Cytogenetic profiles of two circumglobal snake mackerel species (Scombriformes: Gempylidae) from deep waters of the São Pedro and São Paulo Archipelago

Glaicon de Sousa Santos¹ , Gideão Wagner Werneck Félix da Costa¹, Marcelo de Bello Cioffi², Luiz Antonio Carlos Bertollo², Karlla Danielle Jorge Amorim¹, Rodrigo Xavier Soares¹ and Wagner Franco Molina¹

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Abstract​

Introduction​

Deep-sea regions constitute the largest habitat of the planet (Haedrich, 1996; Hobday et al., 2011), and are the home of the most abundant vertebrates on the Earth, the mesopelagic fishes (Kaartvedt et al., 2012; Proud et al., 2018). Eco-evolutionary studies have shown that genomic signatures are associated with fish adaptation to depth environments (Gaither et al., 2018). However, although mesopelagic species may provide important models for differentiation and adaptation processes in deep waters, very little is still known about their life history, mainly due to the inaccessibility that such marine regions offer (Caiger et al., 2021).

Scombriformes are among the fish groups with remarkable diversification and specialization in mesopelagic or deep environments. They comprise the suborders Scombroidei and Stromateoidei, and three families for the former: Gempylidae, Trichiuridae, and Scombridae (Miya et al., 2013). Gempylidae, the snake mackerels, includes 16 genera and 26 species (Fricke et al., 2024). They are usually large and fast meso- and bento-pelagic predators (Nelson et al., 2016), and can be found in the tropical and subtropical zones of all oceans, at depths from 200 to 500 m (Nakamura, Parin, 1993).

Some Atlantic snake mackerels have a circumtropical occurrence, such as the oilfish Ruvettus pretiosus Cocco, 1833, a benthopelagic species that reach up to three meters in length and has a high commercial value (Viana et al., 2012). The species occurs in tropical, subtropical and temperate waters of all oceans, at depths of 100 to 1,500 m (Nakamura, Parin, 1993). Another species, the Roudi escolar Promethichthys prometheus (Cuvier, 1832), is distributed in tropical and warm temperate waters, at continental slopes around oceanic islands and submarine rises, at depths from 100 to 800 m (Schneider, 1990; Lorenzo, Pajuelo, 1999). Both species perform daily vertical migration, moving to shallower waters at night in search of food (Nakamura, Parin, 1993).

Phylogeographic and population aspects of Gempylidae are still largely unknown, but some studies indicate that they can achieve genetic homogenization even between distantly situated regions (Hüne et al., 2021). Despite increasing chromosomal data among marine fish, large gaps remain for pelagic (Soares et al., 2021) and mesopelagic species (Molina et al., 2024), among which the Atlantic Gempylidae species are included.

Besides to chromosomal diversification at the macrostructural level, the particular organization of repetitive sequences is decisory for understanding the evolutionary trends within a biological group. In eukaryotes, about 20 to 90% of the genome is composed of repetitive sequences (Mehrotra, Goyal, 2014), which include multigene families, mobile elements, and satellite DNAs (Biscotti et al., 2015). Their high dynamic nature (Mehrotra, Goyal, 2014; Garrido-Ramos, 2015) allows for useful biogeographic, phylogenetic, and populational analyses (Vicari et al., 2010; Cioffi et al., 2018; Amorim et al., 2018; Soares et al., 2021; Fernandes et al., 2021).

In this study we aimed to improve the knowledge of evolutionary processes within mesopelagic ecosystems, using Gempylidae fish as a model. Thus, it was performed the first cytogenetic-evolutionary investigation in two Atlantic species, R. pretiosus and P. prometheus, using conventional analyses, staining with base-specific fluorochromes, and fluorescence in situ hybridization (FISH) of six repetitive DNA sequences, including rDNAs, transposable elements, and microsatellites. These first results already allow us to infer about the chromosomal diversification in Gempylidae species and its correlation with other marine fish.

Material and methods

Cytogenetic analyses were performed on 10 individuals (4 males and 6 females) of Ruvettus pretiosus, and 5 individuals (3 males and 2 females) of Promethichthys prometheus from deep waters of the Brazilian São Pedro and São Paulo archipelago (00º55’15”N 29º20’60”W), in the Mid-Atlantic region (Fig. 1). Mitotic chromosomes were obtained by short-term in vitro culture of kidney tissues (Gold et al., 1990) and by lymphocyte culture (Moorhead et al., 1960). Cell suspensions were dripped on slides covered with a hot water film (60ºC), and stained with a 5% Giemsa solution diluted in phosphate buffer pH 6.8. Chromosomes were also analyzed after C-banding (Sumner, 1972), Silver nitrate impregnation (Howell, Black, 1980), and chromomycin (CMA₃) and 4’-6-diamino-2-phenylindole (DAPI) staining (Schweizer, 1980), to identify the heterochromatin distribution, the nucleolar organizer regions location and the chromosomal GC- and AT-rich regions, respectively.

FIGURE 1| South America map showing the geographic location of the São Pedro and São Paulo Archipelago, and the Gempylidae species analyzed in this study. Scale bar = 10 cm.

Fluorescence in situ hybridization (FISH) was performed using 18S rDNA, 5S rDNA, theretroelement of Xiphophorus 3 (Rex 3) and transposable element (TE) of Oryzias latipes, number 2 (Tol2) as probes. The 5S rDNA (200 base pairs) and 18S rDNA (1400 bp) probes were obtained from the genomic DNA of Rachycentron canadum (Rachycentridae) via PCR, using the primers A 5’-TAC GCC CGA TCT CGT CCG ATC-3’/ B 5’ GAG AGC GCT GGT ATG GCC AGC-3’ (Pendás et al., 1994) and NS1 5’-GTA GTA ATA TGC TTG TCT C-3’ / NS8 5’-TCC GCA GGT TCA CCT ACG GA-3’ (White et al., 1990), respectively. Rex3 and Tol2 probes were obtained via PCR from the amplification of the P. prometheus DNA, using the primers Rex 3 F 5′ – CGG TGA TAA AGG GCA GCC GTC – 3′ and Rex 3 R 5′- TGG CAG ACN GTG GTG GTG – 3’ (Volff et al., 1999, 2000) and 4F 5’ – ATA GCT GAA GCT GCT CTG ATC – 3’ and 4R 5’ – CTC AAT ATG CTT CCT TAG G – 3’ (Kawakami, Shima, 1999). The probes were labeled by nick translation (Roche®, Mannheim, Germany) with digoxigenin-11-dUTP, following the manufacturer’s instructions (Roche®, Mannheim, Germany). The d(CA)₁₅ and d(GA)₁₅ oligonucleotides were directly labeled with Alexa-Fluor 555 (InvitrogenTM, Thermo Fisher Scientific, California, USA), at the 5’ terminal position (Kubat et al., 2008). The FISH protocol was performed according to Pinkel et al. (1986).

The best metaphases were photographed using an Olympus™BX51 epifluorescence microscope, coupled with an Olympus™DP73 digital image capture system (Olympus Corp., Tokyo, Japan). The images were compiled with CellSens v. 1.5 Imaging software (Olympus Corp.). Chromosomes were classified according to their arm ratios (AR) as metacentric (m: AR = 1.00-1.70), submetacentric (sm: AR = 1.71-3.00), subtelocentric (st: AR = 3.01-7.00), and acrocentric (a: AR > 7.01), according to Levan et al. (1964). The number of chromosome arms (Fundamental Number, FN) was obtained considering the m, sm, and st chromosomes with two arms, and the acrocentric ones with only one arm.

Results​

TABLE 1 |

Promethichthys prometheus and R. pretiosus share 2n = 48 chromosomes but differ considerably in their karyotypic formulas. The karyotype of R. pretiosus is composed of 2 submetacentric and 46 acrocentric chromosomes (FN = 50), while P. prometheus has 34 submetacentric, 4 subtelocentric and 10 acrocentric chromosomes (FN = 86) (Fig. 2). The Ag-NOR site is located in the short arms of the only submetacentric pair (pair 1) in R. pretiosus,and the short arm of the sm pair 6 in P. Prometheus.In the two species, the Ag-NORs are associated with conspicuous heterochromatic blocks, which are the only chromosomal regions showing differential fluorescence patterns (CMA₃⁺/DAPI^–). The heterochromatin is also preferentially located in the peri- and centromeric regions of the chromosomes in both species (Fig. 2).

FIGURE 2| Karyotypes of Ruvettus pretiosus and Promethichthys prometheus, under Giemsa staining and C-banding. The Ag-NORs sites and the correspondent CMA⁺/DAPI^– regions are highlighted in the boxes. Scale bar = 5µm.

The 18S rDNA hybridization signals are coincident with the Ag-NORs sites. However, while in R. pretiosus the 18S rDNA has a syntenic arrangement with the 5S in pair 1, in P. prometheus the 18S and 5S rDNAs have an independent location, the first in pair 6 and the second in pair 8 (Fig. 3). Furthermore, (GA)₁₅ and (CA)₁₅ microsatellites, and Tol2 transposable element just have scattered signals on the chromosomes in R. pretiosus and P. prometheus. Rex3 showed scattered signals on the chromosomes in R. pretiosus and P. prometheus besides accumulations in pericentromeric region of chromosome pairs 1, 2, 7, and 12 in P. prometheus (Figs. 3–4).

FIGURE 3| Karyotypes of Ruvettus pretiosus and Promethichthys prometheus showing the distribution of the 18S rDNA (red), 5S rDNA (green) probes, and microsatellites (GA)₁₅ and (CA)₁₅ under fluorescence in situ hybridization. Scale bar = 5 µm.

FIGURE 4| Karyotypes of Ruvettus pretiosus and Promethichthys prometheus showing the distribution of the Tol2 and Rex3 elements in the chromosomes under fluorescence in situ hybridization. Scale bar = 5 µm.

Discussion​

Cytogenetic data have not been described for a significant number of marine fish yet, especially those whose access or management is difficult due to their large size, remote geographic distribution or very specific ecological habitats. All these attributes apply to Gempylidae species, usually living at great ocean depths. Therefore, this study provides the first information about this small and little-studied fish group.

Although sharing the same diploid number, 2n = 48, R. pretiosus and P. prometheus have diversified karyotypic structures. Their chromosomal number is considered a basal trait for Percomorpha fish (Galetti et al., 2000; Motta-Neto et al., 2019), and is also shared by 15 other Scombridae species, a sister family of Gempylidae also belonging to the Scombroidei clade (Arai, 2011; Soares et al., 2013). This symplesiomorphic condition is frequently found among Perciformes (Molina, 2007; Motta-Neto et al., 2019), indicating that other rearrangements, regardless of centric fissions, have played an important role in the karyotypic evolution of this fish group. However, in contrast to other Scombroidei fish, the two analyzed Gempylidae species have a very distinctive FN, because of their divergent karyotypic diversification. Thus, while R. pretiosus has all acrocentric chromosomes, except for a single sm pair (FN = 50), P. prometheus, has almost two-armed chromosomes (FN = 86). Such expressive differentiation is likely due to pericentric inversions, the most frequent chromosomal rearrangements in Percomorpha (Galetti et al., 2006), but not excluding a priori other rearrangements that may have acted in the shuffling of syntenic regions of the chromosomes. Pericentric rearrangements are seen as important tools for local adaptations (Wellenreuther, Bernatchez, 2018), and have been correlated with such processes in several fish groups (Matschiner et al., 2022). Therefore, it is also likely that they are acting in the adaptation of some species of Gempylidae to deep marine environments.

Biological factors, such as their dispersive potential, can influence the karyotypic evolution in marine fishes (Molina, Galetti, 2004; Sena, Molina, 2007; Soares et al., 2021). In fact, the dispersive capacity, including the transposition of geographic barriers (Fernandes et al., 2021), and variable ecological abilities, may minimize the genetic structuring and reduce the fixation of chromosomal rearrangements, while opposite characteristics may facilitate them (Molina, 2007; Motta-Neto et al., 2019). Phylogeographic data are still unavailable to R. pretiosus and P. prometheus, but their diversified karyotypic patterns are apparently in concordance with their dispersive potentials. Phylogenetically, R. pretiosus is a more basal species (Miya et al., 2013), with extensive distribution in tropical, subtropical, and temperate deep waters of all oceans (Nakamura, Parin, 1993), indicating a bigger dispersive potential. Accordingly, it presents a more conserved karyotypic structure. On the other hand, P. prometheus, which is included in a more recent divergent group among the snake mackerels (Miya et al., 2013), and with a circumglobal distribution, but not in the eastern Pacific (Nakamura, Parin, 1993), presents a significantly differentiated karyotype.

The distribution of the rDNA sequences shows that microstructural divergences also occur between the two species. Outstandingly, the 18S and 5S rDNA sites are localized in two different chromosome pairs in P. prometheus, while in R. pretiosus these sequences are localized in the telomeric regions of the same chromosome pair. Although contiguous syntenic arrays have been sporadically reported for some Percomorpha species (Nirchio et al., 2009; Amorim et al., 2016; Motta-Neto et al., 2019), the bi-telomeric rDNA organization is a rare array in marine fish.

In fish, microsatellites are frequently associated with TEs (Costa et al., 2015; Gouveia et al., 2017), and can show highly variable accumulation patterns (Cioffi et al., 2012; Lima-Filho et al., 2014). However, in P. prometheus and R. pretiosus, the (CA)₁₅ and (GA)₁₅ repeats are homogeneously dispersed in chromosomes, with some centromeric and terminal clusters in a few chromosomes. The distributions of the microsatellites repeats and Tol2 elements show no significant differences between both species. Except by the accumulation in few chromosomes of P. prometheus, the Rex3 sequences are disperse on the chromosomes of both species, in contrast with other marine species, in which they are visibly clustered (Ferreira et al., 2011; Costa et al., 2013, 2014, 2015). Despite TEs are recognized as sources of chromosomal instability, favoring karyotypic differentiation (Lonnig, Saedler, 2002; Shao et al., 2019), were not evidenced complex arrays involving the analyzed TEs with repetitive DNA sequences, such rDNA regions, or microsatellites, suggesting their less direct participation on karyotype divergence of these snake mackerel species.

These chromosomal data, now recorded for the first time for Gempylidae, indicate clear macrostructural differences between the two investigated species, in contrast to the conservative trend that occurs in its phylogenetically close and cytogenetically more studied Scombridae family (Soares et al., 2013). It is known that high intrafamilial diversification is a common scenario in some reef fish groups (Molina et al., 2014; Getlekha et al., 2016), but hitherto unknown in deep-sea fish such as Gempylidae.

The vast areas of the Mid-Atlantic Ridge and other global Mid-Oceanic Ridges systems, used as spawning grounds for deep-sea fish, may have a strong influence on their genetic structure (Sutton et al., 2007). In fact, the common strategy of the vertically migrating mesopelagic species in releasing eggs near the surface (Gjøsæter, Tilseth, 1988; Flynn, Paxton, 2012), amplifies their dispersive potential, making them good models for investigating chromosomal evolution in marine environments.

Regions with little to no coverage of mesopelagic fish research include the South Atlantic, large parts of Indo-Pacific region and some polar environments (Caiger et al., 2021). The lack of knowledge of the characteristics of deep pelagic species constitutes a challenge for the conservation of global oceanic biodiversity (Sutton et al., 2017). The cytogenetic patterns and life history of pelagic fish are beginning to be better analyzed. Undoubtedly, this will be an important step towards better understanding our rich biodiversity and its correlation with the environment where it lives.

Acknowledgments​

We thank to the Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq) for the financial support to WFM (#442664/2015–0; #442626/2019–3, and #301458/2019–7), and to ICMBio/SISBIO for the collection authorizations. We also thank the crews of the ships Transmar I and II for the support during collections and José Garcia Júnior for species identification.

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Authors

Glaicon de Sousa Santos¹ , Gideão Wagner Werneck Félix da Costa¹, Marcelo de Bello Cioffi², Luiz Antonio Carlos Bertollo², Karlla Danielle Jorge Amorim¹, Rodrigo Xavier Soares¹ and Wagner Franco Molina¹

^[1]    Departamento de Biologia Celular e Genética, Centro de Biociências, Universidade Federal do Rio Grande do Norte, Campus Universitário, 59078-970 Natal, RN, Brazil. (GSS) glaiconpesca@hotmail.com (corresponding author), (GWWFC) wagnerwf@yahoo.com.br, (KDJA) karlla_danielle@msn.com, (RXS) roxsoares@gmail.com, (WFM) molinawf@yahoo.com.br.

^[2]    Departamento de Genética e Evolução, Universidade Federal de São Carlos, Rod. Washington Luis, km 235, 13565-905 São Carlos, SP, Brazil. (LACB) bertollo@ufscar.br, (MBC) mbcioffi@ufscar.br.

Authors’ Contribution

Glaicon de Sousa Santos: Conceptualization, Investigation, Methodology, Writing-original draft, Writing-review and editing.

Gideão Wagner Werneck Félix da Costa: Formal analysis, Methodology, Writing-review and editing.

Marcelo de Bello Cioffi: Formal analysis, Writing-review and editing.

Luiz Antonio Carlos Bertollo: Formal analysis, Writing-review and editing.

Karlla Danielle Jorge Amorim: Methodology, Writing-review and editing.

Rodrigo Xavier Soares: Formal analysis, Methodology, Writing-review and editing.

Wagner Franco Molina: Conceptualization, Funding acquisition, Project administration, Writing-original draft, Writing-review and editing.

Ethical Statement​

Collections had the authorization of the Instituto Chico Mendes de Conservação da Biodiversidade (ICMBio), Sistema de Autorização e Informação em Biodiversidade (SISBIO Licenses N^o 19135–1, 131360–1 and 27027–2), and Sistema Nacional de Gestão do Patrimônio Genético e do Conhecimento Tradicional Associado (SISGEN). All experiments followed ethical protocols approved by the Animal Ethics Committee of the Universidade Federal do Rio Grande do Norte (Protocol 44/2015).

Competing Interests

The authors no declare competing interests.

How to cite this article

Santos GS, Costa GWWF, Cioffi MB, Bertollo LAC, Amorim KDJ, Soares RX, Molina WF. Cytogenetic profiles of two circumglobal snake mackerel species (Scombriformes: Gempylidae) from deep waters of the São Pedro and São Paulo Archipelago. Neotrop Ichthyol. 2024; 22(2):e220087. https://doi.org/10.1590/1982-0224-2022-0087

Copyright​

This is an open access article under the terms of the Creative Commons Attribution License, which permits use, distribution and reproduction in any medium, provided the original work is properly cited.

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© 2024 The Authors.

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