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Article

Genetic Variability and Connectivity in the Western Mediterranean Populations of the Bathyal Crab Geryon longipes

by
Ariadna Colmenero
1,
Bruna Serra
1,
Clàudia Lagares
1,
Eva Rojo-Francàs
1,
José L. Pérez-Gil
2,
Francesc Mestres
1,* and
Pere Abelló
3,*
1
Departament Genètica, Microbiologia i Estadística and IRBio, Universitat de Barcelona, Av. Diagonal 643, 08028 Barcelona, Spain
2
Centro Oceanográfico de Málaga (CNIEO-CSIC), Puerto Pesquero, 29640 Fuengirola, Spain
3
Institut de Ciències del Mar (ICM-CSIC), Passeig Marítim de la Barceloneta, 37-49, 08003 Barcelona, Spain
*
Authors to whom correspondence should be addressed.
Diversity 2023, 15(4), 534; https://doi.org/10.3390/d15040534
Submission received: 24 February 2023 / Revised: 23 March 2023 / Accepted: 4 April 2023 / Published: 7 April 2023
(This article belongs to the Special Issue Diversity and Ecology of Marine Benthic Communities)
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Abstract

:
Geryon longipes is a crab species that inhabits the muddy bottoms of the middle and lower slopes, as well as bathyal bottoms ranging from 400 to 2000 m in depth. To assess its molecular diversity, a fragment of 572 bp of the COI (Cytochrome Oxidase subunit I) mitochondrial gene was sequenced in eight Western Mediterranean locations. Within the studied area, two oceanographic fronts are present (Almeria-Oran Front and Ibiza Channel). From the 124 sequences obtained, only 7 distinct haplotypes were identified. The population distribution indicated three well-differentiated regions: the Alboran Sea, the Gulf of Vera and the Levantine/Catalan coasts. The molecular diversity was compared with that obtained in the same year for the same gene in Liocarcinus depurator, a crab species that is captured on the continental shelf and upper slope (40 to 500 m). The estimates of molecular diversity parameters for the COI gene fragment were rather similar between both species, but the number of haplotypes was higher for L. depurator. Finally, the obtained COI sequences of G. longipes were compared to those from other populations of the species distribution range, recovered from the DNA repository. Only one additional, different haplotype was reported (Sicily), whereas all the rest were common with those described in our study. Therefore, the COI gene fragment would indicate that all the sequences analysed in the Mediterranean and NE Atlantic belong to the same species, G. longipes.

1. Introduction

There was a time when evolutionary biologists tended to consider that marine organisms would not have major restrictions in their mobility and dispersion since the oceans showed no directly evident physical barriers like those present in the terrestrial environment [1]. As a result, it was assumed that marine organisms could move rather freely in the water mass, leading to a high degree of gene flow and minimal differentiation between populations. However, this assumption was found to be far from reality as marine currents create oceanographic fronts that disrupt the connectivity between populations. As such, in addition to isolation by distance, permanent and semi-permanent oceanic barriers are now recognised as one of the primary factors contributing to population genetic differentiation [2,3,4,5,6]. Nonetheless, the situation is markedly different for deep-sea species, as deep current patterns are poorly understood and the environmental conditions in these regions tend to be relatively stable, except for occasional and local high-energy processes [7]. Deep-sea fronts between water masses and geological deep-sea structures, such as mountain ranges, may create isolation for benthic and epibenthic populations unless the species exhibit epiplanktonic larval stages that allow them to surmount these barriers. Furthermore, although knowledge of deep-sea larval stages is limited, evidence suggests that at least some species have epiplanktonic larval stages that may, depending on their developmental stage, be affected by epipelagic fronts and currents, while later developmental stages are located in deeper waters [8,9].
The Mediterranean Sea is an ideal marine system for studying these essential evolutionary processes due to its rich biodiversity and well-characterised currents and epipelagic oceanographic fronts [6,10,11,12,13,14]. Specifically, on its western basin, the Mediterranean contains four oceanographic barriers of interest: Gibraltar Strait (GS), Almeria-Oran Front (AOF), Ibiza Channel (IC) and Balearic Front (BF). In previous studies, the effect of the first three discontinuities was analysed by using the portunid crab Liocarcinus depurator as a model to study geographic variability of the Cytochrome Oxidase subunit I (COI) gene [15,16]. These studies identified two haplogroups, one from Atlantic-influenced waters and the other predominant in Mediterranean waters. Additionally, it was possible to study its spatial and temporal distribution along different populations of the Atlanto-Mediterranean transition. The GS and AOF were found to be the primary oceanographic discontinuities that differentiated populations with Atlantic or Mediterranean influence. Notably, the strength of the AOF displays significant seasonal and interannual variability that affects connectivity at the population level [17,18].
Building on this knowledge, an interesting evolutionary question arises as to whether we would obtain similar results using a crab species living in a deep-sea environment. L. depurator is a portunid crab dwelling on the continental shelf and upper slope muddy bottoms in the Mediterranean Sea and NE Atlantic, where it is commonly caught as bycatch in demersal trawl fisheries [19,20]. This species is characterised by the occurrence of a relatively long series of epipelagic planktonic larval stages [21,22], which are affected and transported by coastal currents [23]. This mechanism is considered the primary means of population dispersion for the species. To make a comparison, we selected a deep-sea species, the bathyal crab Geryon longipes (Geryonidae), which is also distributed along the Atlantic-Mediterranean transition but differs from L. depurator in that it inhabits much deeper muddy bottoms on the middle and lower continental slope, from around 400 m to 2000 m [24,25,26].
Two species are presently recognised in the genus Geryon, namely G. longipes, distributed in the Mediterranean and adjacent Atlantic waters, and G. trispinosus, present in the Eastern Central Atlantic waters off the northern European coasts [27,28,29,30]. G. longipes is frequently collected from the red shrimp (Aristeus antennatus) fishery, along with other co-occurring species such as the squat lobster Munida tenuimana, polychelid lobsters, and caridean shrimps [19,31]. G. longipes is often commercialised as a demersal trawling bycatch of the red shrimp fishery in the Western Mediterranean ports [32]. While its larval morphology has been described [33], information concerning the depths of its larval occurrence or its behaviour and dispersion is still scarce [34,35]. Concerning other geryonid species, information on this subject is also scarce, but it shows that the first larval stages are also epipelagic [34,36,37] and that early-stage larvae show physiological and behavioural mechanisms that allow them to ascend in the water column, while late stages descend into deep waters [8]. The size-depth relationship reported for juveniles and adults of the closely related species G. trispinosus (but see below) suggests that larval settlement takes place in deeper areas than those at which adult specimens occur [27]. Larval ecology and behaviour may therefore be very different between the continental shelf crab L. depurator and the deep-sea crab G. longipes.
The main aim of this research is to check for possible genetic structuration in the western Mediterranean populations of G. longipes, taking into account the different oceanographic fronts present, by analysing a fragment of the COI mitochondrial gene, equivalent to that previously sequenced in L. depurator. For this genetic marker, its molecular diversity was estimated in G. longipes, and the population distribution of the recorded haplotypes was studied. Since the G. longipes samples were obtained from the same areas where we previously analysed the samples of L. depurator [18], a comparison of the molecular diversity and geographic distribution of haplotypes between both species in the same year was possible. Additionally, COI mitochondrial gene fragments from other alleged G. longipes specimens downloaded from DNA databases were analysed for comparison, and the geographic patterns of all described haplotypes were also analysed.

2. Materials and Methods

2.1. Samples and Sequencing

Samples of G. longipes were collected during the April and May 2016 MEDITS_ES fishery research cruise using a standardised fisheries research bottom trawl gear [38]. The studied populations were: West Alboran (WA), East Alboran (EA), Vera (VE), Ibiza Is. (EI), Alicante (AC), Valencia (VA), Central Catalonia (CC) and North Catalonia (NC) (Figure 1). The precise sampling locations and depths are described in Table 1.
All studied samples were adults, mainly males (85% males and only 15% females), with carapace lengths between 20.7 mm and 71.2 mm (mean = 50.5 ± 9.8 mm). From each crab, a piece of muscular tissue (0.1 g) from a leg (a tissue rich in mitochondria) was preserved in absolute alcohol on board the ship. In the laboratory, DNA was extracted using the Qiagen Puregene® Cell Kit (2 × 108) kit. The Cytochrome Oxidase subunit I (COI) gene fragment was amplified through the universal primers LCO1490 (forward) and HCO2198 (reverse) [39]. PCR reactions were carried out in 20 μL final volume, containing 1 μL sample DNA and 19 μL mix: 12.5 μL H2O, 4 μL buffer X5, 1 μL MgCl2, 0.5 μL dNTPs (1 mM), 0.4 μL primer forward (10 μM), 0.4 μL primer reverse (10 μM) and 0.2 μL Taq polymerase (Go Taq 5 U/μL, Promega). The PCR protocol was 4 min at 94 °C, 30 cycles of 1 min at 94 °C, 1 min at 50 °C, 1 min at 72 °C, and a final extension of 7 min at 72 °C. The resulting PCR products were cleaned with ExoSAP (1.2 U of Exonuclease and 1.2 U of Shrimp Alkaline Phosphatase) in a 2:1 proportion for 15 min at 37 °C. Finally, the samples were dried at 80 °C for 15 min and sent to Serveis Científics i Tecnològics de la Universitat de Barcelona for sequencing.

2.2. Data Analysis

A total of 124 samples were sequenced (Table 1), which were initially aligned and trimmed to obtain a final alignment of 622 bp using the BioEdit v7.2.6.1 [40]. Only one strand was sequenced, and the possible presence of stop codons or indels was checked. However, these sequences were later aligned with those deposited in DNA data repositories (13 in total) to obtain the maximum common fragment for all sequences, which had a length of 572 bp. The description of the downloaded sequences from databases is also shown in Table 1. The haplotype sequences obtained in the present research were deposited in GenBank under accession numbers MK720650–MK720669 and OQ283874–OQ283977. The accession numbers for the sequences downloaded from GenBank were: JQ305902 and JQ305903 (Castellammare del Golfo, Sicily, Italy), JQ306198–JQ306202 (South coast of Portugal), JQ306134 and JQ306135 (SW coast of Portugal) and JQ305968–JQ305970 (NW of St. Kilda, Scotland). The sequence from Nahariyya (Israel) was downloaded from the BOLD database (accession number: BIM369-13.COI-5P BOLD). The number of different haplotypes (h), the number of polymorphic sites (S), the haplotype diversity (Hd) and the nucleotide diversity (π) were computed with the DnaSP v6.12 software [41]. A network of haplotypes was constructed using the Median Joining network algorithm from the Network v5.0.1.1 software [42] and a phylogenetic tree was generated using the Neighbour-Joining method of MEGA X [43]. Moreover, with the Western Mediterranean samples, a comparison between the genetic (GammaST) and geographic distances was carried out. Genetic distances were computed with the DnaSP v6.12 software [41], whereas geographic distances were obtained using the Karto v5.2 software [44], following an isobathic line at 200 m depth. The comparison between the groups of populations was carried out with an AMOVA analysis. The genetic and geographic distance matrices were compared using a Mantel test. Furthermore, a PCoA was carried out with the genetic distances to study the distribution of the Western Mediterranean samples. These computations were carried out using the R package vegan [45].

3. Results

The parameters estimating the molecular diversity for 124 sequences of the studied populations are presented in Table 2. Neither stop codons nor indels were detected. West Alboran and Vera presented the highest values for haplotype and nucleotide diversity, whereas the lowest were recorded at Alicante and North of Catalonia. It is worth comparing the molecular diversity between G. longipes and L. depurator samples in the same localities (West Alboran, East Alboran, Alicante, Valencia and Central Catalonia) collected in 2016 (Table 3).
The values of Hd and π are higher for L. depurator in West Alboran, East Alboran and Alicante, and the opposite result was observed in Valencia and Central Catalonia (although the sample size for L. depurator was rather small). Considering all five populations together, Hd is higher in G. longipes than in L. depurator (0.734 ± 0.024 and 0.592 ± 0.052, respectively), but not for π (0.203 ± 0.011 in G. longipes and 0.300 ± 0.034 in L. depurator). However, the h/n ratio was always higher for L. depurator, considering the five populations separately or together (0.064 for G. longipes and 0.202 for L. depurator). A summary of the molecular diversity parameters, computed for all 137 G. longipes sequences (124 from the present study and 13 from databases), is shown in Table S1. These sequences belonged to eight haplotypes, which were named Glon_1 to Glon_8 (Table S2). They were characterised by 6 polymorphic positions, of which 286 and 367 presented heteroplasmy in different individuals. Positions showing heteroplasmy were not excluded from the computations. The presence of these eight haplotypes in the studied populations is presented in Table 4.
Haplotypes Glon_1, Glon_2, Glon_3 and Glon_7 were frequent, whilst Glon_6 was only found in two populations (East Alboran and Vera) and Glon_4, Glon_5 and Glon_8 were detected only once (the first in Castellamare del Golfo and the other two in Vera). Vera was the population presenting more different haplotypes (five). The haplotype network showing the similarity regarding the sequence of the eight haplotypes and their relative abundance is presented in Figure 2.
This network was rather linear with few ramifications (only two), with Glon_1, Glon_2 and Glon_7 haplotypes being the most frequent. There was only one nucleotide change between Glon_1 and Glon_2 and Glon_1 and Glon_7. The next frequent haplotype was Glon_3, but it was related to Glon_7 through Glon_6. Finally, Glon_4, Glon_5 and Glon_8 were infrequent and located at the tips of the network. The neighbour-joining tree confirmed the resemblances between the sequences of the different haplotypes (Figure 3).
The distribution and abundance of the haplotypes in the Western Mediterranean populations (Figure 4) qualitatively suggests the existence of three different geographic areas or groups of populations: (1) the region with Atlantic water influence (West and East Alboran), represented by the presence of Glon_3 in high frequency; (2) the Levantine/Catalan zone with predominant Mediterranean waters (Alicante, Ibiza Is., Valencia, Central and North Catalonia), in which Glon_1 and Glon_2 were predominant; and (3) Vera population, likely influenced by both Atlantic and Mediterranean waters and presenting five haplotypes: Glon_1 in a frequency similar to that observed in the Levantine/Catalan region; Glon_7, which is found in the Atlantic and most Mediterranean populations; Glon_6, which was also detected in East Alboran; and finally, Glon_5 and Glon_8 detected only in this population and related with Glon_3 by two and three changes, respectively. The obtained results by the AMOVA analysis indicated a significant differentiation between the Alboran Sea populations and those from the Levantine/Catalan zone (p = 0.047). However, no significant differentiation was observed between Vera and the Levantine/Catalan populations (p = 0.217) or between Vera and the Alboran Sea populations (p = 0.667). Interestingly, Glon_1 was detected in all studied Western Mediterranean populations but was most abundant from Vera to North Catalonia and was also found in St. Kilda, Scotland. In all the populations studied in this research, with the exception of Alicante and North Catalonia, the haplotype Glon_7 was rather common and was also reported in St. Kilda. Finally, and also concerning the haplotype distribution, it is remarkable that seven of the eight described haplotypes were detected in our Western Mediterranean populations (Glon_1, Glon_2, Glon_3, Glon_5, Glon_6, Glon_7 and Glon_8). Most important, all sequences from different geographic origins belonged to any of these haplotypes (Table S2), with the only exception of Glon_4, which was only found in Castellamare del Golfo (Sicily); however, this population also presented Glon_2. Thus, the reported haplotypes are usually shared between different populations.
There was a significant correlation between genetic and geographic distances (Mantel test r = 0.473, p = 0.036). The PCoA analysis allowed for a graphical representation of all Western Mediterranean populations (Figure 5). The first and second coordinates explain 98.36% and 1.64% of the variability, respectively. Thus, the first coordinate explains almost all variability. It separates the previously mentioned three areas: the Alboran Sea populations, Vera and the remaining populations. However, in the third group (Alicante, Ibiza Is., Valencia, Central and North Catalonia), populations do not follow a geographic pattern because Alicante and North Catalonia were grouped on the far right of the graph, likely due to the absence of Glon_7 in them.

4. Discussion

For the 572-bp fragment of the G. longipes COI gene analysed, the observed number of polymorphic sites (only 6) was scarce considering all 137 sequences together. Of these positions, 4 presented sporadic substitutions (49, 292, 424 and 496), whereas the other 2 (286 and 367) showed heteroplasmy in many individuals. This heteroplasmy could be produced by a mixture of different mtDNA molecules from the same species in the same individual, an introgression between different species or a simulation of heteroplasmy generated by the presence of Numts (nuclear mitochondrial pseudogenes) [46]. It has been described that Numts are rather common in crustaceans [47,48], and they have been previously reported from G. longipes [49], although this was in a specimen preserved in a museum, and, if preservation in origin has not been optimal, DNA extraction and PCR amplification can yield anomalous results [46]. We hypothesize that in our case, heteroplasmy is a consequence of a mixture of mtDNA molecules belonging to the same species, as we used fresh tissue rich in mitochondria for mtDNA extraction, stop codons have not been detected in any of our sequences, the polymorphic position for heteroplasmy showed high variability among the analysed individuals, and both peaks (for G and A) showed similar height in heteroplasmic individuals, which could likely indicate a current source of species variation.
In the comparison of the same populations (West Alboran, East Alboran, Alicante, Valencia and Central Catalonia) and for the same year (Table 3), L. depurator presented higher molecular variability for the COI gene fragment than G. longipes. Moreover, the global estimates of haplotype and nucleotide diversities obtained for G. longipes (Table S1) were similar but lower than those observed in samples of L. depurator and M. intermedia collected in the same region in other surveys [15]. Furthermore, our values of Hd and π from G. longipes were similar to those obtained from the deep-sea red shrimp Aristeus antennatus (0.624 ± 0.050 and 0.0017 ± 0.0002, respectively). In the latter species, the molecular variability was estimated from both the information provided by a fragment of the COI gene and the S16 subunit gene in 137 shrimps from the Western Mediterranean [50]. It is worth pointing out that G. longipes and A. antennatus widely co-occur on the middle and lower continental shelves in the Mediterranean, and their habitats are therefore highly coincident [51,52]. In summary, the levels of molecular variation detected in the sampled populations of G. longipes would indicate that deep-sea species would present lower genetic diversity than those present in shallower waters, in agreement with [15]. These results provide additional and new information on the relevant topic of the role of depth as an evolutionary factor [53,54].
The haplotype network for G. longipes (Figure 2) showed one main haplotype (Glon_1), together with three other rather abundant haplotypes (Glon_2, Glon_3 and Glon_7), and the four remaining haplotypes being sporadic (Glon_4, Glon_5, Glon_6 and Glon_8). The obtained network is rather lineal, presenting only a couple of ramifications, a pattern not found in other networks generated from the COI fragments in other decapod crustaceans from the study area, such as the hermit crabs Pagurus excavates (shallow-water species) and Pagurus alatus (deep-sea species), the caridean shrimp Plesionika heterocarpus (deep-sea), the penaeid shrimp Parapenaeus longirostris (deep-sea), the portunid crab Macropipus tuberculatus (deep-sea) [15], or in other decapods from European waters, such as the crawfish Palinurus elephas (shallow-water) [4], the crabs Pachygrapsus marmoratus (shallow-water) [55], Carcinus aestuarii (shallow-water) [56], Acanthonyx brevifrons and A. lunulatus (both shallow-water) [57] and the deep-sea red shrimp Aristaeomorpha foliacea (deep-sea) [58].
Although only eight different haplotypes were detected in our study, they showed a particular distribution in the studied Mediterranean populations (Figure 4). Thus, three areas could be defined: the Alboran Sea (West and East), Vera, and Levantine/Catalan area (Alicante, Ibiza, Valencia, Central and North Catalonia). The Alboran Sea populations showed a high frequency of the Glon_3 haplotype, which was absent in the rest of the studied populations. This suggests that the Glon_3 haplotype is characteristic of Atlantic waters since it is present in both the Alboran Sea and Portuguese populations sampled, but it was also found in Israel (Table 4). The case of Vera is particular, with five different haplotypes and a frequency of Glon_1 close to 50%. It could be a population with waters from different origins—the Atlantic and Mediterranean. The remaining populations presented only two haplotypes (Glon_1 and Glon_2), as is the case of Alicante and North Catalonia, or three haplotypes (Glon_1, Glon_2 and Glon_7), with Glon_1 being the most common. These three groupings are corroborated by the results of PCoA (Figure 5). However, the haplotype distribution pattern in L. depurator for the same year was rather different. In this species, two haplogroups (Atlantic and Mediterranean) were well defined [15,16,17,18], and their distribution was likely conditioned by the gene flow mediated by the pattern of currents and the position and intensity of the oceanic fronts [16,17,18]. In 2016, the haplotype distribution of L. depurator showed a clear differentiation between the Western and Eastern Alboran, with the Atlantic haplotype being predominant in Cadiz and West Alboran and the Mediterranean haplotype in the remaining Mediterranean populations (East Alboran, Alicante, Valencia, Ebro Delta and Central Catalonia). It is now well known that the molecular composition of adult L. depurator populations depends on the larval movements in the plankton during the previous year [15,16]. However, there is no distribution and behavioural information on the larval behaviour of G. longipes. A fundamental question arises: whether the molecular differentiation found in our Mediterranean samples is adaptive or not. If it is adaptive, the observed distribution of the haplotypes should be the result of natural selection acting on the larvae, adults or both larvae and adults. These are open questions that deserve more research to be properly answered.
Another remarkable result is the haplotype distribution of the COI fragment in all populations so far sequenced (Table 4). None of the common haplotypes is restricted to particular geographic areas. Furthermore, all the sequences obtained are very similar, with just a few nucleotide changes (Figure 2 and Figure 3). Accordingly, all individuals analysed in this research (137 sequences) would likely belong to the same species. The identification of geryonid crabs based on morphological characters is relatively difficult, as Reference [59] already pointed out, so molecular markers can produce new insights into the taxonomy of this group [60]. From our study of the 572 bp of COI, the three sequences obtained from NE Atlantic individuals (attributed to Geryon trispinosus) belonged to the most common haplotypes present in Mediterranean G. longipes. This result agrees with the remarks reported by Reference [61] and would therefore indicate that the Atlantic individuals examined in the present study would belong to the same species present in the Mediterranean G. longipes. However, the COI fragment used is relatively small, and other regions and additional molecular markers would be useful to fully confirm this conclusion.
Ecologically, larval behaviour is considered the main mechanism of dispersion for populations of benthic and epibenthic species occurring in the marine benthos [62,63]. In particular, larval transport along systems of currents and counter-currents coupled to larval migrations has been particularly suggested as a possible mechanism of larval dispersal for deep-sea geryonid species [8,60]. Thus, migration of ovigerous females to the upper distribution limits of G. trispinosus and its role as a mechanism for larval release to take place at appropriate depth locations to minimise the larval treks to epipelagic waters have been reported [27]. Similarly, Reference [64] showed that large-sized individuals clearly dominated the population present at the upper distribution range of G. longipes.
Our results clearly suggest that there is a need for further comparative studies of population biology patterns, including population genetics and behavioural aspects in deep-sea species. These studies should assess the geographical and temporal patterns that may help to appropriately understand deep marine habitats, providing essential information for their management.

5. Conclusions

The estimates of molecular diversity parameters for the COI gene fragment are similar in G. longipes and L. depurator, although molecular diversity is slightly higher in the latter species. However, the number of haplotypes detected is different for both species. In G. longipes, only eight haplotypes were detected considering both our sequences and those downloaded from the databases. In the Western Mediterranean region and according to the haplotypes for the COI gene fragment, the G. longipes populations were clearly distributed in three major regions: the Alboran Sea, Vera and Levantine/Catalan area. This result can be relevant to properly defining the Marine Protected Areas and for the correct implementation of fishery conservation and management policies. Finally, the COI gene fragment indicated that all sequences obtained in this research and from genetic databases belong to the same species.

Supplementary Materials

The following supporting information can be downloaded at: https://www.mdpi.com/article/10.3390/d15040534/s1, Table S1: Molecular diversity for all G. longipes sequences (124 from the present study and 13 from databases). (n) number of sequences, (h) the number of different haplotypes, (S) the number of polymorphic sites, (Hd) the haplotype diversity with the standard deviation and (π × 100) the nucleotide diversity multiplied by 100, with the standard deviation.; Table S2: Description of the eight haplotypes of G. longipes observed based on their nucleotide composition at the polymorphic sites. All sequences were aligned presenting a total length of 572 bp. Polymorphic sites are referred to as this length.

Author Contributions

Conceptualization, F.M. and P.A.; methodology, F.M. and P.A.; sampling, P.A. and J.L.P.-G.; sequencing, A.C., B.S., C.L. and E.R.-F.; data analysis, A.C., B.S., C.L., E.R.-F. and F.M.; writing—original draft preparation, F.M. and P.A.; writing—review and editing, F.M., P.A., A.C., B.S., C.L., E.R.-F. and J.L.P.-G.; supervision, F.M. and P.A.; the authors A.C., B.S., C.L. and E.R.-F. contributed equally to this research. All authors have read and agreed to the published version of the manuscript.

Funding

This research was funded by MINECO/FEDER (Grant number CTM2015-66-400-C3-3-R) and Project MarGech (PID2020-118550RB-C22), MCIN/AEI/10.13039/501100011033 of the Spanish Government; Generalitat de Catalunya, Spain (Grant number 2021 SGR 01271) and partial support was also provided by the Spanish Government through the “Severo Ochoa Centre of Excellence” accreditation (CEX2019-000928-S) to the Institut de Ciències del Mar (ICM-CSIC).

Institutional Review Board Statement

Not applicable.

Data Availability Statement

The data (DNA sequences) presented in this study are openly available in GenBank. All accession numbers are indicated in the text.

Acknowledgments

We thank all the members of the MEDITS_ES fisheries research cruise for all their help and support. We are mainly grateful to all colleagues and students that directly contributed to the at-sea sampling work. We also thank Owen S. Wagensteen (Universitat de Barcelona) for corrections to the English and Concepció Arenas (Universitat de Barcelona) for her statistical advice.

Conflicts of Interest

The authors declare no conflict of interest.

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Figure 1. Sampling populations of G. longipes (red colour) in the Western Mediterranean area. Populations are identified by the following abbreviations: West Alboran (WA), East Alboran (EA), Vera (VE), Ibiza Is. (EI), Alicante (AC), Valencia (VA), Central Catalonia (CC) and North Catalonia (NC). Dashed black lines identify the location of the main currents and gyres in the studied area. Oceanographic fronts are shown as solid blue lines: Gibraltar Strait (GS), Almeria-Oran Front (AOF) and Ibiza Channel (IC).
Figure 1. Sampling populations of G. longipes (red colour) in the Western Mediterranean area. Populations are identified by the following abbreviations: West Alboran (WA), East Alboran (EA), Vera (VE), Ibiza Is. (EI), Alicante (AC), Valencia (VA), Central Catalonia (CC) and North Catalonia (NC). Dashed black lines identify the location of the main currents and gyres in the studied area. Oceanographic fronts are shown as solid blue lines: Gibraltar Strait (GS), Almeria-Oran Front (AOF) and Ibiza Channel (IC).
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Figure 2. Haplotype network using the eight haplotypes detected in G. longipes. Circle sizes are proportional to the abundance of each haplotype. Transversal small lines in branches indicate one nucleotide change between the connected haplotypes. Colours indicate the origin of the haplotypes: yellow (West Alboran), brown (East Alboran), light green (Vera), pink (Ibiza Is.), blue (Alicante), purple (Valencia), light blue (Central Catalonia), red (North Catalonia), grey (Israel), dark green (Sicily), white (West Portugal), dark blue (South Portugal) and black (Scotland).
Figure 2. Haplotype network using the eight haplotypes detected in G. longipes. Circle sizes are proportional to the abundance of each haplotype. Transversal small lines in branches indicate one nucleotide change between the connected haplotypes. Colours indicate the origin of the haplotypes: yellow (West Alboran), brown (East Alboran), light green (Vera), pink (Ibiza Is.), blue (Alicante), purple (Valencia), light blue (Central Catalonia), red (North Catalonia), grey (Israel), dark green (Sicily), white (West Portugal), dark blue (South Portugal) and black (Scotland).
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Figure 3. Phylogenetic tree for the eight different haplotypes of G. longipes. This result is due to the fact that all the sequences are rather similar.
Figure 3. Phylogenetic tree for the eight different haplotypes of G. longipes. This result is due to the fact that all the sequences are rather similar.
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Figure 4. Frequencies of the haplotypes for each western Mediterranean population. Colours indicate each haplotype: blue (Glon_1), yellow (Glon_2), dark red (Glon_3), dark green (Glon_5), light green (Glon_6), brown (Glon_7) and purple (Glon_8). The abbreviations stand for the following populations: WA (West Alboran), EA (East Alboran), VE (Vera), AC (Alicante), EI (Ibiza Is.), VA (Valencia), CC (Central Catalonia) and NC (North Catalonia).
Figure 4. Frequencies of the haplotypes for each western Mediterranean population. Colours indicate each haplotype: blue (Glon_1), yellow (Glon_2), dark red (Glon_3), dark green (Glon_5), light green (Glon_6), brown (Glon_7) and purple (Glon_8). The abbreviations stand for the following populations: WA (West Alboran), EA (East Alboran), VE (Vera), AC (Alicante), EI (Ibiza Is.), VA (Valencia), CC (Central Catalonia) and NC (North Catalonia).
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Figure 5. Graphical representation of the PCoA. The abbreviations stand for the following populations: WA (West Alboran), EA (East Alboran), VE (Vera), AC (Alicante), EI (Ibiza Is.), VA (Valencia), CC (Central Catalonia) and NC (North Catalonia).
Figure 5. Graphical representation of the PCoA. The abbreviations stand for the following populations: WA (West Alboran), EA (East Alboran), VE (Vera), AC (Alicante), EI (Ibiza Is.), VA (Valencia), CC (Central Catalonia) and NC (North Catalonia).
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Table
Table 1. Population name (with its abbreviation), latitude, longitude, depth (in meters), number of analysed individuals and reference of all populations studied. Information from samples obtained by other researchers is also included.
Table 1. Population name (with its abbreviation), latitude, longitude, depth (in meters), number of analysed individuals and reference of all populations studied. Information from samples obtained by other researchers is also included.
PopulationLatitudeLongitudeDepthnReference
West Alboran (WA)36.312 N4.340 W77015This study
East Alboran (EA)36.581 N2.498 W52814This study
Vera (VE)36.856 N1.759 W71416This study
Ibiza Is. (EI)38.838 N0.842 E68115This study
Alicante (AC)38.069 N0.040 W58116This study
Valencia (VA)39.453 N0.156 E56116This study
Central Catalonia (CC)41.161 N2.358 E66517This study
North Catalonia (NC)41.391 N3.269 E622.515This study
Nahariyya, Israel (IS)33.050 N34.830 E10431Tel Aviv University
Castellammare del Golfo, Sicily (CG)35.730 N14.050 E6052Matzen da Silva et al., 2011
South coast of Portugal (SP)36.600 N 8.030 W7525Matzen da Silva et al., 2011
SW coast of Portugal (WP)37.540 N 9.190 W6122Matzen da Silva et al., 2011
NW of St. Kilda, Scotland (SC)58.170 N 9.000 W6003Matzen da Silva et al., 2011
Table
Table 2. Molecular diversity of the G. longipes populations: West Alboran (WA), East Alboran (EA), Vera (VE), Ibiza Is. (EI), Alicante (AC), Valencia (VA), Central Catalonia (CC) and North Catalonia (NC). (n) number of sequences, (h) the number of different haplotypes, (S) the number of polymorphic sites, (Hd) the haplotype diversity with the standard deviation and (π × 100) the nucleotide diversity multiplied by 100 with the standard deviation.
Table 2. Molecular diversity of the G. longipes populations: West Alboran (WA), East Alboran (EA), Vera (VE), Ibiza Is. (EI), Alicante (AC), Valencia (VA), Central Catalonia (CC) and North Catalonia (NC). (n) number of sequences, (h) the number of different haplotypes, (S) the number of polymorphic sites, (Hd) the haplotype diversity with the standard deviation and (π × 100) the nucleotide diversity multiplied by 100 with the standard deviation.
PopulationnhSHdπ × 100
WA15420.714 ± 0.0810.223 ± 0.020
EA14420.495 ± 0.1510.146 ± 0.044
VE16550.708 ± 0.0940.246 ± 0.065
EI15320.590 ± 0.1060.117 ± 0.027
AC16210.458 ± 0.0950.080 ± 0.017
VA16320.658 ± 0.0750.137 ± 0.024
CC17320.699 ± 0.0490.154 ± 0.020
NC15210.343 ± 0.1280.060 ± 0.022
Table
Table 3. Molecular diversity of the G. longipes and L. depurator populations sampled in 2016: West Alboran (WA), East Alboran (EA), Alicante (AC), Valencia (VA) and Central Catalonia (CC). (n) number of sequences, (h) the number of different haplotypes, (h/n) ratio of different haplotypes to number of sequences, (Hd) the haplotype diversity with the standard deviation and (π × 100) the nucleotide diversity multiplied by 100 with the standard deviation. G. long. and L. dep. stand for Geryon longipes and Liocarcinus depurator, respectively. L. depurator data are from [18].
Table 3. Molecular diversity of the G. longipes and L. depurator populations sampled in 2016: West Alboran (WA), East Alboran (EA), Alicante (AC), Valencia (VA) and Central Catalonia (CC). (n) number of sequences, (h) the number of different haplotypes, (h/n) ratio of different haplotypes to number of sequences, (Hd) the haplotype diversity with the standard deviation and (π × 100) the nucleotide diversity multiplied by 100 with the standard deviation. G. long. and L. dep. stand for Geryon longipes and Liocarcinus depurator, respectively. L. depurator data are from [18].
PopulationSpeciesnhh/nHdπ × 100
WAG. long.1540.2670.714 ± 0.0810.223 ± 0.020
L. dep.24110.4580.815 ± 0.0630.431 ± 0.055
EAG. long.1440.2860.495 ± 0.1510.146 ± 0.044
L. dep.2380.3480.581 ± 0.1200.246 ± 0.075
ACG. long.1620.1250.458 ± 0.0950.080 ± 0.017
L. dep.2570.2800.633 ± 0.1040.301 ± 0.402
VAG. long.1630.1880.658 ± 0.0750.137 ± 0.024
L. dep.4180.1950.316 ± 0.0950.093 ± 0.039
CCG. long.1730.1760.699 ± 0.0490.154 ± 0.020
L. dep.620.3330.333 ± 0.2150.063 ± 0.083
TOTALG. long7850.0640.734 ± 0.0240.203 ± 0.011
L. dep.119240.2020.592 ± 0.0520.300 ± 0.034
Table
Table 4. Distribution of the eight haplotypes detected in G. longipes in the studied populations. The presence of a particular haplotype is indicated by “+” and its absence by “−”. Abbreviations of populations: WA (West Alboran), EA (East Alboran), VE (Vera), EI (Ibiza Is.), AC (Alicante), VA (Valencia), CC (Central Catalonia), NC (North Catalonia), IS (Nahariyya, Israel), CG (Castellammare del Golfo, Sicily), SP (South coast of Portugal), WP (SW coast of Portugal) and SC (NW of St. Kilda, Scotland).
Table 4. Distribution of the eight haplotypes detected in G. longipes in the studied populations. The presence of a particular haplotype is indicated by “+” and its absence by “−”. Abbreviations of populations: WA (West Alboran), EA (East Alboran), VE (Vera), EI (Ibiza Is.), AC (Alicante), VA (Valencia), CC (Central Catalonia), NC (North Catalonia), IS (Nahariyya, Israel), CG (Castellammare del Golfo, Sicily), SP (South coast of Portugal), WP (SW coast of Portugal) and SC (NW of St. Kilda, Scotland).
PopulationHaplotype
Glon_1Glon_2Glon_3Glon_4Glon_5Glon_6Glon_7Glon_8
WA+++−−−+−
EA+−+−−++−
VE+−−−++++
EI++−−−−+−
AC++−−−−−−
VA++−−−−+−
CC++−−−−+−
NC++−−−−−−
IS−−+−−−−−
CG−+−+−−−−
SP−++−−−−−
WP−−+−−−−−
SC++−−−−+−
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Colmenero, A.; Serra, B.; Lagares, C.; Rojo-Francàs, E.; Pérez-Gil, J.L.; Mestres, F.; Abelló, P. Genetic Variability and Connectivity in the Western Mediterranean Populations of the Bathyal Crab Geryon longipes. Diversity 2023, 15, 534. https://doi.org/10.3390/d15040534

AMA Style

Colmenero A, Serra B, Lagares C, Rojo-Francàs E, Pérez-Gil JL, Mestres F, Abelló P. Genetic Variability and Connectivity in the Western Mediterranean Populations of the Bathyal Crab Geryon longipes. Diversity. 2023; 15(4):534. https://doi.org/10.3390/d15040534

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Colmenero, Ariadna, Bruna Serra, Clàudia Lagares, Eva Rojo-Francàs, José L. Pérez-Gil, Francesc Mestres, and Pere Abelló. 2023. "Genetic Variability and Connectivity in the Western Mediterranean Populations of the Bathyal Crab Geryon longipes" Diversity 15, no. 4: 534. https://doi.org/10.3390/d15040534

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