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Article

Phylogeography of a Widely Distributed Atlantic Species: The Case of the Ghost Crab Ocypode quadrata (Fabricius, 1787) (Decapoda: Brachyura: Ocypodidae)

by
Ana Francisca Tamburus
1,2,
Ivana Miranda
1,3,
Bárbara Benati Naves
1 and
Fernando Luis Mantelatto
1,*
1
Laboratório de Bioecologia e Sistemática de Crustáceos (LBSC), Departamento de Biologia, Faculdade de Filosofia, Ciências e Letras de Ribeirão Preto (FFCLRP), Universidade de São Paulo (USP), Av. Bandeirantes 3900, Monte Alegre, Ribeirão Preto, São Paulo 14040-901, Brazil
2
Laboratório de Biologia e Ecologia de Camarões Marinhos e de Água Doce (LABCAM), Departamento de Biologia, Faculdade de Ciências, Universidade Estadual Paulista “Júlio de Mesquita Filho” (UNESP), Av. Engenheiro Luiz Edmundo Carrijo Coube 14-01, Vargem Limpa, Bauru, São Paulo 17033-360, Brazil
3
Laboratório de Morfologia de Invertebrados (IML) e Centro de Aquicultura da Unesp (CAUNESP), Departamento de Biologia Aplicada à Agropecuária, Faculdade de Ciências Agrárias e Veterinária, Universidade Estadual Paulista “Júlio de Mesquita Filho” (UNESP), Via de Acesso Professor. Paulo Donato Castellane, s/n, Jaboticabal, São Paulo 14884-900, Brazil
*
Author to whom correspondence should be addressed.
Arthropoda 2024, 2(2), 130-148; https://doi.org/10.3390/arthropoda2020010
Submission received: 14 February 2024 / Revised: 27 March 2024 / Accepted: 3 April 2024 / Published: 8 April 2024
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Abstract

:
Ocypode Weber, 1795 (Brachyura: Ocypodidae) is popularly known as ghost crab, and encompasses 21 valid species, including Ocypode quadrata (Fabricius, 1787). This species has wide distribution along the Atlantic coast of America, from the USA (Massachusetts) to Brazil (Rio Grande do Sul), Central America, and Antilles. Such distribution, along with some biological characteristics of its life cycle and the presence of geographic barriers, could lead to genetic structuring. Herein, we evaluate the hypothesis of the presence of geographic barriers using COI and 16S partial gene fragments. The Maximum Likelihood tree suggests the monophyly of O. quadrata, while the values of intraspecific genetic distance along with the star-shaped haplotype network suggested a lack of genetic structure in Brazilian, Panama, and French Guiana populations, probably caused by larval dispersion. USA and Mexico populations may be a new lineage, but we cannot say it with few sequences and with no morphological characters.

1. Introduction

Ocypode Weber, 1795 (Brachyura: Ocypodidae) [1] is the popularly known ghost crab, with 21 recognized species and it is one of the most abundant crabs of the family Ocypodidae Rafinesque, 1815. Ocypode quadrata (Fabricius, 1787) is the only species of the genus that occurs across the western Atlantic region, from the USA (Massachusetts) to Brazil (Rio Grande do Sul), Central America, and Antilles [2,3,4] (Figure 1). This species is semiterrestrial and typically inhabits the entire supralittoral zone, including dunes, sandy beaches, and vegetated areas, also being found in the upper midlittoral zone, where individual burrows are flooded during high tides [2,5]. This crab can provide essential information about the negative impact on beach ecosystems and contribute in efforts towards the conservation of beach biodiversity, since the threat of human impact is to have an irreversible effect on this environment [6,7]. The widespread distribution of O. quadrata, along with its semiterrestrial habitat, its long planktonic larval phases, and its potential as a tool for impact on beach ecosystems, make this species an interesting example to understand different patterns of genetic differentiation, and population structure, mainly through the study of genetic variability.
The ecological characteristics of this species were widely studied [5,8,9,10,11,12,13,14], as well as its capability of survival in the intertidal areas [9], which facilitates its collection and monitoring. Furthermore, it can be used as a bioindicator for human actions on several beaches in the Americas [11,15,16].
Ocypode quadrata has planktonic larvae, five zoeal stages, and a megalopa that stays 60 days in the water column [17,18]; the morphology of the megalopa is probably adaptive for survival through postponed metamorphosis for more than 34 days into the first crab stage [19]. Those larval features can facilitate high dispersal capacity, which can be related to genetic structure, as well as observed in populations that are not panmictic but are very widely dispersed [20].
All these characteristics draw attention to O. quadrata being a potential model for several studies, as was the case in other regional genetic population studies [6,21] and in systematics and taxonomy [1]. Despite this well-developed knowledge on biology and ecology of O. quadrata, the information on genetic variability with this taxon is still scanty. In this way, molecular analyses using the genetic barcoding can help in the characterization of the genetic variability among the populations, detecting homogeneity or structuring, and improving the knowledge of the dispersion mechanism of this species.
Studies of genetic variability and using the barcoding approach can be seen not only in different groups of Decapoda (e.g., [22,23,24,25,26]), but also in many other organisms (e.g., [27,28,29,30]).
Some species are widely spread due to their planktonic larval characteristics and, along with potential barriers to gene flow, such as isolation by distance, sea currents, or changes in salinity caused by the outflow of the mouth of the Amazon River into the Atlantic Ocean [31,32,33,34,35,36], are a promising model in studies, for example, of genetic variability. Our study is going to increase the number of DNA sequences from two genes’ fragments (COI and 16S), amplifying the sample area of this species distribution, different from what has been previously studied. From this, our study tests the hypothesis of genetic structure in O. quadrata across the western Atlantic coast of America among populations of the Caribbean Sea and Northeast and Southeast Brazil influenced by the Amazon River plume.

2. Materials and Methods

Specimens of O. quadrata were obtained from donations and loans and are deposited in the following collections: Coleção de Crustáceos do Departamento de Biologia (CCDB), Faculdade de Filosofia, Ciências e Letras de Ribeirão Preto–Universidade de São Paulo (FFCLRP/USP), Ribeirão Preto, Brazil; Museu de Zoologia, Universidade de São Paulo (MZUSP), São Paulo, Brazil; Coleção de Crustáceos da Universidade Federal do Rio Grande do Sul (UFRGS), Porto Alegre, Brazil. The specimens examined are listed in Table 1.
Genomic DNA was extracted from muscle samples from pereiopods with Chelex® (Chelating Ion Exchange Resin; [41]). The final concentration of extracted DNA was measured using a spectrophotometer (NanoDrop 2000/2000c) to calculate the amount of DNA to be used in the PCR reaction.
We used a two-locus mitochondrial approach that included partial sequences of 16S rRNA (16S) and cytochrome oxidase I (COI), which were found to be valuable in other marine decapod population studies [23,26,33,35,36,42]. Fragments of 600 bp (16S) and 700 bp (COI) were amplified by means of a polymerase chain reaction (PCR), using the universal primers LCO1490 (5′-GGT CAA ATC ATA AAG ATA TTG-3′) and HCO2198 (5′-TAA ACT TCA GGG TGA CCA AAA AAT CA-3′) [43], and 16Sar (5′-CGC CTG TTT ATC AAA AAC AT-3′) and 16Sbr (5′-CCG GTC TGA ACT CAG ATC ACG T-3′) [44]. PCR procedures followed [45,46,47] with adjustments in annealing temperatures according to the specific primers, decreasing until a 5 °C melting temperature. PCRs were performed in a total volume of 25 μL, which included 4.5 μL of Millipore-filtered water, 5 μL of betaine (5 M), 4 μL of dNTP (10 μM), 3 μL of MgCl2 (25 μM), 3 μL of a 10× PCR Taq buffer with (NH4)2SO4, 1 μL of each primer (10 μM for 16S and 20 μM for COI), 0.5 μL of 1.5 U Taq DNA polymerase. We followed the thermal cycles of initial denaturing for 4 min at 94 °C; pairing for 40 cycles (50 s at 94 °C, 70 s at 45/48 °C, and 1 min at 72 °C); final extension for 10 min at 72 °C [1]. PCR products were purified using a Sure Clean Plus® kit (Bioline, Tauton, MA, USA) and were sequenced with the ABI 3730 XL DNA Analyzer® (Applied Biosystems, 850 Lincoln Centre Drive, Foster City, CA 94404, USA).
All sequences were confirmed by sequencing forward and reverse strands. The consensus sequence for both strands was obtained using the computational program Geneious v.2021.2 [48]. Sequences were aligned in MAFFT v.7 [49] using default parameters. We used the program GBlocks v.091b [50,51] to locate and exclude ambiguous areas of the alignment or each locus, using relaxed gap selection criteria (allowed gap positions = all). Alignments were concatenated in the software Geneious v.2021. 2. All sequences were submitted to GenBank under specific accession numbers (COI: OR354404-OR354434; 16S: OR352135-OR352150; see Table 1). Genetic vouchers used in molecular analyses are deposited in the collection of the CCDB/FFCLRP/USP or at the institution of origin.
Samples were grouped according to geographical distribution in Brazilian States, and countries for those localities with fewer individuals (USA, Mexico, Panama, and French Guiana). Genetic distances were calculated to determine intra- and interspecific variation rates with the software MEGA v. 11.0.10 [52], using the p-distance method; distance values are in percentages.
Phylogenetic hypotheses were proposed using Maximum Likelihood (ML) [53] performed on the W-IQ-TREE online platform using models selected by the program based on the data provided [54]. For the concatenate ML tree, we chose just specimens with both DNA fragments (16S and COI), since the other samples have just one sequence, which would configure a lot of missing data (Table 1); this analysis aimed to contextualize O. quadrata within the genus. The best-fit models according to BIC were GTR+F+I+G4 for concatenate genes; branch support was evaluated by ultrafast bootstrapping (1000 pseudoreplicates); bootstrap values > 60% are shown in all trees.
GenBank sequences from Ocypode africana De Man, 1881; Ocypode ceratophthalmus (Pallas, 1772); Ocypode macrocera H. Milne Edwards, 1837; Ocypode nobilii De Man, 1902; Ocypode cordimana Latreille, 1818; Ocypode kuhlii De Haan, 1835; Ocypode rotundata Miers, 1882; Ocypode ryderi Kingsley, 1880; Ocypode sinensis Dai & Yang in Song & Yang, 1985; Ocypode stimpisoni Ortmann, 1897; Ocypode occidentalis Stimpson, 1860; and Ocypode gaudichaudii H. Milne Edwards & Lucas, 1843 were analyzed as sister groups and Afruca tangeri (Eydoux, 1835) as an outgroup (Table 1), following the phylogeny proposal for Ocypodidae [1].
Population parameters of genetic variability within each locality are represented by the number of haplotypes (h), segregating sites (S), haplotype diversity (Hd), nucleotide diversity (π), and average number of nucleotide differences (k), estimated in DnaSP 6.12.1 [55]. The haplotype networks were constructed with PopART v. 4.8.4 [56] using the statistical parsimony method TCS Network [57]. A linear cross-mark and the total number of mutational steps represent the links among lineages; the number in the circle represents the frequency of each haplotype, and the smallest circles indicate only one haplotype. The black dots show missing haplotypes and the connections among haplotypes indicate one mutation step. The black dots or the average vectors are considered hypothetical haplotypes (sequences), generated by the program to connect the sampled haplotypes [58]. The analysis of molecular variance (AMOVA) and the pairwise fixation index (FST) were evaluated in Arlequin 3.5 [59], with 10,000 permutations, to calculate the variance within localities, and between Brazilian States, the USA, Mexico, Panama, and French Guiana.
The neutrality tests Tajima’s D [60] and Fu’s Fs [61] were performed in DnaSP 6.12.1 [55] to explain observed patterns in genetic variation within populations of O. quadrata considering the interaction between genetic drift and mutation, including other parameters like nucleotide heterozygosity and the number of segregating sites in a DNA sequences’ dataset; these tests are useful to detect whether mutations were neutral or under the influence of selection, and also for detecting population growth. In addition, pairwise mismatch distribution was analyzed to test occurrence of contraction or population expansion [62], assay demographic expansion, and detect stability. The sample distribution of pairwise differences will usually deviate from the distribution expected. From this, a variety of shapes can be found, including bimodal and trimodal distributions; this wide variety of distributions is correlated to the pairwise differences and can be because of the history of coalescent events in a single sample of genes [63]. Furthermore, if the observed distribution of pairwise differences is close to a Poisson distribution, that means it is consistent with the hypothesis that the population has been growing exponentially in size [63]; the continued exponential growth suggests a sudden burst of population growth [62]. If the population decreases in size, distributions are initially L-shaped, and then converge quickly to an equilibrium; if the populations are in equilibrium, the theoretical curves are free of waves [62], or a population that has been growing presents mismatch distributions that are smooth and have a peak [64].

3. Results

The present study contributes with 50 new sequences of O. quadrata, 16 sequences from 16S and 34 from COI, another 86 sequences (74 from 16S, 12 for COI) from the same species taken from GenBank, and 24 sequences from other species of the genus (Table 1).
The final alignment of the COI fragment consists of 636 base pairs (bp) and the alignment of the 16S rRNA fragment consists of 511 bp. The intraspecific divergence for Ocypode quadrata varied from 0 to 13.9% and 0 to 6.4% for COI and 16S, respectively, whereas interspecific values ranged from 12.1 to 21.7% for COI (Table S1) and 6.8 to 14.0% for 16S (Table S2), with these values corresponding to the divergence between sequences of O. africana and O. ceratophthalmus. Genetic distances among localities ranged from 0.4 to 19.7% (Table 2) for COI and 0.0 to 6.4% (Table 3) for 16S.
The concatenated phylogram suggested the monophyly of O. quadrata with bootstrap values of 100 (Figure 2), with an external branch consisting of a specimen from Rio Grande do Norte, and a subclade with specimens from different localities (bootstrap: 78%), configuring no pattern dividing groups that could reveal genetic structure.
The genetic variability of Ocypode quadrata could be evaluated by the number of segregating sites (S) with 121 and 33 for COI and 16S, respectively; a nucleotide diversity (π) of 0.0373 (COI) and 0.01108 (16S), with k values of 20.853 (COI) and 5.243 (16S); and haplotype diversity (Hd) of 0.9707 for COI and 0.6014 for 16S (Table 4).
For the COI fragment (34 new sequences, 12 from GenBank), the number of haplotypes (Hap) was 33, with 1 highly frequent haplotype (Hap_9) with seven individuals from four different localities, linked with several unique haplotypes (Hap_10, Hap_17, Hap_18, Hap_20; Hap_26; Hap_27), and 2 less frequent haplotypes (Hap_12, Hap_22). One individual from the USA (Hap_1) with other Mexican haplotypes were separated by more than 20 mutation steps from the Brazilian haplotypes (Figure 3).
For the 16S fragment (16 new sequences, 74 from GenBank), the number of haplotypes was 24; the most common was Hap_2 with 56 specimens from 14 localities, linked with 11 unique haplotypes (Hap_3, Hap_6, Hap_7, Hap_10, Hap_11, Hap_13, Hap_16, Hap_20, Hap_22, Hap_23, Hap_24), and 4 were less frequent (Hap_4, Hap_9, Hap_12, Hap_14, Hap_18). One individual from the USA was separated by 17 mutation steps from three Brazilian haplotypes (Hap_4, Hap_14, Hap_18) (Figure 4). Within Brazilian States, among Brazil, Panama, and French Guiana, both haplotype networks for O. quadrata fit into the star-shaped pattern, suggesting a recent demographic expansion, with no apparent population genetic structure; mainly for the COI gene, the USA and Mexico populations may be a new lineage.
AMOVA results also did not detect any genetic structure among populations (within Brazilian States; among Brazil, Panama, and French Guiana), with p = 0.00168 for the COI fragment, and p = 0.21465 for 16S (Table 5). Most of the FST values were not significant, with a few exceptions of the comparison between localities (Table 6). The result of the neutrality test Tajima’s D was −0.69521 and Fu’s Fs was −3.770, which were not significant (p > 0.10) for the COI gene; and Tajima’s D was −2.45254 and the Fu’s Fs statistic was −25.390, which were significant (p < 0.001), for 16S. For the COI fragment, evolution in O. quadrata occurs by genetic drift and mutation, emphasizing the lack of evidence of selection for these populations. For 16S, these significant values demonstrated that populations of O. quadrata do not reach the equilibrium, for example, if they experienced a bottleneck recently [60].
Mismatch distribution graphics revealed multimodal distributions, which means it deviated from the expected, and pronounced waves with rough crests, which suggest coalescent events and ancient population explosion. Populations possibly passed through contraction and expansion events, which is consistent with the neutrality test (Figure 5A,B), and a third peak suggests multiple genetic clusters (Figure 5A), such as the USA plus Mexico separated from the other localities.

4. Discussion

In the present study, the initial hypothesis of genetic structure in O. quadrata, supported by its wide geographic distribution, was refuted. Other marine Decapoda presented the same pattern, lack of genetic structure, for short and long distances such as the crab Ucides cordatus Linnaeus, 1763 [42]; the mangrove crab Sesarma rectum Randall, 1840 [33]; the swimming crab Callinectes danae Smith, 1869 [35,36]; the western Atlantic hermit crab Clibanarius antillensis Stimpson, 1859 [26]; and the shrimp Artemesia longinaris [23]. Therefore, the wide distribution cannot be considered as a predictive character for this condition in marine organisms. Furthermore, since the barriers to gene flow in these environments influence each organism in a singular way, patterns of genetic structure are not easily established [65,66]. The USA and Mexican specimens presented higher values of genetic distances and many mutation steps at the haplotype networks, suggesting signs of a new lineage. Like those observed herein, for the orange claw hermit crab Calcinus tibicen (Herbst, 1791), results suggested two genetically well-defined groups, North and South Atlantic, but no morphological pattern for each genetic group was observed [34].
There were low intraspecific genetic distances when comparing interspecific values between O. quadrata from Brazilian, Panama, and French Guiana specimens, giving evidence of a lack of structuring, as well as in other marine crabs, like Ocypode species, in which the intraspecific variation for homogeneous populations was around 0.52 ± 0.11%, whereas the values between populations of other genetically structured species were 10.14 ± 0.46% [67]. Considering that individuals of the same species are not identical to each other and may present transversions or random transitions in their genetic material, as well as being subject to environmental factors with potential for phenotypic changes [68], we can infer that this population group of O. quadrata characterizes a lack of genetic structure, since such minimal variation will be present even in species with constant gene flow. Furthermore, we suggest that genetic variability in Brazil seems to be high and populations are diverse, as observed in the different unique haplotypes. In addition, as previously suggested [6], the USA and Mexican specimens are separated from the other localities and may present a new lineage. However, we cannot infer with a few sequences and without observing morphological characters.
Results among distinct localities within Brazil along with Panama and French Guiana also suggested the absence of genetic separation, evidenced by low genetic distance values, and by the polytomies in the phylogenetic tree and the star-shaped haplotype network, like those observed for other populations of O. quadrata [6,21]. Herein, it is plausible to infer that the absence of a geographic pattern in the composition of the formed subgroups is a good indicator of high panmixia, which is a relevant fact, since the pattern found in most living species tends to be the structuring at some level for distant geographical localities [25,69,70]. Considering the broad extension of the Brazilian coast, it is possible that these crabs have a high dispersion capacity, facilitating gene flow even to distant populations, including the populations of Panama and French Guiana, maintaining genetic homogeneity. This dispersion may be attributed to larval characteristics, as five zoeal stages and a megalopa, and their long period of permanence in the plankton [17,18,19].
Different from the other localities, the individual from the USA together with the Mexican population were separated by many mutation steps from the Brazilian with Panama and French Guiana populations, possibly representing a distinct lineage. This aspect has already been subtly pointed out, suggesting an existing barrier to gene flow in the tropical–temperate transition between the Caribbean and the east coast of the USA [6]. The megalopae of O. quadrata have been reported ≈190 km beyond any adult populations in the USA coast, and can tolerate temperature fluctuations, which means that megalopae can migrate for long distances along the coast and might survive long enough to burrow into a sandy beach [71]. In the present study, these characteristics can explain the separation of the USA and Mexico populations from the Brazilian and the other populations. Furthermore, we suggested that the sea currents of the North Atlantic Current and Gulf Stream [72] are influencing the larval dispersion of O. quadrata in long distances and can be responsible for such northern and southern distinct groups. In the present study, we expanded the number of specimens and localities, mainly in Brazil, which increase the number of mutation steps and reinforce the idea of a distinct entity. However, although outside the scope of this study, it would be interesting to analyze morphological characters of USA specimens along with the taxonomical history of O. quadrata and related species.
In Ocypode quadrata, the nucleotide diversity and the haplotype diversity were like other brachyuran species, including the congener species O. ceratophthalmus (Pallas, 1772), which also did not show significant genetic variation among the Japanese populations, but showed a slight difference between the Philippine populations, separated by 30 to 1200 km [67], and three genetically distinct geographical groups, corresponding to the east, west, and central region of the species’ range in the Indo-Pacific region [73]. This small difference between populations is possibly a result of recent population expansion or dispersion [66,67], along with gene flow.
Regarding population size changes, our results indicated that the population of O. quadrata from Brazil, Panama, and French Guina did not show recent abrupt expansions or a bottleneck, which is corroborated by the genetic balance between these populations because of the same demographic balance [74,75], which can also be noted in neutrality data and the star-like haplotype network. Another possibility, a star-like haplotype network with a great quantity of rare haplotypes, could also suggest an insufficient sampling of intraspecific genetic variation since O. quadrata has a wide distribution. Thus, no demographic change was drastic enough to promote lineage divergence between Brazilian, Panama, and French Guiana populations.
Possibly, USA and Mexican populations have been exposed to events of strong selective pressure and/or genetic drift, changing their size abruptly, which makes certain individuals more efficient in transmitting their genes than others [62,76]. Genetic structure and many mutational steps were also observed for Ilyoplax pusilla (De Haan, 1835) [77] and in the swimming crab Callinectes ornatus Ordway, 1863 [78]. These steps indicate modifications by transversions or transitions in the nitrogenous bases, in relation to the previous haplotype, increasing the genetic distance between them. Along the generations, this process can facilitate the genetic structure within populations and posteriorly, the speciation [68]. A population expansion can be indicated by the smoothness of the mismatch distribution, which is not affected by population structure, whereas mean sequence divergence increases in a pooled sample from highly isolated subpopulations [64]. The increase in sequence divergence may be the case of the USA and Mexican populations. Different from O. quadrata, the unimodal distribution observed in the mismatch distributions’ graphics was related to demographic and spatial expansion, suggesting a recent bottleneck effect or sudden population expansion for the crab species S. rectum [33], the occurrence of a recent demographic expansion during the evolutionary history for another crab, U. cordatus [15], and demographic expansion for the hermit crab C. antillensis [26]. As well as in the present study for populations of O. quadrata from the USA and Mexico, the haplotype network and long branches in the phylogram indicate some groups that could present haplotypic structure [6,77], despite the low number of mutational steps. However, the low number of mutational steps within Brazilian populations of O. quadrata was attributed to non-exclusive continuous gene flow and/or genetic variations to each individual, in which some subgroups do not necessarily indicate a genetic separation.
Possible explanations for the high gene flow between populations of geographically distant organisms can be related to the type of occupied habitat [79], its ability to disperse [80,81], and dependency of the life-history strategies [82]. In marine animals, water temperature is an important variable that is influenced by the currents and that can even determine their survival and subsequent reproductive success of individuals in its respective environment. The semiterrestrial Ocypode quadrata is exposed to temperatures that vary between about 16 °C in the north of the United States, 25 °C in the north of Brazil, and 20 °C in the south [18,83]. At temperatures lower than 16 °C, the organism can survive, but in an inactive state, and can remain in its sealed burrow for almost three months of the year [18], which may have an influence on its wide distribution.
As individuals of O. quadrata inhabit supralittoral and intertidal zones, their ability to disperse is mainly attributed to larvae [84]. There are six larval stages, five zoea and a megalopa, that stay in the water column for 60 days [17,18]. It is also described as a unique characteristic of this group, when in the early stages of development, that the megalopa can regulate its development cycle and postpone the metamorphosis until 34 days [19], which further increases its dispersive success, preventing maturation/settlement in not-favorable environments. Those larval features allow us to attribute a high dispersal capacity to the larvae, which explain the lack of genetic structuring in this species. It is like those observed, along the Brazilian coast, in the fiddler crab, Uca maracoani (Latreille, 1803), a semiterrestrial coastal species with an extensive marine pelagic larval duration [66,85]; Minuca panema (Coelho, 1972) [86], and the eastern Pacific Emerita analoga (Stimpson, 1857), an intertidal sandy beach crab with an especially wide latitudinal distribution and a long pelagic larval phase, whose populations are not panmictic but are very widely dispersed and approaching genetic homogeneity [20].
Marine currents may also be facilitators of the dispersion of O. quadrata from southern Brazil to North America. In Brazil, the three main currents are the North Brazil Current (NBC), the Brazil Current, and the Malvinas Current [87], the first two being cold and the last one warm. The NBC is the strongest one, allowing the dispersion of larvae from Rio Grande Norte (Brazil) to Central America [88]. Similar examples were observed for other marine decapods along the western Atlantic, including the tiny shrimp Hippolyte obliquimanus Dana, 1852 [32]; the fiddler crab Minuca rapax (Smith, 1870) (as Uca rapax) [89]; and the orange claw hermit crab C. tibicen [34].
Alternatively, the long-distance larval dispersal can be a consequence of the so-called steppingstone process, which is common for distinct animals, including marine ones [33,90], and can be applicable in O. quadrata. It consists of the connection between fragments of habitats by a given species, enabling the connection between distant regions, providing gene flow from the occupation of these fragments and subsequent dispersal [90,91].

5. Conclusions

In general, there is no genetic structure in O. quadrata; the null hypothesis of the present study was corroborated. The constant gene flow, with low genetic variability, may indicate the absence of sudden selective pressures and genetic drift events in the sampled localities. The individuals from the USA and Mexico were separated from the Caribbean Sea and Brazilian populations, possibly representing a distinct lineage that deserves future attention. Finally, the genetic characteristics of O. quadrata along with its ecological importance improve the knowledge of the life strategy of this crab and should be considered in the management and conservation of sandy beach ecosystems.

Supplementary Materials

The following supporting information can be downloaded at: https://www.mdpi.com/article/10.3390/arthropoda2020010/s1, Table S1. Ocypode quadrata (Fabricius, 1787). The genetic divergence matrix (in percentages) obtained by the pairwise distance method of the partial sequences of the COI gene between specimens. Table S2. Ocypode quadrata (Fabricius, 1787). The genetic divergence matrix (in percentages) obtained by the pairwise distance method of the partial sequences of the 16S gene between specimens. 19–30: Sequences obtained from GenBank. AP: Amapá; BA: Bahia; Br: Brazil; CE: Ceará; PE: Pernambuco; RN: Rio Grande do Norte; SP: São Paulo.

Author Contributions

A.F.T. and B.B.N. carried out the molecular genetic studies, participated in the sequence alignment, analyzed the data. A.F.T. and I.M. revised the paper for intellectual content and wrote the manuscript. F.L.M. conceived the study’s main idea, participated in its design and coordination, developed the molecular protocols, wrote and revised the manuscript. F.L.M. was responsible for and signed for all foundation grants obtained that supported this study in all aspects, for all arrangements and facilities in the USP, and for obtaining the license permits for animal collections. All authors have read and agreed to the published version of the manuscript.

Funding

This research was funded by Conselho Nacional de Desenvolvimento Científico e Tecnológico–CNPq (fellowships IC 114646/2018-0 to B.B.N.; Ph.D. 142082/2015-5 to A.F.T.; and research projects PROTAX 440417/2015-5, PQ 302253/2019-0, and PPBio 2023-07/2023-Linha 8: Rede Costeira Marinha Proc. 442421/2023-0 to F.L.M.); Coordenação de Aperfeiçoamento Pessoal de Nível Superior–CAPES–Finance Code 001 (Ciências do Mar II–2005/2014–23038.004308/201414 granted to F.L.M. and PD fellowship 1989/2014 to I.M.); Fundação de Amparo à Pesquisa do Estado de São Paulo–FAPESP (Temáticos Biota 2010/50188-8 and INTERCRUSTA 2018/13685-5; Coleções Científicas 2009/54931-0; PROTAX 2016/50376-5 and 2021/08075-6) granted to F.L.M.

Institutional Review Board Statement

Not applicable.

Informed Consent Statement

Not applicable.

Data Availability Statement

Data are contained within the article and Supplementary Materials.

Acknowledgments

The authors express thanks to Marcos Tavares (Museu de Zoologia da Universidade de São Paulo–MZUSP/USP, São Paulo, Brazil) and Mariana Terossi (Universidade Federal do Rio Grande do Sul–UFRGS/RS, Rio Grande do Sul, Brazil) for providing specimens/tissue that were used in this study. Specimens from Brazil were obtained under collection permits (permanent license to F.L.M. for collection of Zoological Material No. 11777-2 MMA/IBAMA/SISBIO and SISGEN AE942E3).

Conflicts of Interest

The authors declare no conflicts of interest.

References

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Figure 1. Ocypode quadrata (Fabricius, 1787). A distribution map including localities sampled (black dots) in the present study shown with different colors. Male, CCDB 5087 (Photo: Buranelli, R.C., modified from [4]); scale bar: 27 mm. Brazilian States—AL: Alagoas; AP: Amapá; BA: Bahia; CE: Ceará; ES: Espírito Santo; FN: Fernando de Noronha; PA: Pará; PB: Paraíba; PE: Pernambuco; RJ: Rio de Janeiro; RN: Rio Grande do Norte; SC: Santa Catarina; SE: Sergipe; SP: São Paulo (see more details in Table in Section 2). The colors used on the map correspond to the haplotype networks.
Figure 1. Ocypode quadrata (Fabricius, 1787). A distribution map including localities sampled (black dots) in the present study shown with different colors. Male, CCDB 5087 (Photo: Buranelli, R.C., modified from [4]); scale bar: 27 mm. Brazilian States—AL: Alagoas; AP: Amapá; BA: Bahia; CE: Ceará; ES: Espírito Santo; FN: Fernando de Noronha; PA: Pará; PB: Paraíba; PE: Pernambuco; RJ: Rio de Janeiro; RN: Rio Grande do Norte; SC: Santa Catarina; SE: Sergipe; SP: São Paulo (see more details in Table in Section 2). The colors used on the map correspond to the haplotype networks.
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Figure 2. Ocypode quadrata (Fabricius, 1787). The Maximum Likelihood phylogram obtained for 16S and COI concatenated sequences of O. quadrata specimens and other species of Ocypode. Numbers represent bootstrap values (1000 replicates) and only bootstrap values > 50% are shown. Outgroup and congeners’ sequences were taken from GenBank. AL: Alagoas; AP: Amapá; BA: Bahia; Br: Brazil; CE: Ceará; ES: Espírito Santo; PE: Pernambuco; RJ: Rio de Janeiro; RN: Rio Grande do Norte; SC: Santa Catarina; SE: Sergipe; SP: São Paulo.
Figure 2. Ocypode quadrata (Fabricius, 1787). The Maximum Likelihood phylogram obtained for 16S and COI concatenated sequences of O. quadrata specimens and other species of Ocypode. Numbers represent bootstrap values (1000 replicates) and only bootstrap values > 50% are shown. Outgroup and congeners’ sequences were taken from GenBank. AL: Alagoas; AP: Amapá; BA: Bahia; Br: Brazil; CE: Ceará; ES: Espírito Santo; PE: Pernambuco; RJ: Rio de Janeiro; RN: Rio Grande do Norte; SC: Santa Catarina; SE: Sergipe; SP: São Paulo.
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Figure 3. Ocypode quadrata (Fabricius, 1787). The haplotype network using the statistical parsimony method with 33 haplotypes obtained from COI sequences. The number in the circle represents the frequency of each haplotype, according to the caption; black dots indicate median vectors; each line indicates one mutation step; the total number of mutational steps represents the links among lineages. AL: Alagoas; AP: Amapá; BA: Bahia; CE: Ceará; ES: Espírito Santo; FG: French Guiana; MX: Mexico; Pan: Panama; PE: Pernambuco; RN: Rio Grande do Norte; SC: Santa Catarina; SP: São Paulo; USA: United States of America. The colors used in the haplotype network correspond to the localities on the map (see Figure 1).
Figure 3. Ocypode quadrata (Fabricius, 1787). The haplotype network using the statistical parsimony method with 33 haplotypes obtained from COI sequences. The number in the circle represents the frequency of each haplotype, according to the caption; black dots indicate median vectors; each line indicates one mutation step; the total number of mutational steps represents the links among lineages. AL: Alagoas; AP: Amapá; BA: Bahia; CE: Ceará; ES: Espírito Santo; FG: French Guiana; MX: Mexico; Pan: Panama; PE: Pernambuco; RN: Rio Grande do Norte; SC: Santa Catarina; SP: São Paulo; USA: United States of America. The colors used in the haplotype network correspond to the localities on the map (see Figure 1).
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Figure 4. Ocypode quadrata (Fabricius, 1787). The haplotype network using the statistical parsimony method with 24 haplotypes obtained from 16S sequences. The number in the circle represents the frequency of each haplotype, according to the caption; black dots indicate median vectors; each line indicates one mutation step; the total number of mutational steps represents the links among lineages. AL: Alagoas; AP: Amapá; BA: Bahia; CE: Ceará; ES: Espírito Santo; FN: Fernando de Noronha; PA: Pará; Pan: Panama; PB: Paraíba; PE: Pernambuco; RJ: Rio de Janeiro; RN: Rio Grande do Norte; SC: Santa Catarina; SE: Sergipe; SP: São Paulo; USA: United States of America. The colors used in the haplotype network correspond to the localities on the map (see Figure 1).
Figure 4. Ocypode quadrata (Fabricius, 1787). The haplotype network using the statistical parsimony method with 24 haplotypes obtained from 16S sequences. The number in the circle represents the frequency of each haplotype, according to the caption; black dots indicate median vectors; each line indicates one mutation step; the total number of mutational steps represents the links among lineages. AL: Alagoas; AP: Amapá; BA: Bahia; CE: Ceará; ES: Espírito Santo; FN: Fernando de Noronha; PA: Pará; Pan: Panama; PB: Paraíba; PE: Pernambuco; RJ: Rio de Janeiro; RN: Rio Grande do Norte; SC: Santa Catarina; SE: Sergipe; SP: São Paulo; USA: United States of America. The colors used in the haplotype network correspond to the localities on the map (see Figure 1).
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Figure 5. Mismatch distribution for COI (A) and 16S (B) sequences of Ocypode quadrata (Fabricius, 1787).
Figure 5. Mismatch distribution for COI (A) and 16S (B) sequences of Ocypode quadrata (Fabricius, 1787).
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Table 1. Specimens of the ghost crab Ocypode quadrata (Fabricius, 1787), sister groups, and outgroups used in the molecular analyses. CCDB: Coleção de Crustáceos do Departamento de Biologia–Fa-culdade de Filosofia, Ciências e Letras de Ribeirão Preto, Universidade de São Paulo; MZUSP: Museu de Zoologia, Universidade de São Paulo, Brazil; NCHUZOOL: Zoological Collections of the Department of Life Science, National Chung Hsing University, Taichung, Taiwan; ULLZ: University of Louisiana at Lafayette Zoological Collection, USA; ZRC: Zoological Reference Collection of the Lee Kong Chian Natural History Museum (formerly Raffles Museum of Biodiversity Research). N = number of sequences used; “-” = absence of sequences.
Table 1. Specimens of the ghost crab Ocypode quadrata (Fabricius, 1787), sister groups, and outgroups used in the molecular analyses. CCDB: Coleção de Crustáceos do Departamento de Biologia–Fa-culdade de Filosofia, Ciências e Letras de Ribeirão Preto, Universidade de São Paulo; MZUSP: Museu de Zoologia, Universidade de São Paulo, Brazil; NCHUZOOL: Zoological Collections of the Department of Life Science, National Chung Hsing University, Taichung, Taiwan; ULLZ: University of Louisiana at Lafayette Zoological Collection, USA; ZRC: Zoological Reference Collection of the Lee Kong Chian Natural History Museum (formerly Raffles Museum of Biodiversity Research). N = number of sequences used; “-” = absence of sequences.
SpeciesLocalityCatalogue NumberGenBank Accession NumbersReference Numbers
16S (N)COI (N)
Ocypode quadrata Fabricius, 1787USA, Georgia, Jekyll IslandULLZ 4261FN539018 (1)-[37]
USA, VirginiaUSNM IZ 1287556-KU905799 (1)unpublished
Mexico, Veracruz--KY568733; KY568753-KY568756 (5)[21]
Panama, Bocas del ToroULLZ 13411MK971527 (1)MN184090 (1)[38]
CCDB 3562-OR354404 (1)present study
French GuianaMZUSP 21560-OR354405 (1)present study
Brazil, Amapá (AP), CalçoeneCCDB 5409OR352135-OR352137 (3)OR354406-OR354409 (4)present study
-MG805792-MG805798 (7)-[6]
Brazil, Pará (PA), Ajuruteua-MG805700-MG805707 (8)-[6]
-MG805698, MG805699 (2)-
Brazil, Caeará (CE), CaucaiaCCDB 4506OR352138 (1)OR354410, OR354411 (2)present study
Brazil, Rio Grande do Norte (RN), ParnamirimCCDB 3395OR352139 (1)OR354412 (1)present study
Brazil, Rio Grande do Norte (RN), Tabatinga-MG805713-MG805721 (9)-6
Brazil, Rio Grande do Norte (RN), Tibau do SulCCDB 5559-OR354413, OR354414, OR355675 (3)present study
Brazil, Rio Grande do Norte (RN), NatalCCDB 5422-OR354426 (1)present study
Brazil, Paraíba (PB), Intermares-MG805728-MG805730 (3)-[6]
Brazil, Pernambuco (PE), IpojucaCCDB 5733OR352140, KT279697 (2)OR354415 (1)present study, [39]
CCDB 2926OR352141 (1)OR354416 (1)present study
Brazil, Fernando de Noronha (FN-PE), Conceição-MG805687-MG805696 (10)-[6]
Brazil, Alagoas (AL), Barra do CamaragibeCCDB 4225, CCDB 5409-OR354417 (1)present study
Brazil, Alagoas (AL), JequiáCCDB 2966OR352142 (1)OR355676 (1)present study
Brazil, Alagoas (AL)NCHUZOOL 14920LC150368 (1)LC150423 (1)[1]
Brazil, Sergipe (SE), Atalaia MG805722-MG805726 (5)-[6]
Brazil, Bahia (BA), Canavieiras MG805751 (1)-[6]
Brazil, Bahia (BA), Forte MG805750, MG805782-MG805784 (3)-[6]
Brazil, Bahia (BA), ItacimirimCCDB 2189, CCDB 2190OR352144, OR352145, OR352147 (3)OR354422, OR354423, OR354427 (3)present study
Brazil, Bahia (BA), Lauro de FreitasCCDB 3797-OR354424 (1)present study
Brazil, Bahia (BA), PradoCCDB 4264-OR354420, OR354421 (2)present study
Brazil, Bahia (BA), Mata de São JoãoCCDB 6126OR352146 (1)OR354425 (1)present study
Brazil, Bahia (BA), SalvadorCCDB 1016OR352143 (1)OR354419 (1)present study
Brazil, Espírito Santo (ES), MarataízesCCDB 3973-OR354418 (1)present study
Brazil, Espírito Santo (ES), Setiba Pina-MG805727 (1)-[6]
Brazil, Rio de Janeiro (RJ), Bananal-MG805753-MG805761 (9)-[6]
Brazil, Rio de Janeiro (RJ), Restinga da Marambaia-MG805785 (1)-
Brazil, São Paulo (SP), Ilha CompridaCCDB 3677OR352148, OR352149 (2)OR354428, OR354429, MT623344 (3)present study, [40]
Brazil, São Paulo (SP), RegistroCCDB 3186OR352150 (1)OR354430, OR355677, MT623342 (3)present study, [40]
Brazil, São Paulo (SP), UbatubaCCDB 5087-OR354431, MT623343 (2)present study, [40]
Brazil, São Paulo (SP), UbatubaCCDB 1926KU313182 (1)KU313197 (1)[40]
Brazil, Santa Catarina (SC), FlorianópolisUFRGS 1859-OR354432, OR354433 (2)present study
MZUSP 25171-OR354434 (1)present study
Brazil, Santa Catarina (SC), Praia de Ubatuba-MG805665-MG805674 (10)-[6]
Sister Groups
Ocypode africana De Man, 1881LiberiaSMF 9823LC150354LC150409[1]
Ocypode ceratophthalmus (Pallas, 1772)Taiwan, TainanNCHUZOOL 14916LC150355LC150410
Ocypode macrocera H. Milne Edwards, 1837India, Tamil, NadiZRCLC150361LC150416
Ocypode nobilii De Man, 1902Malaysia, KuchingNCHUZOOL 14918LC150362LC150417
Ocypode cordimana Latreille, 1818GuamNCHUZOOL 14917LC150358LC150413
Ocypode gaudichaudii H. Milne Edwards & Lucas, 1843Panama, CulebraZRCLC150359LC150414
Ocypode kuhlii De Haan, 1835Christmas I.ZRCLC150360LC150415
Ocypode occidentalis Stimpson, 1860Costa RicaZRC 2012.0125LC150365LC150420
Ocypode rotundata Miers, 1882IranSMF 40586LC150369LC150424
Ocypode ryderi Kingsley, 1880Mozambique, InharrimeZRCLC150370LC150425
Ocypode sinensis Dai & Yang in Song & Yang, 1985Taiwan, PingtungNCHUZOOL 14806LC150372LC150427
Ocypode stimpsoni Ortmann, 1897Taiwan, HsinchuNCHUZOOL 14921LC150373LC150428
Outgroup
Afruca tangeri (Eydoux, 1835)Spain, Puerto de Santa Maria, CadizNCHUZOOL 13585AB813666AB813682[1]
Table 2. Ocypode quadrata (Fabricius, 1787). The genetic divergence matrix (distance values are in percentages) obtained by the pairwise distance method of the partial sequences of the COI gene between localities.
Table 2. Ocypode quadrata (Fabricius, 1787). The genetic divergence matrix (distance values are in percentages) obtained by the pairwise distance method of the partial sequences of the COI gene between localities.
1234567891011121314
1USA
2Mexico0.6
3Panama11.011.3
4French Guiana13.413.63.5
5Brazil—Amapá11.511.80.63.1
6Brazil—Ceará10.711.01.44.21.7
7Brazil—Rio Grande do Norte11.511.80.73.30.41.8
8Brazil—Pernambuco11.712.00.93.51.01.91.1
9Brazil—Alagoas11.411.70.83.40.61.30.81.3
10Brazil—Bahia11.611.90.93.70.81.91.01.31.2
11Brazil—Espírito Santo11.511.80.53.00.11.60.40.90.50.7
12Brazil—São Paulo11.912.10.93.60.62.00.91.41.11.20.6
13Brazil—Santa Catarina11.411.70.73.40.61.70.70.90.91.00.51.0
14Sister Group15.916.117.919.718.217.918.118.218.318.218.218.518.0
Table 3. Ocypode quadrata (Fabricius, 1787). The genetic divergence matrix (distance values are in percentages) obtained by the pairwise distance method of the partial sequences of the 16S gene between localities.
Table 3. Ocypode quadrata (Fabricius, 1787). The genetic divergence matrix (distance values are in percentages) obtained by the pairwise distance method of the partial sequences of the 16S gene between localities.
1234567891011121314151617
1USA
2Panama3.7
3Brazil—Amapá3.70.1
4Brazil—Pará3.80.20.3
5Brazil—Ceará6.42.52.62.7
6Brazil—Rio Grande do Norte3.70.10.20.32.6
7Brazil—Fernando de Noronha3.70.00.10.22.50.1
8Brazil—Paraíba3.70.00.10.22.50.10.0
9Brazil—Pernambuco3.90.30.40.52.80.40.30.3
10Brazil—Alagoas3.70.00.30.42.50.30.20.20.4
11Brazil—Sergipe3.80.20.20.32.60.20.20.20.40.3
12Brazil—Bahia3.70.10.10.32.50.20.10.10.40.20.2
13Brazil—Espírito Santo3.70.00.10.22.50.10.00.00.30.20.20.1
14Brazil—Rio de Janeiro3.70.10.10.32.50.10.10.10.40.20.20.10.1
15Brazil—São Paulo3.80.10.20.42.60.20.20.10.50.20.30.20.10.2
16Brazil—Santa Catarina3.80.10.20.32.50.20.10.10.40.30.20.20.10.10.2
17Sister Group9.510.010.110.212.810.110.110.110.49.910.210.110.110.110.210.1
Table 4. Ocypode quadrata (Fabricius, 1787). Values of the number of sequences (N), number of haplotypes (nHap), number of segregating sites (S), nucleotide diversity (π), average number of nucleotide differences (k), and haplotype diversity (Hd) of the COI and 16S genes.
Table 4. Ocypode quadrata (Fabricius, 1787). Values of the number of sequences (N), number of haplotypes (nHap), number of segregating sites (S), nucleotide diversity (π), average number of nucleotide differences (k), and haplotype diversity (Hd) of the COI and 16S genes.
NhSπkHd
COI45331210.037320.8530.9707
16S8924530.011085.2430.6014
Table 5. Ocypode quadrata (Fabricius, 1787). Results of the analysis of molecular variance (AMOVA) and pairwise fixation index (FST).
Table 5. Ocypode quadrata (Fabricius, 1787). Results of the analysis of molecular variance (AMOVA) and pairwise fixation index (FST).
dfVariance ComponentsPercentage of VariationFixation Index
COI
Among populations120.04141 8.46FST = 0.08463
Within populations320.44792 91.54
Total440.48933
16S
Among populations150.009143.03FST = 0.03032
Within populations730.2923196.97
Total880.30146
Table 6. Ocypode quadrata (Fabricius, 1787). The matrix of significant FST and p values, with a significance level of 0.05.
Table 6. Ocypode quadrata (Fabricius, 1787). The matrix of significant FST and p values, with a significance level of 0.05.
COI
FST (p value)Amapá, BrazilCeará, BrazilBahia, Brazil
Mexico-0. 28571 (0.04861)-
Ceará, Brazil--0.27150 (0.04415)
São Paulo, Brazil0. 22239 (0.01317)0.27150 (0.04811)-
16S
FST (p value)Fernando de Noronha, Brazil
Pará, Brazil0.22374 (0.99990)
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Tamburus, A.F.; Miranda, I.; Naves, B.B.; Mantelatto, F.L. Phylogeography of a Widely Distributed Atlantic Species: The Case of the Ghost Crab Ocypode quadrata (Fabricius, 1787) (Decapoda: Brachyura: Ocypodidae). Arthropoda 2024, 2, 130-148. https://doi.org/10.3390/arthropoda2020010

AMA Style

Tamburus AF, Miranda I, Naves BB, Mantelatto FL. Phylogeography of a Widely Distributed Atlantic Species: The Case of the Ghost Crab Ocypode quadrata (Fabricius, 1787) (Decapoda: Brachyura: Ocypodidae). Arthropoda. 2024; 2(2):130-148. https://doi.org/10.3390/arthropoda2020010

Chicago/Turabian Style

Tamburus, Ana Francisca, Ivana Miranda, Bárbara Benati Naves, and Fernando Luis Mantelatto. 2024. "Phylogeography of a Widely Distributed Atlantic Species: The Case of the Ghost Crab Ocypode quadrata (Fabricius, 1787) (Decapoda: Brachyura: Ocypodidae)" Arthropoda 2, no. 2: 130-148. https://doi.org/10.3390/arthropoda2020010

APA Style

Tamburus, A. F., Miranda, I., Naves, B. B., & Mantelatto, F. L. (2024). Phylogeography of a Widely Distributed Atlantic Species: The Case of the Ghost Crab Ocypode quadrata (Fabricius, 1787) (Decapoda: Brachyura: Ocypodidae). Arthropoda, 2(2), 130-148. https://doi.org/10.3390/arthropoda2020010

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