. (2020). vegan: Community ecology package. R package version 2.5-7. https://CRAN.R-project.org/package=vegan
O'Leary, S. J., Puritz, J. B., Willis, S. C., Hollenbeck, C. M., & Portnoy, D. S. (2018). These aren't the loci you'e looking for: Principles of effective SNP filtering for molecular ecologists. Molecular Ecology, 27(16), 3193-3206.
Orbigny, A. D. (1841). Voyage dans l'Amérique méridionale. Mollusques, 5, 409-488.
Page, L. R. (2002). Apical sensory organ in larvae of the patellogastropod Tectura scutum. Biological Bulletin, 202(1), 6-22.
Pantoja, S., Iriarte, J. L., & Daneri, G. (2011). Oceanography of the Chilean Patagonia. Continental Shelf Research, 31(3-4), 149-153.
Paris, J. R., Stevens, J. R., & Catchen, J. M. (2017). Lost in parameter space: A road map for stacks. Methods in Ecology and Evolution, 8(10), 1360-1373.
Privé, F., Luu, K., Vilhjálmsson, B. J., & Blum, M. G. (2020). Performing highly efficient genome scans for local adaptation with R package pcadapt version 4. Molecular Biology and Evolution, 37(7), 2153-2154.
Quesada-Calderón, S., Giles, E. C., Morales-González, S., & Saenz-Agudelo, P. (2021). Pinpointing genetic breaks in the southeastern Pacific: Phylogeography and genetic structure of a commercially important tunicate. Journal of Biogeography, 48(10), 2604-2615.
Ragionieri, L., Fratini, S., Vannini, M., & Schubart, C. D. (2009). Phylogenetic and morphometric differentiation reveal geographic radiation and pseudo-cryptic speciation in a mangrove crab from the Indo-West Pacific. Molecular Phylogenetics and Evolution, 52(3), 825-834.
Ramajo, L., Valladares, M., Astudillo, O., Fernández, C., Rodríguez-Navarro, A. B., Watt-Arévalo, P., Núñez, M., Grenier, C., Román, R., Aguayo, P., Lardies, M. A., Broitman, B. R., Tapia, P., & Tapia, C. (2020). Upwelling intensity modulates the fitness and physiological performance of coastal species: Implications for the aquaculture of the scallop Argopecten purpuratus in the Humboldt current system. Science of the Total Environment, 745, 140949.
Riginos, C., & Liggins, L. (2013). Seascape genetics: Populations, individuals, and genes marooned and adrift. Geography Compass, 7(3), 197-216.
Ríoz Cardoza, C. F. (1992). Dinámica del asentamiento larvario de Scurria scurra (Lesson, 1830) (Gastropoda: Acmaeidae) en el intermareal rocoso de Mehuín (X Región). [Master Dissertation, Facultad de Ciencias, Universidad Austral de Chile].
Rivadeneira, M. M., Fernández, M., & Navarrete, S. A. (2002). Latitudinal trends of species diversity in rocky intertidal herbivore assemblages: Spatial scale and the relationship between local and regional species richness. Marine Ecology Progress Series, 245, 123-131.
Rodríguez-Romero, A., Gaitán-Espitía, J. D., Opitz, T., & Lardies, M. A. (2022). Heterogeneous environmental seascape across a biogeographic break influences the thermal physiology and tolerances to ocean acidification in an ecosystem engineer. Diversity and Distributions, 28, 1542-1553.
Roughan, M., Mace, A. J., Largier, J. L., Morgan, S. G., Fisher, J. L., & Carter, M. L. (2005). Subsurface recirculation and larval retention in the lee of a small headland: A variation on the upwelling shadow theme. Journal of Geophysical Research, C: Oceans, 110(10), 1-18.
Saenz-Agudelo, P., Peluso, L., Nespolo, R., Broitman, B. R., Haye, P. A., & Lardies, M. A. (2022). Population genomic analyses reveal hybridization and marked differences in genetic structure of Scurria limpet sister species with parapatric distributions across the south eastern Pacific. Ecology and Evolution, 12(5), 1-13.
Saldías, G. S., Largier, J. L., Mendes, R., Pérez-Santos, I., Vargas, C. A., & Sobarzo, M. (2016). Satellite-measured interannual variability of turbid river plumes off Central-Southern Chile: Spatial patterns and the influence of climate variability. Progress in Oceanography, 146, 212-222.
Saldías, G. S., Sobarzo, M., & Quiñones, R. (2019). Freshwater structure and its seasonal variability off western Patagonia. Progress in Oceanography, 174, 143-153.
Sánchez, R., Sepúlveda, R. D., Brante, A., & Cárdenas, L. (2011). Spatial pattern of genetic and morphological diversity in the direct developer Acanthina monodon (Gastropoda: Mollusca). Marine Ecology Progress Series, 434, 121-131.
Selkoe, K. A., D'Aloia, C. C., Crandall, E. D., Iacchei, M., Liggins, L., Puritz, J. B., Von Der Heyden, S., & Toonen, R. J. (2016). A decade of seascape genetics: Contributions to basic and applied marine connectivity. Marine Ecology Progress Series, 554, 1-19.
Sowerby, G. B. (1839). Molluscous animals and their shells. In F. W. Beechey (Ed.), The zoology of captain Beechey's voyage to the Pacific and Behring's straits (pp. 103-155). H. G. Bohn.
Strub, P. T., James, C., Montecino, V., Rutllant, J. A., & Blanco, J. L. (2019). Ocean circulation along the southern Chile transition region (38°-46°S): Mean, seasonal and interannual variability, with a focus on 2014-2016. Progress in Oceanography, 172, 159-198.
Swearer, S. E., Treml, E. A., & Shima, J. S. (2019). A review of biophysical models of marine larval dispersal. Oceanography and Marine Biology, 57, 325-356.
Thiel, M., Macaya, E. C., Acuña, E., Arntz, W., Bastias, H., Brokordt, K., Camus, P., Castilla, J., Castro, L., Cortés, M., Dumont, C., Escribano, R., Miriam, F., Gajardo, J. A., Gaymer, C. F., Gómez, I., Gonzalez, A., González, H., Haye, P., … Vega, J. (2007). The Humboldt current system of northern and Central Chile oceanographic processes, ecological interactions and socioeconomic feedback. Oceanography and Marine Biology, 45, 195-344.
Valdivia, N., Aguilera, M. A., Navarrete, S. A., & Broitman, B. R. (2015). Disentangling the effects of propagule supply and environmental filtering on the spatial structure of a rocky shore metacommunity. Marine Ecology Progress Series, 538, 67-79.
Valdovinos, C. (1999). Biodiversidad de moluscos chilenos : base de datos taxonómica y distribucional. Gayana, 63(2), 111-164.
Vargas, C. A., Cuevas, L. A., Broitman, B. R., San Martin, V. A., Lagos, N. A., Gaitán-Espitia, J. D., & Dupont, S. (2020). Upper environmental pCO2 drives sensitivity to ocean acidification in marine invertebrates. Nature Climate Change, 12(2), 200-207.
Zakas, C., Binford, J., Navarrete, S. A., & Wares, J. P. (2009). Restricted gene flow in Chilean barnacles reflects an oceanographic and biogeographic transition zone. Marine Ecology Progress Series, 394(2), 165-177.
Zheng, X., Levine, D., Shen, J., Gogarten, S., Laurie, C., & Weir, B. (2012). A high-performance computing toolset for relatedness and principal component analysis of SNP data. Bioinformatics, 28(24), 3326-3328.