Skip to main content
SpringerLink
Log in

High chromosomal evolutionary dynamics in sleeper gobies (Eleotridae) and notes on disruptive biological factors in Gobiiformes karyotypes (Osteichthyes, Teleostei)

  • Research Paper
  • Published:
Marine Life Science & Technology Aims and scope Submit manuscript

Abstract

The order Gobiiformes is made up of more than 2200 species, representing one of the most diverse groups among teleost fishes. The biological causes for the tachytelic karyotype evolution of the gobies have not yet been fully studied. Here we expanded cytogenetic data for the Eleotridae family, analyzing the neotropical species Dormitator maculatus, Eleotris pisonis, Erotelis smaragdus, and Guavina guavina. In addition, a meta-analytical approach was followed for elucidating the karyotype diversification versus biological aspects (habitat and egg type) of the Gobiiformes. The species E. smaragdus and E. pisonis present 2n = 46 acrocentric chromosomes (NF = 46), D. maculatus 2n = 46 (36sm + 4st + 6a; NF = 86), and G. guavina, the most divergent karyotype, with 2n = 52 acrocentric chromosomes (NF = 52). Besides numeric and structural diversification in the karyotypes, the mapping of rDNAs and microsatellites also showed noticeable numerical and positional variation, supporting the high chromosomal evolutionary dynamism of these species. In Gobiiformes, karyotype patterns which are more divergent from the basal karyotype (2n = 46a) are associated with characteristics less effective to dispersion, such as the benthic habit. These adaptive characteristics, connected with the organization of the repetitive DNA content in the chromosomes, likely play a synergistic role in the remarkable karyotype diversification of this group.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2

Similar content being viewed by others

References

  • Amores A, Giles V, Thode G (1990) Adaptive character of a Robertsonian fusion in chromosomes of the fish Gobius paganellus (Pisces, Perciformes). Heredity 65:151–155

    Article  Google Scholar 

  • Arai R (2011) Fish karyotypes: a check list. Springer, Japan

    Book  Google Scholar 

  • Arai R, Sawada Y (1974) Chromosomes of Japanese gobioid fishes. Bull Natl Sci Mus [Tokyo] 17:97–102

    Google Scholar 

  • Araújo WC, Martínez PA, Molina WF (2010) Mapping of ribosomal DNA by FISH, EcoRI digestion and replication bands in the cardinalfish Apogon americanus (Perciformes). Cytologia 75:109–117

    Article  Google Scholar 

  • Ayala D, Acevedo P, Pombi M, Dia I, Boccolini D, Costantini C, Simard F, Fontenille D (2017) Chromosome inversions and ecological plasticity in the main African malaria mosquitoes. Evolution 71:686–701

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Baensch HA, Riehl R (1991) Aquarien Atlas. Band. 3. Melle: Mergus, Verlag für Natur-und Heimtierkunde, Germany, p 992

  • Berg P, Star B, Pampoulie C, Sodeland M, Barth JMI, Knutsen H, Jakobsen KS, Jentoft S (2016) Three chromosomal rearrangements promote genomic divergence between migratory and stationary ecotypes of Atlantic cod. Sci Rep 6:23246

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Berg P, Star B, Pampoulie C, Bradbury IR, Bentzen P, Hutchings JA, Jentoft S, Jakobsen KS (2017) Trans-oceanic genomic divergence of Atlantic cod ecotypes is associated with large inversions. Heredity 119:418–428

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Betancur-R R, Broughton RE, Wiley EO, Carpenter K, Lopez JA, Li C, Holcroft NI, Arcila D, Sanciangco M, Cureton JC II, Zhang F, Buser T, Campbell MA, Ballesteros JA, Roa-Varon A, Willis S, Borden WC, Rowley T, Reneau PC, Hough DJ et al (2013) The tree of life and a new classification of bony fishes. PLoS Curr 5:ecurrents.tol.53ba26640df0ccaee75bb165c8c26288

    PubMed  PubMed Central  Google Scholar 

  • Betancur-R R, Wiley EO, Arratia G, Acero A, Bailly N, Miya M, Lecointre G, Orti G (2017) Phylogenetic classification of bony fishes. BMC Evol Biol 17:162

    Article  PubMed  PubMed Central  Google Scholar 

  • Caputo V, Marchegiani F, Sorice M, Olmo E (1997) Heterochromatin heterogeneity and chromosome variability in four species of gobiid fishes (Perciformes: Gobiidae). Cytogenet Cell Genet 79:266–271

    Article  CAS  PubMed  Google Scholar 

  • Caputo V, Caniglia ML, Machella N (1999) The chromosomal complement of Aphia minuta, a paedomorphic goby. J Fish Biol 55:455–458

    Google Scholar 

  • Ene AC (2003) Chromosomal polymorphism in the goby Neogobius eurycephalus (Perciformes: Gobiidae). Mar Biol 142:583–588

    Article  CAS  Google Scholar 

  • Eschmeyer WN, Fong JD (2020) Species by family/subfamily. http://researcharchive.calacademy.org/research/ichthyology/catalog/SpeciesByFamily.asp. Accessed 30 Jun 2020.

  • Fanta E (1997) Behaviour and circadian rhythm of the fish Bathygobius soporator Valenciennes (Gobiidae) under the influence of environmental salinity and temperature. Rev Bras Zool 1:221–244

    Article  Google Scholar 

  • Faria R, Johannesson K, Butlin RK, Westram AM (2019) Evolving inversions. Trends Ecol Evol 34:239–248

    Article  PubMed  Google Scholar 

  • Galetti PM Jr, Aguilar CT, Molina WF (2000) An overview of marine fish cytogenetics. Hydrobiologia 420:55–62

    Article  Google Scholar 

  • Galván-Quesada S, Doadrio I, Alda F, Perdices A, Reina RG, Varela MG, Hernández N, Mendoza AC, Bermingham E, Domínguez-Domínguez O (2016) Molecular phylogeny and biogeography of the amphidromous fish genus Dormitator Gill 1861 (Teleostei: Eleotridae). PLoS ONE 11:e0153538

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Giovannotti M, La Mesa M, Caputo V (2009) Life style and genetic variation in teleosts: the case of pelagic (Aphia minuta) and benthic (Gobius niger) gobies (Perciformes: Gobiidae). Mar Biol 156:239–252

    Article  Google Scholar 

  • Gold JR, Li C, Shipley NS, Powers PK (1990) Improved methods for working with fish chromosomes with a review of metaphase chromosome banding. J Fish Biol 37:563–575

    Article  Google Scholar 

  • Gornung E (2013) Twenty years of physical mapping of major ribosomal RNA genes across the teleosts: a review of research. Cytogenet Genome Res 141:90–102

    Article  CAS  PubMed  Google Scholar 

  • Grigoryan KA, Vasiliev VP (1993) Karyotypes of five species of goby (Gobiidae) from the basins of the Black and Caspian seas. J Ichthyol 33:137–143

    Google Scholar 

  • Howell WM, Black DA (1980) Controlled silver staining of nucleolus organizer region with protective colloidal developer: a 1-step method. Experientia 36:1014–1015

    Article  CAS  PubMed  Google Scholar 

  • Kess T, Bentzen P, Lehnert SJ, Sylvester EVA, Lien S, Kent MP, Sinclair-Waters M, Morris C, Wringe B, Fairweather R, Bradbury IR (2020) Modular chromosome rearrangements reveal parallel and nonparallel adaptation in a marine fish. Ecol Evol 10:638–653

    Article  PubMed  PubMed Central  Google Scholar 

  • Kirubakaran TG, Grove H, Kent MP, Sandve SR, Baranski M, Nome T, De Rosa MC, Righino B, Johansen T, Otterå H, Sonesson A, Lien S, Andersen Ø (2016) Two adjacent inversions maintain genomic differentiation between migratory and stationary eco-types of Atlantic cod. Mol Ecol 25:2130–2143

    Article  CAS  PubMed  Google Scholar 

  • Kottelat M, Freyhof J (2007) Handbook of European freshwater fishes. Publications Kottelat, Cornol and Freyhof, Berlin, p 646

    Google Scholar 

  • Kubat Z, Hobza R, Vyskot B, Kejnovsky E (2008) Microsatellite accumulation on the Y chromosome in Silene latifolia. Genome 51:350–356

    Article  CAS  PubMed  Google Scholar 

  • Levan A, Fredga K, Sandeberg AA (1964) Nomenclature for centromeric position on chromosomes. Heredity 52:201–220

    Article  Google Scholar 

  • Lima-Filho PA, Cioffi MB, Bertollo LAC, Molina WF (2012) Chromosomal and morphological divergences in Atlantic populations of the frillfin goby Bathygobius soporator (Gobiidae, Perciformes). J Exp Mar Biol Ecol 434:63–70

    Article  Google Scholar 

  • Lima-Filho PA, Bertollo LAC, Cioffi MB, Costa GWWF, Molina WF (2014a) Karyotype divergence and spreading of 5S rDNA sequences between genomes of two species: darter and emerald gobies (Ctenogobius, Gobiidae). Cytogenet Genome Res 3:197–203

    Article  Google Scholar 

  • Lima-Filho PA, Amorim KDJ, Cioffi MB, Bertollo LAC, Molina WF (2014b) Chromosomal mapping of repetitive DNAs in Gobionellus oceanicus and G. stomatus (Gobiidae; Perciformes): a shared XX/XY system and an unusual distribution of 5S rDNA sites on the Y chromosome. Cytogenet Genome Res 144:333–340

    Article  PubMed  Google Scholar 

  • Lima-Filho PA, Rosa RS, Souza AS, Costa GWWF, Oliveira C, Molina WF (2016) Evolutionary diversification of Western Atlantic Bathygobius species based on cytogenetic, morphologic and DNA barcode data. Rev Fish Biol Fisher 26:109–121

    Article  Google Scholar 

  • Maldonado-Monroy MC, Uribe-Alcocer M, Arreguin-Espinosa J, Castro-Perez A (1985) Karyological studies on Dormitator maculatus Bloch and Gobiomorus dormitor Lacépède (Gobiidae: Perciformes). Cytologia 50:663–669

    Article  Google Scholar 

  • Molina WF (2005) Intraspecific karyotypical diversity in brackish water fishes of the Eleotridae family (Pisces, Perciformes). Cytologia 70:39–45

    Article  Google Scholar 

  • Molina WF, Alves DEO, Araújo WC, Martinez PA, Silva MFM, Costa GWWF (2010) Performance of human immunostimulating agents in the improvement of fish cytogenetic preparations. Genet Mol Res 9:1807–1814

    Article  CAS  PubMed  Google Scholar 

  • Molina WF, Martinez PA, Bertollo LAC, Bidau CJ (2014a) Evidence for meiotic drive as an explanation for karyotype changes in fishes. Mar Genomics 15:29–34

    Article  PubMed  Google Scholar 

  • Molina WF, Martinez PA, Bertollo LAC, Bidau CJ (2014b) Preferential accumulation of sex and Bs chromosomes in biarmed karyotypes by meiotic drive and rates of chromosomal changes in fishes. An Acad Bras Ciênc 86:1801–1812

    Article  PubMed  Google Scholar 

  • Motta-Neto CC, Cioffi MB, Costa GWWF, Amorim KDJ, Bertollo LAC, Artoni RF, Molina WF (2019) Overview on karyotype stasis in Atlantic grunts (Eupercaria, Haemulidae) and the evolutionary extensions for other marine fish groups. Front Mar Sci 6:628

    Article  Google Scholar 

  • Muus BJ, Nielsen JG (1999) Sea fish. Scandinavian Fishing Year Book, Hedehusene, p 340

    Google Scholar 

  • Nakashima Y, Kuwamura T, Yogo Y (1996) Both-ways sex change in monogamous coral gobies, Gobiodon spp. Environ Biol Fishes 3:281–288

    Article  Google Scholar 

  • Nelson JS, Grande TC, Wilson MVH (2016) Fishes of the world, 5th edn. Wiley, Hoboken, p 752

    Book  Google Scholar 

  • Nishikawa S, Amaoka K, Nakanishi K (1974) A comparative study of chromosomes of twelve species of gobioid fishes in Japan. Jpn J Ichthyol 21:61–71

    Google Scholar 

  • Ocalewicz K, Sapota MR (2011) Cytogenetic characteristics of the round goby Neogobius melanostomus (Pallas, 1814) (Teleostei: Gobiidae: Benthophilinae). Mar Biol Res 7:195–201

    Article  Google Scholar 

  • Oliveira C, Almeida-Toledo LF (2006) Evidence of an XX/XY sex chromosome system in the fish Dormitator maculatus (Teleostei, Eleotrididae). Genet Mol Biol 4:635–655

    Google Scholar 

  • Oliveira EJ, Pádua JG, Zucchi MI, Vencovsky R, Vieira MLC (2006) Origin, evolution and genome distribution of microsatellites. Genet Mol Biol 29:294–307

    Article  CAS  Google Scholar 

  • Oto Y, Nakamura M, Murakami H, Masuda R (2017) Inconsistency between salinity preference and habitat salinity in euryhaline gobiid fishes in the Isazu River, northern Kyoto Prefecture. J Ethol 35:203–211

    Article  Google Scholar 

  • Patzner RA, Tassell JLV, Kovacic M, Kapoor BG (2012) The biology of gobies. CRC Press, Taylor & Francis Group, New York

    Google Scholar 

  • Pearse DE, Miller MR, Abadía-Cardoso A, Garza JC (2014) Rapid parallel evolution of standing variation in a single, complex, genomic region is associated with life history in steelhead/rainbow trout. Proc R Soc B 281:20140012

    Article  PubMed  PubMed Central  Google Scholar 

  • Pendás AM, Morán P, García-Vázquez E (1994) Organization and chromosomal location of the major histone cluster in brown trout, Atlantic salmon and rainbow trout. Chromosoma 103:147–152

    Article  PubMed  Google Scholar 

  • Pezold F (1984) Evidence for multiple sex chromosomes in the freshwater goby, Gobionellus shufeldti (Pisces: Gobiidae). Copeia 1984:235–238

    Article  Google Scholar 

  • Prazdnikov DV, Vasil’ev VP, Vasil’eva ED (2013) Polymorphism and interpopulation variability of karyotype of Caspian bighead goby Neogobius gorlap (Gobiidae, Perciformes). J Ichthyol 53:425–430

    Article  Google Scholar 

  • Rocha LA, Robertson DR, Rocha CR, Van-Tassell JL, Craig MT, Bowen BW (2005) Recent invasion of the tropical Atlantic by an Indo-Pacific coral reef fish. Mol Ecol 14:3921–3928

    Article  PubMed  Google Scholar 

  • Ruber L, Vantassell JL, Zardoya R (2003) Rapid speciation and ecological divergence in the American seven-spined gobies (Gobiidae, Gobiosomatini) inferred from a molecular phylogeny. Evolution 57:1584–1598

    Article  PubMed  Google Scholar 

  • Schweizer D (1976) Reverse fluorescent chromosome banding with chromomycin and DAPI. Chromosome 58:307–224

    Article  CAS  Google Scholar 

  • Skóra K, Olenin S, Gollasch S (1999) Neogobius melanostomus (Pallas, 1811) In: Gollasch S, Michin D, Rosenthal H, Voight M (eds) Exotics across the ocean. Case histories on introduced species: their general biology, distribution, range expansion and impact: prepared by members of the European Union Concerted Action on testing monitoring systems for risk assessment of harmful introductions by ships to European waters (MAS-CT-97-0111), Department of Fishery Biology, Institute for Marine Science, University of Kiel, Germany, pp 69–73

  • Sumner AT (1972) A simple technique for demonstrating centromeric heterochromatin. Exp Cell Res 75:304–306

    Article  CAS  PubMed  Google Scholar 

  • Suzuki T (1996) Hypseleotris cyprinoides. In: Fisheries Agency of Japan (ed) Basic data on rare Japanese wild aquatic species. (III). Nihonsuisanshigenhogokyokai, Tokyo, pp 215–221.

  • Suzuki T, Shibukawa K, Senou H, Chen I (2015) Redescription of Rhinogobius similis Gill 1859 (Gobiidae: Gobionellinae), the type species of the genus Rhinogobius Gill 1859, with designation of the neotype. Ichthyol Res 63:227–238

    Article  Google Scholar 

  • Thacker CE (2003) Molecular phylogeny of the gobioid fishes (Teleostei: Perciformes: Gobioidei). Mol Phylogenet Evol 26:354–368

    Article  CAS  PubMed  Google Scholar 

  • Thacker CE (2009) Phylogeny of Gobioidei and placement within Acanthomorpha, with a new classification and investigation of diversification and character evolution. Copeia 2009:93–104

    Article  Google Scholar 

  • Thode G, Martinez G, Ruiz JL, Lopez JR (1988) A complex chromosomal polymorphism in Gobius fallax (Gobiidae, Perciformes). Genetica 76:65–71

    Article  Google Scholar 

  • Uribe-Alcocer M, Diaz-Jaimes P (1996) Chromosome complements of Gobionellus microdon and Eleotris picta collected in México. J Fish Biol 48:796–798

    Google Scholar 

  • Uribe-Alcocer M, Ramirez-Escamilla A (1989) Comparacion citogenetica entre las especies del genero Dormitator (Pisces: Gobiidae). An Inst Cienc del Mary Limnol Univ Nal Auton México 16:75–80

    Google Scholar 

  • Uribe-Alcocer M, Espinosa JA, Padilla AT, Pérez AC (1983) Los cromosomas de Dormitator latifrons (Pisces: Gobiidae). An Inst Cienc del Mary Limnol Univ Nal Auton México 10:23–30

    Google Scholar 

  • Vasilev VP, Grigoryan KA (1994) Chromosome polymorphism and karyological relationships in the group of gobies Neogobius cephalarges Pallas-Neogobius platyrostris Pallas (Gobiidae). Russ J Genet 30:1251–1259

    Google Scholar 

  • Webb CJ (1986) Karyology of the Indo-Pacific Parioglossus raoi (Herre) (Teleostei: Gobioidei) from Fiji. Mar Freshwater Res 37:347–351

    Article  Google Scholar 

  • Wellenreuther M, Bernatchez L (2018) Eco-evolutionary genomics of chromosomal inversions. Trends Ecol Evol 33:427–440

    Article  PubMed  Google Scholar 

  • White TJ, Bruns TD, Lee S, Taylor J (1990) Amplification and direct sequencing of fungal ribosomal RNA genes for phylogenetics. In: Innis MA, Gelfand DH, Sninsky JJ, White TJ (eds) PCR protocols, a guide to methods and applications. Academic Press, San Diego, pp 315–322

    Google Scholar 

  • Xu D, Molina WF, Yano CF, Zhang Y, De OEA, Lou B, Cioffi MB (2017) Comparative cytogenetics in three sciaenid species (Teleostei, Perciformes): evidence of interspecific chromosomal diversification. Mol Cytogenet 10:37

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Yu X, Zhou T, Li K, Zhou M (1987) On the karyosystematics of cyprinid fishes and a summary of fish chromosome studies in China. Genetica 72:225–235

    Article  Google Scholar 

Download references

Acknowledgements

The authors thank to the ICMBio/SISBIO (#19135-4) for the authorization in collecting specimens. We are also grateful to Dr. José Garcia Júnior for the taxonomic identification of specimens utilized in the study. This work was supported by the Conselho Nacional de Desenvolvimento Cient.ico e Tecnol.gico (CNPq) [#442664/2015-0; #442626/2019-3].

Author information

Authors and Affiliations

  1. Departamento de Biologia Celular e Genética, Centro de Biociências, Universidade Federal do Rio Grande do Norte, Natal, RN, 59.078-970, Brazil

    Simião Alefe Soares da Silva, Clóvis Coutinho da Motta-Neto, Gideão Wagner Werneck Félix da Costa & Wagner Franco Molina

  2. Instituto Federal de Ciência e Tecnologia do Rio Grande do Norte, Santa Cruz, RN, 59200-000, Brazil

    Paulo Augusto de Lima-Filho

  3. Departamento de Genética e Evolução, Universidade Federal de São Carlos, Rodovia Washington Luís, Km 235, São Carlos, SP, 13.565-905, Brazil

    Marcelo de Bello Cioffi & Luiz Antônio Carlos Bertollo

Authors
  1. Simião Alefe Soares da Silva
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Paulo Augusto de Lima-Filho
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Clóvis Coutinho da Motta-Neto
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Gideão Wagner Werneck Félix da Costa
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Marcelo de Bello Cioffi
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Luiz Antônio Carlos Bertollo
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Wagner Franco Molina
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

SASS: conceptualization, methodology, writing- original draft preparation, data curation. WFM: conceptualization, methodology, writing- original draft preparation, funding acquisition, project administration, writing—reviewing and editing. GWWFC: investigation, validation. PAL-F, CCM-N: supervision, visualization. MBC, LACB: writing—reviewing and editing.

Corresponding author

Correspondence to Wagner Franco Molina.

Ethics declarations

Conflict of interest

The authors declare that they have no conflict of interest.

Animal and human rights statement

The experimental work fulfilled all ethical guidelines regarding the handling of specimens. The experiments followed ethical and anesthesia conducts in accordance with the Ethics Committee on the Use of Animals (#044/2015) at the Federal University of Rio Grande do Norte (UFRN). The procedures used in this study adhere to the tenets of the Declaration of Helsinki.

Additional information

Edited by Jiamei Li.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

da Silva, S.A.S., de Lima-Filho, P.A., da Motta-Neto, C.C. et al. High chromosomal evolutionary dynamics in sleeper gobies (Eleotridae) and notes on disruptive biological factors in Gobiiformes karyotypes (Osteichthyes, Teleostei). Mar Life Sci Technol 3, 293–302 (2021). https://doi.org/10.1007/s42995-020-00084-6

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s42995-020-00084-6

Keywords

Search

Navigation