Mitochondrial genetic divergence of Chiton articulatus (Polyplacophora: Chitonida) in the Mexican Tropical Pacific
Thelma A. Aguilar-Rendon A B # , Omar Hernando Avila-Poveda
A B C # and Nancy C. Saavedra-Sotelo A C *
A
B
C
# These authors contributed equally to this paper
Handling Editor: Max Finlayson
Abstract
Chiton articulatus is a gonochoric, free-spawning mollusc with short-lived trochophore larvae inhabiting rocky shores along the fragmented and heterogeneous Mexican Tropical Pacific (MTP). Its limited dispersal in this patchy environment may lead to genetic divergence among populations.
Our objective was to characterise the genetic diversity and population structure of C. articulatus based on mitochondrial DNA.
We conducted a phylogeographic analysis using the cytochrome c oxidase subunit I (COI) gene of mitochondrial DNA collected from 100 C. articulatus organisms located across its geographic distribution.
The findings showed high levels of genetic diversity and a high number of private haplotypes. The structure analysis indicated six genetically distinct clusters with low connectivity. Divergence between the northern and southern populations was evident, with central mixing suggesting that gene flow adhered to the stepping-stone model. The historical demography indicated that the populations experienced sudden expansions during the late Pleistocene and early Holocene.
The northernmost and southernmost C. articulatus populations exhibit significant genetic divergence, suggesting the presence of distinct stocks in the MTP. Nevertheless, we recommend prioritising the conservation of central populations, as they serve as essential genetic reservoirs for all populations.
Our findings contribute to the broader understanding of how limited larval dispersal and habitat fragmentation shape population structure in marine invertebrates. The identification of distinct genetic stocks and central populations acting as genetic reservoirs underscores the importance of integrating genetic data into marine spatial planning and fisheries management. This research provides a framework for the conservation of other intertidal species with similar life histories in fragmented coastal environments.
Keywords: ecoregion Mexican Tropical Pacific, fishery, genetic drift, heteroplasmy, isolation-by-distance, marine invertebrates, mtDNA, rocky intertidal.
References
Abadia-Chanona QY (2015) Maduración gonádica, ciclo reproductivo y talla de madurez sexual del quitón Chiton (Chiton) articulatus (Mollusca: Polyplacophora) de la costa rocosa de Puerto Ángel, Oaxaca, México. MSc thesis, Centro Interdisciplinario de Ciencias Marinas, Instituto Politécnico Nacional, La Paz, BCS, Mexico. [In Spanish]
Abadia-Chanona QY, Avila-Poveda OH, Arellano-Martínez M, Ceballos-Vázquez BP (2016) Observation and establishment of gonad development stages in polyplacophorans (Mollusca): Chiton (Chiton) articulatus a case study. Acta Zoologica 97, 506-521.
| Crossref | Google Scholar |
Abadia-Chanona QY, Avila-Poveda OH, Arellano-Martínez M, Ceballos-Vázquez BP, Benitez-Villalobos F, Parker GA, Rodriguez-Dominguez G, Garcia-Ibañez S (2018) Reproductive traits and relative gonad expenditure of the sexes of the free spawning Chiton articulatus (Mollusca: Polyplacophora). Invertebrate Reproduction & Development 62, 268-289.
| Crossref | Google Scholar |
Al Rawi S, Louvet-Vallée S, Djeddi A, Sachse M, Culetto E, Hajjar C, Boyd L, Legouis R, Galy V (2011) Postfertilization autophagy of sperm organelles prevents paternal mitochondrial DNA transmission. Science 334, 1144-1147.
| Crossref | Google Scholar | PubMed |
Aljanabi SM, Martinez I (1997) Universal and rapid salt-extraction of high quality genomic DNA for PCR-based techniques. Nucleic Acids Research 25, 4692-4693.
| Crossref | Google Scholar | PubMed |
Alvarez-Cerrillo LR, Benitez-Villalobos F, García-Ibañez S, Avila-Poveda OH (2021) Biodiversity patterns of epibiotic invertebrates occupying an edible polyplacophoran across a latitudinal gradient of the Mexican Pacific. Journal of Experimental Marine Biology and Ecology 545, e151644.
| Crossref | Google Scholar |
Alvarez-Garcia IL, Abadia-Chanona QY, Arellano-Martínez M, Avila-Poveda OH (2025) Maximum gonad investment reveals male bias when temperature decreases or latitude increases for a broadcast-spawning intertidal chiton (Polyplacophora: Chitonida). Hydrobiologia 852, 69-88.
| Crossref | Google Scholar |
Avila-Poveda OH (2013) Annual change in morphometry and in somatic and reproductive indices of Chiton articulatus adults (Polyplacophora: Chitonidae) from Oaxaca, Mexican Pacific. American Malacological Bulletin 31, 65-74.
| Crossref | Google Scholar |
Avila-Poveda OH (2020) Large-scale project ‘Chiton of the Mexican Tropical Pacific’: Chiton articulatus (Mollusca: Polyplacophora). Research Ideas and Outcomes 6, e60446.
| Crossref | Google Scholar |
Avila-Poveda OH, Abadia-Chanona QY (2013) Emergence, development, and maturity of the gonad of two species of chitons “sea cockroach” (Mollusca: Polyplacophora) through the early life stages. PLoS ONE 8, e69785.
| Crossref | Google Scholar |
Avila-Poveda OH, Rodriguez-Dominguez G, Ramirez-Perez JS, Perez-Gonzalez R (2020) Plasticity in growth parameters of an intertidal rocky shore chiton (Polyplacophora: Chitonida) under pre-ENSO and ENSO events. Journal of Molluscan Studies 86(1), 72-78.
| Crossref | Google Scholar |
Avila-Poveda OH, Abadia-Chanona QY, Alvarez-Garcia IL, Arellano-Martínez M (2021) Plasticity in reproductive traits of an intertidal rocky shore chiton (Polyplacophora: Chitonida) under pre-ENSO and ENSO events. Journal of Molluscan Studies 87, eyaa033.
| Crossref | Google Scholar |
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.
| Crossref | Google Scholar | PubMed |
Barahona M, Broitman BR, Faugeron S, Jaugeon L, Ospina-Alvarez A, Véliz D, Navarrete SA (2019) Environmental and demographic factors influence the spatial genetic structure of an intertidal barnacle in central-northern Chile. Marine Ecology Progress Series 612, 151-165.
| Crossref | Google Scholar |
Beerli P (2012) Migrate documentation version 3.2.1. (Department of Scientific Computing, Florida State University: Tallahassee, FL, USA) Available at https://popgen.sc.fsu.edu/migratedoc.pdf
Benzie JAH (1999) Genetic structure of coral reef organisms: ghosts of dispersal past. American Zoologist 39, 131-145.
| Crossref | Google Scholar |
Birky CW, Jr (2001) The Inheritance of genes in mitochondria and chloroplasts: laws, mechanisms, and models. Annual Review of Genetics 35, 125-148.
| Crossref | Google Scholar | PubMed |
Breton S, Stewart DT, Brémaud J, Havird JC, Smith CH, Hoeh WR (2022) Did doubly uniparental inheritance (DUI) of mtDNA originate as a cytoplasmic male sterility (CMS) system? BioEssays 44, 2100283.
| Crossref | Google Scholar |
Buckland-Nicks J (2008) Fertilization biology and the evolution of chitons. American Malacological Bulletin 25, 97-111.
| Crossref | Google Scholar |
Buckland-Nicks J (2014) Apocrine secretion of the egg hull in oogenesis and exclusion of sperm organelles at fertilization make reproduction in Chitonida (Mollusca) unique. Journal of Natural History 48, 2885-2897.
| Crossref | Google Scholar |
Buckland-Nicks J, Brothers E (2008) On fertilization in Chaetopleura apiculata and selected chitonida. The Biological Bulletin 214, 184-193.
| Crossref | Google Scholar | PubMed |
Bullock RC (1985) The Stenoplax limaciformis (Sowerby, 1832) species complex in the new world (Mollusca: Polyplacophora: Ischnochitonidae). The Veliger 27, 291-307.
| Google Scholar |
Bullock RC (1988) The genus Chiton in the new world (Polyplacophora: Chitonidae). The Veliger 31, 141-191.
| Google Scholar |
Chiappa-Carrara X, Enríquez C, Papiol V, Mariño-Tapia I, Reyes-Hernández C (2019) Chapter 28: Pacific Coast of Mexico. In ‘World Seas: an environmental evaluation. Vol. I: Europe, The Americas and West Africa’. (Ed. C Sheppard) pp. 655–671. (Academic Press) Available at https://www.elsevier.com/books/world-seas-an-environmental-evaluation/sheppard/978-0-12-805068-2
Clement M, Posada D, Crandall KA (2000) TCS: a computer program to estimate gene genealogies. Molecular Ecology 9, 1657-1659.
| Crossref | Google Scholar | PubMed |
Conover DO, Clarke LM, Munch SB, Wagner GN (2006) Spatial and temporal scales of adaptive divergence in marine fishes and the implications for conservation. Journal of Fish Biology 69, 21-47.
| Crossref | Google Scholar |
Cowen RK, Sponaugle S (2009) Larval dispersal and marine population connectivity. Annual Review of Marine Science 1, 443-466.
| Crossref | Google Scholar | PubMed |
Deng QE, Hazel W (2010) Population structure and phylogeography of an acorn barnacle with induced defense and its gastropod predator in the Gulf of California. Marine Biology 157, 1989-2000.
| Crossref | Google Scholar |
Diario Oficial de la Federación (2023) ACUERDO mediante el cual se da a conocer la Actualización de la Carta Nacional Pesquera. (DOF) Available at https://www.gob.mx/cms/uploads/attachment/file/892410/CNP_2023.pdf [In Spanish]
Doonan J, Beatty GE, Sigwart JD, Provan J (2012) Extensive local-scale gene flow and long-term population stability in the intertidal mollusc Katharina tunicata (Mollusca: Polyplacophora). Biological Journal of the Linnean Society 106, 589-597.
| Crossref | Google Scholar |
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.
| Crossref | Google Scholar | PubMed |
Fernández R, Lemer S, Mcintyre E, Giribet G (2015) Comparative phylogeography and population genetic structure of three widespread mollusc species in the Mediterranean and near Atlantic. Marine Ecology 36, 701-715.
| Crossref | Google Scholar |
Ferreira AJ (1983) The chiton fauna of the Revillagigedo archipelago, Mexico. The Veliger 25, 307-322.
| Google Scholar |
Ferrera-Rodríguez MR, Malpica-Cruz L, Munguía-Vega A, Beas-Luna R, Flores-Morales AL, Abadía-Cardoso A (2024) Revealing genetic patterns across ecoregions in the northeastern Pacific of California and Baja California. Journal of Biogeography 51, 2298-2311.
| Crossref | Google Scholar |
Flores-Campaña LM, Arzola-González JF, Jimenez-Diaz O, Leon-Herrera R (2012) Estimación del potencial pesquero de Chiton articulatus Sowerby, 1832, en las islas de la Bahia de Mazatlán, Sinaloa. In ‘La investigación científica, tecnológica y social en la uas (profapi 2008)’. pp. 89–98. (Universidad Autónoma de Sinaloa: Culiacán de Rosales, Sinaloa, Mexico) [In Spanish]
Folmer O, Black M, Hoeh W, Lutz R, Vrijenhoek R (1994) DNA primers for amplification of mitochondrial cytochrome c oxidase subunit I from diverse metazoan invertebrates. Molecular Marine Biology and Biotechnology 3, 294-299.
| Google Scholar | PubMed |
Fu Y-X (1997) Statistical tests of neutrality of mutations against population growth, hitchhiking and background selection. Genetics 147, 915-925.
| Crossref | Google Scholar | PubMed |
Fu YX, Li WH (1993) Statistical tests of neutrality of mutations. Genetics 133, 693-709.
| Crossref | Google Scholar | PubMed |
Garcia-Ibañez S, Flores-Garza R, Flores-Rodríguez P, Violante-González J, Valdés-González A, Olea-de-la-Cruz FG (2013) Diagnostico pesquero de Chiton articulatus (Mollusca: Polyplacophora) en Acapulco, México. Revista de Biología Marina y Oceanografía 48, 293-302 [In Spanish].
| Crossref | Google Scholar |
García-Ibáñez S, Flores-Rodríguez P, Flores-Garza R, Nieto-Navarro JT, Bernabé-Moreno IE (2014) Respuesta del carnívoro Plicopurpura pansa (mollusca: gastropoda) y el herbívoro Chiton articulatus (mollusca: polyplacophora) a factores ambientales en Acapulco, México. CienciaUAT 8, 11-21 [In Spanish].
| Crossref | Google Scholar |
García-Ríos CI, Pérez-Pérez NM, Fernandez-Lopez J, Fuentes FA (2014) Calibrating the chitons (Mollusca: Polyplacophora) molecular clock with the mitochondrial DNA cytochrome C oxidase I gene. Calibrando un reloj molecular para quitones (Mollusca: Polyplacophora) utilizando el gen mitocondrial que codifica para el citocromo oxidasa I. Revista de Biología Marina y Oceanografía 49, 193-207 [In English with title, abstract and keywords in English and Spanish].
| Crossref | Google Scholar |
Ghiselli F, Maurizii MG, Reunov A, Ariño-Bassols H, Cifaldi C, Pecci A, Alexandrova Y, Bettini S, Passamonti M, Franceschini V, Milani L (2019) Natural heteroplasmy and mitochondrial Inheritance in bivalve molluscs. Integrative and Comparative Biology 59, 1016-1032.
| Crossref | Google Scholar | PubMed |
Ghiselli F, Gomes-dos-Santos A, Adema CM, Lopes-Lima M, Sharbrough J, Boore JL (2021a) Molluscan mitochondrial genomes break the rules. Philosophical Transactions of the Royal Society of London – B. Biological Sciences 376, 20200159.
| Crossref | Google Scholar |
Ghiselli F, Iannello M, Piccinini G, Milani L (2021b) Bivalve molluscs as model systems for studying mitochondrial biology. Integrative and Comparative Biology 61, 1699-1714.
| Crossref | Google Scholar | PubMed |
Gomez-Valdivia F, Pares-Sierra A, Flores-Morales AL (2015) The Mexican coastal current: a subsurface seasonal bridge that connects the tropical and subtropical Northeastern Pacific. Continental Shelf Research 110, 100-107.
| Crossref | Google Scholar |
Gusman A, Lecomte S, Stewart DT, Passamonti M, Breton S (2016) Pursuing the quest for better understanding the taxonomic distribution of the system of doubly uniparental inheritance of mtDNA. PeerJ 4, e2760.
| Crossref | Google Scholar |
Hays CG, Hanley TC, Hughes AR, Truskey SB, Zerebecki RA, Sotka EE (2021) Local adaptation in marine foundation species at microgeographic scales. The Biological Bulletin 241, 16-29.
| Crossref | Google Scholar | PubMed |
Hurtado LA, Frey M, Gaube P, Pfeiler E, Markow TA (2007) Geographical subdivision, demographic history and gene flow in two sympatric species of intertidal snails, Nerita scabricosta and Nerita funiculata, from the tropical eastern Pacific. Marine Biology 151, 1863-1873.
| Crossref | Google Scholar |
Jacobs DK, Haney TA, Louie KD (2004) Genes, diversity, and geologic process on the Pacific coast. Annual Review of Earth and Planetary Sciences 32, 601-652.
| Crossref | Google Scholar |
Jensen JL, Bohonak AJ, Kelley ST (2005) Isolation by distance, web service. BMC Genetics 6, 13.
| Crossref | Google Scholar |
Kelly RP, Palumbi SR (2010) Genetic structure among 50 species of the northeastern Pacific rocky intertidal community. PLoS ONE 5, e8594.
| Crossref | Google Scholar |
Kelly RP, Oliver TA, Sivasundar A, Palumbi SR (2010) A method for detecting population genetic structure in diverse, high gene-flow species. Journal of Heredity 101, 423-436.
| Crossref | Google Scholar | PubMed |
Kessler WS (2006) The circulation of the eastern tropical Pacific: a review. Progress in Oceanography 69, 181-217.
| Crossref | Google Scholar |
Kimura M (1953) Stepping-stone model of population. Annual Report of the National Institute of Genetics, Japan 3, 62-63.
| Google Scholar |
Kimura M (1980) A simple method for estimating evolutionary rates of base substitutions through comparative studies of nucleotide sequences. Journal of Molecular Evolution 16, 111-120.
| Crossref | Google Scholar | PubMed |
Kimura M, Weiss GH (1964) The stepping stone model of population structure and the decrease of genetic correlation with distance. Genetics 49, 561-576.
| Crossref | Google Scholar | PubMed |
Kumar S, Stecher G, Tamura K (2016) MEGA7: Molecular Evolutionary Genetics Analysis version 7.0 for bigger datasets. Molecular Biology and Evolution 33, 1870-1874.
| Crossref | Google Scholar | PubMed |
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.
| Crossref | Google Scholar |
Lavin MF, Fiedler PC, Amador JA, Ballance LT, Färber-Lorda J, Mestas-Nuñez AM (2006) A review of eastern tropical Pacific oceanography: summary. Progress in Oceanography 69, 391-398.
| Crossref | Google Scholar |
Lee HJ, Boulding EG (2007) Mitochondrial DNA variation in space and time in the northeastern Pacific gastropod, Littorina keenae. Molecular Ecology 16, 3084-3103.
| Crossref | Google Scholar | PubMed |
Leigh JW, Bryant D (2015) PopART: full−feature software for haplotype network construction. Methods in Ecology and Evolution 6, 1110-1116.
| Crossref | Google Scholar |
Lewis JB (1960) The fauna of rocky shores of Barbados, West Indies. Canadian Journal of Zoology 38, 391-435.
| Crossref | Google Scholar |
Lindsay WR, Andersson S, Bererhi B, Höglund J, Johnsen A, Kvarnemo C, Leder EH, Lifjeld JT, Ninnes CE, Olsson M, Parker GA, Pizzari T, Qvarnström A, Safran RJ, Svensson O, Edwards SV (2019) Endless forms of sexual selection. PeerJ 7, e7988.
| Crossref | Google Scholar |
Lopez-Chavez FJ, Chassin-Noria O, Ríos-Chávez P, Rocha-Ramírez V, Macip-Ríos R, Oyama K (2016) Phylogeography of the purple snail Plicopurpura pansa along the Mexican Pacific coast. Filogeografía del caracol púrpura Plicopurpura pansa a lo largo de la costa del Pacífico mexicano. Ciencias Marinas 42, 1-14 [In English with title, abstract and keywords in English and Spanish].
| Crossref | Google Scholar |
López-Sandoval DC, Lara-Lara JR, Álvarez-Borrego S, Gaxiola-Castro G (2009) Primary productivity observations in the eastern tropical Pacific off Cabo Corrientes, Mexico. Productividad primaria en el Pacífico oriental tropical adyacente a Cabo Corrientes, México. Ciencias Marinas 35, 169-182 [In English with title, abstract and keywords in English and Spanish].
| Crossref | Google Scholar |
Mann DH, Hamilton TD (1995) Late Pleistocene and Holocene paleoenvironments of the North Pacific coast. Quaternary Science Reviews 14, 449-471.
| Crossref | Google Scholar |
Marshall DJ, Krug PJ, Kupriyanova EK, Byrne M, Emlet RB (2012) The biogeography of marine invertebrate life histories. Annual Review of Ecology, Evolution, and Systematics 43, 97-114.
| Crossref | Google Scholar |
Meyer CP, Geller JB, Paulay G (2005) Fine scale endemism on coral reefs: archipelagic differentiation in turbinid gastropods. Evolution 59, 113-125.
| Crossref | Google Scholar | PubMed |
Ni G, Kim T, Shin Y, Park J, Lee Y, Kill H-J, Park J-K (2020) Life-history features and oceanography drive phylogeographic patterns of the chiton Acanthochitona cf. rubrolineata (Lischke, 1873) in the northwestern Pacific. PeerJ 8, e8794.
| Crossref | Google Scholar |
Olea-de-la-Cruz F, Garcia-Ibañez S, Flores-Garza R, Flores-Rodríguez P, Rojas-Herrera A (2013) Pesca, oferta y demanda de la cucaracha de mar Chiton articulatus (Mollusca: Polyplacophora) en aguas de la zona costera del estado de Guerrero, Mexico. Ciencia Pesquera 21, 69-81 [In Spanish].
| Google Scholar |
Palmer ANS (2012) Spatial and genetic investigation of aggregation in Ischnochiton (Polyplacophora; Neoloricata; Ischnochitonina; Ischnochitonidae; Ischnochitoninae) species with different larval development. Austral Ecology 37, 110-124.
| Crossref | Google Scholar |
Palumbi SR (1997) Molecular biogeography of the Pacific. Coral Reefs 16, S47-S52.
| Crossref | Google Scholar |
Parakatselaki M-E, Ladoukakis ED (2021) mtDNA Heteroplasmy: origin, detection, significance, and evolutionary consequences. Life 11, 633.
| Crossref | Google Scholar |
Pfeiler E, Hurtado LA, Knowles LL, Torre-Cosío J, Bourillón-Moreno L, Márquez-Farías JF, Montemayor-López G (2005) Population genetics of the swimming crab Callinectes bellicosus (Brachyura: Portunidae) from the eastern Pacific Ocean. Marine Biology 146, 559-569.
| Crossref | Google Scholar |
Pineda J, Hare JA, Sponaugle S (2007) Larval transport and dispersal in the coastal ocean and consequences for population connectivity. Oceanography 20, 22-39.
| Crossref | Google Scholar |
Pinsky ML, Montes HR, Jr, Palumbi SR (2010) Using isolation by distance and effective density to estimate dispersal scales in anemonefish. Evolution 64, 2688-2700.
| Crossref | Google Scholar | PubMed |
Planes S, Fauvelot C (2002) Isolation by distance and vicariance drive genetic structure of a coral reef fish in the Pacific Ocean. Evolution 56, 378-399.
| Crossref | Google Scholar | PubMed |
Portela E, Beier E, Barton ED, Castro R, Godínez V, Palacios-Hernández E, Fiedler PC, Sánchez-Velasco L, Trasviña A (2016) Water masses and circulation in the Tropical Pacific off central Mexico and surrounding areas. Journal of Physical Oceanography 46, 3069-3081.
| Crossref | Google Scholar |
Poutiers J (1995) Quitones (Anfineuros, loricados, poliplacoforos). In ‘Guia FAO para la identificacion de especies para los fines de la pesca. Pacífico Centro-Oriental: Plantas e Invertebrados’. (Eds W Fischer, F Krupp, W Schneider, C Sommer, KE Carpenter, VH Niem) pp. 299–304. (Food and Agriculture Organization of the United Nations: Rome, Italy) Available at https://www.fao.org/4/t0851s/t0851s00.htm [In Spanish]
Quesada H, Stuckas H, Skibinski DOF (2003) Heteroplasmy suggests paternal co-transmission of multiple genomes and pervasive reversion of maternally into paternally transmitted genomes of mussel (Mytilus) mitochondrial DNA. Journal of Molecular Evolution 57, S138-S147.
| Crossref | Google Scholar | PubMed |
Ramirez-Santana BP, Rodriguez-Dominguez G, Avila-Poveda OH (2019) De herbivoro a omnivoro: evidencia anatómica del tipo de alimentación en Chiton articulatus (Mollusca: Polyplacophora). In ‘XV Reunión Nacional de Malacología y Conquiliología’, 8–11 October 2019, Mérida, Mexico. Abstract, p. 19. (Sociedad de Malacología de México A.C.) Available at https://www.smmac.org.mx/xv-renamac-2019 [In Spanish]
Ramı́rez-Herrera M-T, Urrutia-Fucugauchi J (1999) Morphotectonic zones along the coast of the Pacific continental margin, southern Mexico. Geomorphology 28, 237-250.
| Crossref | Google Scholar |
Reyes-Gomez A (2004) Chitons in Mexican waters. Bollettino Malacologico 39(Suppl. 5), 69-82.
| Google Scholar |
Reyes-Gómez A, Flores-Garza R, Galeana-Rebolledo L, Hernández-Vera G, Galván-Villa C, Torreblanca-Ramirez C, Flores-Rodríguez P, García-Ibañez S, Ríos-Jara E (2022) Intertidal chitons (Mollusca: Polyplacophora) from the rocky coastline of Guerrero, Mexico, with the description of a new species. Zootaxa 5155, 451-492.
| Crossref | Google Scholar |
Rice WR (1989) Analyzing tables of statistical tests. Evolution 43, 223-225.
| Crossref | Google Scholar | PubMed |
Rios-Jara E, Perez-Peña M, Lopez-Uriarte E, Enciso-Padilla I, Juarez-Carrillo E (2006) Biodiversidad de moluscos marinos de la costa de Jalisco y Colima, con anotaciones sobre su aprovechamiento en la región. In ‘Los recursos pesqueros y acuícolas de Jalisco, Colima y Michoacan’. (Eds MC Jiménez-Quiroz, E Espino-Barr) pp. 103–120. (SAGARPA) [In Spanish]
Rogers AR, Harpending H (1992) Population growth makes waves in the distribution of pairwise genetic differences. Molecular Biology and Evolution 9, 552-569.
| Crossref | Google Scholar | PubMed |
Saavedra-Sotelo NC (2013) Viviendo en el límite: evaluación del efecto de hábitats marginales en la diversidad y diferenciación genética de corales hermatípicos en el Golfo de California y el Pacífico Mexicano. PhD thesis, Centro de Investigación Científica y de Educación Superior de Ensenada, Baja California Ensenada, Mexico. Available at http://cicese.repositorioinstitucional.mx/jspui/handle/1007/742 [In Spanish]
Saavedra-Sotelo NC, Calderon-Aguilera LE, Reyes-Bonilla H, López-Pérez RA, Medina-Rosas P, Rocha-Olivares A (2011) Limited genetic connectivity of Pavona gigantea in the Mexican Pacific. Coral Reefs 30, 677-686.
| Crossref | Google Scholar |
Saavedra-Sotelo NC, Calderon-Aguilera LE, Reyes-Bonilla H, Paz-García DA, López-pérez RA, Cupul-Magaña A, Cruz-Barraza JA, Rocha-Olivares A (2013) Testing the genetic predictions of a biogeographical model in a dominant endemic Eastern Pacific coral (Porites panamensis) using a genetic seascape approach. Ecology and Evolution 3, 4070-4091.
| Crossref | Google Scholar | PubMed |
Sanford E, Kelly MW (2011) Local adaptation in marine invertebrates. Annual Review of Marine Science 3, 509-535.
| Crossref | Google Scholar | PubMed |
Scheet P, Stephens M (2006) A fast and flexible statistical model for large-scale population genotype data: applications to inferring missing genotypes and haplotypic phase. American Journal of Human Genetics 78, 629-644.
| Crossref | Google Scholar | PubMed |
Sirenko BI (2015) The enigmatic viviparous chiton Calloplax vivipara (Plate, 1899) (Mollusca: Polyplacophora) and a survey of the types of reproduction in chitons. Russian Journal of Marine Biology 41, 24-31.
| Crossref | Google Scholar |
Skibinski DO, Gallagher C, Beynon CM (1994) Sex-limited mitochondrial DNA transmission in the marine mussel Mytilus edulis. Genetics 138, 801-809.
| Crossref | Google Scholar | PubMed |
Smith AG (1966) The larval development of chitons (Amphineura). Proceedings of the California Academy of Sciences 32, 433-446.
| Google Scholar |
Sotka EE (2005) Local adaptation in host use among marine invertebrates. Ecology Letters 8, 448-459.
| Crossref | Google Scholar |
Spalding MD, Fox HE, Allen GR, Davidson N, Ferdaña ZA, Finlayson M, Halpern BS, Jorge MA, Lombana A, Lourie SA, Martin KD, McManus E, Molnar J, Recchia CA, Robertson J (2007) Marine ecoregions of the world: a bioregionalization of coastal and shelf areas. BioScience 57, 573-583.
| Crossref | Google Scholar |
Stephens M, Donnelly P (2003) A comparison of bayesian methods for haplotype reconstruction from population genotype data. American Journal of Human Genetics 73, 1162-1169.
| Crossref | Google Scholar | PubMed |
Stephens M, Smith NJ, Donnelly P (2001) A new statistical method for haplotype reconstruction from population data. American Journal of Human Genetics 68, 978-989.
| Crossref | Google Scholar | PubMed |
Strathmann MF, Eernisse DJ (1987) Phylum Mollusca, Class Polyplacophora. In ‘Reproduction and Development of Marine Invertebrates of the Northern Pacific Coast: Data and Methods for the Study of Eggs, Embryos, and Larvae’. (Ed. MF Strathmann) pp. 205–219. (University of Washington Press: Seattle, WA, USA)
Teske PR, Sandoval-Castillo J, Sasaki M, Beheregaray LB (2015) Invasion success of a habitat-forming marine invertebrate is limited by lower-than-expected dispersal ability. Marine Ecology Progress Series 536, 221-227.
| Crossref | Google Scholar |
Valencia-Cayetano C, Garcia-Ibañez S, Avila-Poveda OH, Padilla-Serrato JG, Violante-González J, Flores-Garza R (2023) Using a fisherman’s harvest in Acapulco, México, to characterize population structure, allometry, and body condition in the edible intertidal mollusc Chiton articulatus (Chitonida: Chitonidae). Regional Studies in Marine Science 62, 102976.
| Crossref | Google Scholar |
Veale AJ, Lavery SD (2011) Phylogeography of the snakeskin chiton Sypharochiton pelliserpentis (Mollusca: Polyplacophora) around New Zealand: are seasonal near-shore upwelling events a dynamic barrier to gene flow? Biological Journal of the Linnean Society 104, 552-563.
| Crossref | Google Scholar |
Villamor A, Costantini F, Abbiati M (2014) Genetic structuring across marine biogeographic boundaries in rocky shore invertebrates. PLoS ONE 9, e101135.
| Crossref | Google Scholar |
Wang L, Xu Y (2003) Haplotype inference by maximum parsimony. Bioinformatics 19, 1773-1780.
| Crossref | Google Scholar | PubMed |
Weir BS, Cockerham CC (1984) Estimating F-statistics for the analysis of population structure. Evolution 38, 1358-1370.
| Crossref | Google Scholar | PubMed |
Wright S (1943) Isolation by distance. Genetics 28, 114-138.
| Crossref | Google Scholar | PubMed |
Zamudio L, Hurlburt HE, Metzger EJ, Tilburg CE (2007) Tropical wave-induced oceanic eddies at Cabo Corrientes and the María Islands, Mexico. Journal of Geophysical Research: Oceans 112, C05048.
| Crossref | Google Scholar |
Zouros E (2000) The exceptional mitochondrial DNA system of the mussel family Mytilidae. Genes & Genetic Systems 75, 313-318.
| Crossref | Google Scholar | PubMed |
Zouros E, Ball AO, Saavedra C, Freeman KR (1994) An unusual type of mitochondrial DNA inheritance in the blue mussel Mytilus. Proceedings of the National Academy of Sciences of the United States of America 91, 7463-7467.
| Google Scholar | PubMed |
