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Unexpected Absence of Population Structure and High Genetic diversity Article Unexpected Absence of Population Structure and High Genetic Diversity of the Western Atlantic Hermit Crab Clibanarius antillensis Stimpson, 1859 (Decapoda: Diogenidae) Based on Mitochondrial Markers and Morphological Data Keity S. Nishikawa , Mariana Negri and Fernando L. Mantelatto * Laboratory of Bioecology and Crustacean Systematics (LBSC), Department of Biology, Faculty of Philosophy, Sciences and Letters at Ribeirão Preto (FFCLRP), University of São Paulo (USP), Av. Bandeirantes 3900, Ribeirão Preto 14040-901, São Paulo, Brazil; [email protected] (K.S.N.); [email protected] (M.N.) * Correspondence: fl[email protected] Abstract: Recent studies on genetic variability have revealed different patterns of genetic structure among populations of marine decapod species with wide geographical distribution. The hermit crab Clibanarius antillensis has a broad distribution along the western Atlantic Ocean, from south Florida (United States) to Santa Catarina (Brazil). This factor, in addition to differences in larval morphology and in adult coloration, makes this species a good model for studies on intraspecific variations. Therefore, we evaluated the molecular and morphological variability of C. antillensis Citation: Nishikawa, K.S.; Negri, M.; along its distribution in order to check the levels of population structure. The results were based on Mantelatto, F.L. Unexpected Absence the morphological analyses of 187 individuals and 38 partial sequences of the mitochondrial gene 16S of Population Structure and High rRNA and 46 of cytochrome c oxidase subunit I (COI) from specimens whose locations covered the Genetic Diversity of the Western whole species distribution. The molecular analyses did not show any apparent population structure Atlantic Hermit Crab Clibanarius of C. antillensis. This result was corroborated by the morphological analyses since the characters antillensis Stimpson, 1859 (Decapoda: Diogenidae) Based on Mitochondrial analyzed did not show any pattern of variation. Our results may be explained by a set of factors, Markers and Morphological Data. such as the dispersive potential of the species and the absence of barriers that could prevent gene Diversity 2021, 13, 56. https:// flow. In addition, high genetic diversity was observed, mainly for COI, which may be explained doi.org/10.3390/d13020056 by the historical processes of the species, which seem to be in almost constant expansion in the last 700,000 years and experienced no genetic bottleneck. Apparently, this species was little affected Academic Editors: Michael Wink, by the climate fluctuations of Pleistocene. Additionally, our morphological analyses allowed us to Patricia Briones-Fourzán and Michel present herein a redescription of the studied species since we noted differences from the characters in E. Hendrickx the diagnosis. Received: 11 December 2020 Accepted: 27 January 2021 Keywords: cytochrome c oxidase subunit I (COI); larval dispersal; mitochondrial genes; molecular Published: 1 February 2021 data; 16S rRNA; redescription Publisher’s Note: MDPI stays neutral with regard to jurisdictional claims in published maps and institutional affil- 1. Introduction iations. Species and their populations are constantly changing. Their history, as well as details from their current stage of genetic structure, are a combination of different past events [1], which may be understood by investigating their genetic processes [2]. Gene flow, for example, is essential to maintain genetic homogeneity or heterogeneity among populations Copyright: © 2021 by the authors. Licensee MDPI, Basel, Switzerland. of a species [3,4]. This article is an open access article For most marine invertebrate species, planktonic larvae and their life span influence distributed under the terms and their dispersion process which allows them to interconnect populations by reaching long conditions of the Creative Commons distances [5,6]. Therefore, long larval stages are usually related to high dispersal capac- Attribution (CC BY) license (https:// ity and levels of gene flow and reduced population genetic structure [7–9]. However, creativecommons.org/licenses/by/ some studies revealed that high levels of connectivity and genetic homogeneity were not 4.0/). necessarily related to the duration of planktonic stages [10–12]. In addition, gene flow Diversity 2021, 13, 56. https://doi.org/10.3390/d13020056 https://www.mdpi.com/journal/diversity Diversity 2021, 13, 56 2 of 28 Diversity 2021, 13, 56 2 of 28 essarily related to the duration of planktonic stages [10–12]. In addition, gene flow may mayalso alsobe influenced be influenced by marine by marine currents currents circulation, circulation, local local oceanic oceanic conditions, conditions, physical physical bar- barriers,riers, food food availability, availability, ecological ecological interactions, interactions, as aswell well as aspast past geological geological events events and and re- recentcent history history [8,10,13–22]. [8,10,13–22]. Therefore,Therefore, eacheach marinemarine species species has has its its own own patterns patterns of of gene gene flow flow and and genetic genetic differ- dif- encesferences along along its distributionits distribution [14, 23[14,23].]. This This occurs occurs because because each each individual individual has a has unique a unique way toway respond to respond to different to different factors factors at specific at specif momentsic moments [14]. Gene [14]. flow Gene patterns flow maypatterns be revealed may be byrevealed studies by on studies genetic on variability genetic variability of populations of populations [24], which [24], might whic showh might different show levelsdifferent of geographiclevels of geographic structure structure and genetic and diversity genetic [diversity25]. [25]. ManyMany studiesstudies havehave revealedrevealed geographicgeographic structurestructure onon marinemarine decapoddecapod crustaceanscrustaceans withwith widewide distribution.distribution. AsAs examples,examples, thethe hermithermit crabscrabsCalcinus Calcinus tibicentibicenHerbst, Herbst, 17911791 [26[26]] andandClibanarius Clibanarius vittatus vittatusBosc, Bosc, 1802 1802 [27 [27]] exhibited exhibited different differen patternst patterns of populationof population structure struc- alongture along their distributiontheir distribution in the in western the western Atlantic Atlantic Ocean. Ocean. TheThe hermithermit crabcrabClibanarius Clibanarius antillensisantillensis Stimpson,Stimpson, 18591859 (Figure(Figure1 1)) occurs occurs in in Bermuda, Bermuda, FloridaFlorida (US),(US), Gulf Gulf of of Mexico, Mexico, Belize, Belize, Costa Costa Rica, Rica, Panama, Panama, Antilles, Antilles, north north of of South South America Amer- andica and Brazil Brazil (in Atol (in dasAtol Rocas das Rocas and from and the from state the of state Piau íofto Piauí Santa to Catarina) Santa Catarina) (Figure2 )[(Figure28–32 ]2). It[28–32]. is found It inis found intertidal in intertidal zones, shallow zones, waters, shallow over waters, rocks, over coral rocks, reefs, coral and reefs, banks and of Halod- banks uleof Halodule[30,33]. The [30,33]. species The has species a larval has development a larval developme of five tont sixof stagesfive to thatsix stages require that at leastrequire 43 daysat least to complete43 days to [34 complete,35]. [34,35]. FigureFigure 1.1.Clibanarius Clibanarius antillensisantillensis Stimpson,Stimpson, 1859. Preserved female specimen, specimen, CCDB CCDB 5061. 5061. Photo Photo by by Buranelli, R.C. Buranelli, R.C. Diversity 2021, 13, 56 3 of 28 Diversity 2021, 13, 56 3 of 28 Figure 2. Distribution of Clibanarius antillensis Stimpson, 1859 (blue line). Colored dots indicate collecting sites where we sampled specimens whose partial sequences of 16S rRNA andand cytochrome c oxidase subunit I (COI) werewere obtained.obtained. * indicates only sequences of 16S rRNA obtained. Abbreviations: TM: Tamaulipas; VE: Veracruz; TB: Tabasco; QR: indicates only sequences of 16S rRNA obtained. Abbreviations: TM: Tamaulipas; VE: Veracruz; TB: Tabasco; QR: Quintana Quintana Roo; PI: Piauí; CE: Ceará; RN: Rio Grande do Norte; PE: Pernambuco; AL: Alagoas; BA: Bahia; ES: Espírito Roo; PI: Piauí; CE: Ceará; RN: Rio Grande do Norte; PE: Pernambuco; AL: Alagoas; BA: Bahia; ES: Espírito Santo; RJ: Rio de Santo; RJ: Rio de Janeiro; SP: São Paulo; SC: Santa Catarina. Janeiro; SP: São Paulo; SC: Santa Catarina. Some morphological differences were found between larvae from Brazil and Pana- Some morphological differences were found between larvae from Brazil and Panama ma and Mexico populations, such as the number of antennular aesthetascs, the number of and Mexico populations, such as the number of antennular aesthetascs, the number of denticles of crista dentate of the third maxilliped, the development of the external lobe of denticles of crista dentate of the third maxilliped, the development of the external lobe of thethe maxillule andand endopodendopod of of the the maxilla maxilla [34 [34–36–36].]. Additionally, Additionally, distinct distinct coloration coloration patterns pat- ternswere foundwere found among among adults adults from differentfrom different localities localities [37]. [37]. Additional investigations investigations on on genetic genetic variability variability may may contribute contribute to to a a better better compre- hension of biogeographic processes, populationpopulation differentiation and biodiversity along groups/families of hermithermit crabscrabs in in the the western
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