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A remarkable degree of chromosomal conservatism (2n=48, FN=48) has been identified in several families of Perciformes. However, some families exhibit greater karyotypic diversity, although there is still scant information on the Atlantic species. In addition to a review of karyotypic data available for representatives of the suborders Blennioidei and Gobioidei, we have performed chromosomal analyses on Atlantic species of the families Blenniidae, Ophioblennius trinitatis Miranda-Ribeiro, 1919 (2n=46; FN=64) and Scartella cristata (Linnaeus, 1758)(2n=48; FN=50), Labrisomidae, Labrisomus nuchipinnis (Quoy & Gaimard, 1824)(2n=48; FN=50) and Gobiidae, Bathygobius soporator (Valenciennes, 1837)(2n=48; FN=56). Besides variations in chromosome number and karyotype formulas, Ag-NOR sites, albeit unique, were located in different positions and/or chromosome pairs for the species analyzed. On the other hand, the heterochromatic pattern was more conservative, distributed predominantly in the centromeric/pericentromeric regions of the four species. Data already available for Gobiidae, Blenniidae and Labrisomidae show greater intra- and interspecific karyotypic diversification when compared to other groups of Perciformes, where higher uniformity is found for various chromosome characteristics. Evolutionary dynamism displayed by these two families is likely associated with population fractionation resulting from unique biological characteristics, such as lower mobility and/or specific environmental requirements.
Chromosomal evolution, marine fish, Bleniidae, Gobiidae, Labrisomidae
Although karyotypic characteristics for some families of marine fish are already known, information on groups of Perciformes is still significantly disproportionate. Among these, suborders Blennioidei and Gobioidei stand out because of the large number of species they represent.
Suborders Gobioidei, with 2, 121 species, and Blennioidei with 732 species, are spread throughout the tropical zone, typically represented by small specimens with low mobility and the ability to withstand changes in temperature and salinity (
Species of Blennioidei and Gobioidei investigated (e.g. Cataudela et al.1973; Garcia et al.1987;
Cytogenetic data for Blennioidei and Gobioidei (Perciformes).
Suborder/Family | Species | 2n | Karyotype formula | FN | References |
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Blennioidei | |||||
Blenniidae | Aidablennius sphynx | 48 | 4m+4sm+40a | 56 |
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Aidablennius sphynx | 48 | 2st+46a | 50 |
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Atrosalarias fuscus | 48 | 48a | 48 |
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Blennius ocellaris | 48 | 2m+2st+44a | 52 |
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Blennius ponticus | 48 | 16sm+10st+22a | 74 |
|
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Blennius yatabei | 48 | 6sm+12st+30a | 66 |
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Coryphoblennius galerita | 48 | 2m+12sm+34a | 62 | Garcia et al. (1973) | |
Dasson trossulus | 40 | 8m+32st/a | 48 |
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Istiblennius enoshimae | 48 | 2m+46a | 50 |
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Istiblennius lineatus | 48 | 48st/a | 48 |
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Lipophrys canevai | 48 | 8st+40a | 56 |
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Lipophrys pholis | 46 | 8m+8sm+30a | 62 |
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Lipophrys trigloides | 46 | 4m+4sm+10st+28a | 64 |
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Lipophrys trigloides | 48 | 2m+6sm+18st+22a | 74 |
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Lipophrys trigloides | 48 | 2m+22sm+2st+22a | 74 |
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Lipophrys trigloides | 48 | 2m+6sm+18st+22a | 74 |
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Omobranchus elegans | 42 | 10m+2sm+6st+24a | 60 |
|
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Omobranchus punctatus | 44 | 4m+40a | 48 |
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Ophioblennius trinitatis | 46 | 6m+12st+28a | 64 | Present study | |
Parablennius incognitus (= Blennius incognitus) | 48 | 4st+44a | 52 |
|
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Parablennius pilicornis (= Blennius pilicornis) | 48 | 8st+40a | 56 |
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Parablennius gattorugine | 48 | 2m+4sm+42a | 54 |
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Parablennius pilicornis | 48 | 48a | 48 |
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Parablennius sanguinolentus | 48 | 12st+36a | 60 |
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Parablennius sanguinolentus | 48 | 20sm+10st+18a | 78 |
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Parablennius tentacularis | 48 | 48st/a | 48 |
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Parablennius tentacularis | 48 | 1st+47a | 49 |
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Parablennius tentacularis | 47 | 1sm+46a | 48 |
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Salaria fluviatilis | 48 | 48st/a | 48 |
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Salaria pavo | 48 | 8st+40a | 56 |
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Salaria pavo | 48 | 16sm+14st+18a | 78 |
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Salaria pavo | 48 | 2st+46a | 50 | Vasil’ev (1980) | |
Salarias faciatus | 48 | 48a | 48 |
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Salarias luctuosus | 48 | 48st/a | 48 |
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Scartella cristata (= Blennius cristatus) | 48 | 2st+46a | 50 |
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Scartella cristata | 48 | 2sm+46st/a | 50 |
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Scartella cristata | 48 | 4st+44a | 52 | Present study | |
Gobioidei | |||||
Clinidae | Clinithracus argentatus | 48 | 2st+46a | 50 |
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Labrisomidae | Labrisomus nuchipinnis | 48 | 2sm+46a | 50 |
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Labrisomus nuchipinnis | 48 | 2st+46a | 50 | Present study | |
Eleotridae | Dormitator latifrons | 46 | 44m/sm+2st/a | 90 |
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Dormitator maculatus | 46 | 34m/sm+12st/a | 80 |
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Dormitator maculatus | 46 | 40m/sm+6st/a | 86 |
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Dormitator maculatus | 46 | 14m+28sm+2st+2a(♀) 13m+28sm+3st+2a(♂) | 90 |
|
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Eleotrioides strigatus | 44 | 2m+42st/a | 46 |
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Eleotris acanthopomus | 46 | 46st/a | 46 |
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Eleotris picta | 52 | 52a | 52 |
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Eleotris pisonis | 46 | 2m/sm+42st/a | 46 |
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Eleotris pisonis | 46 | 46a | 46 |
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Eleotris pisonis | 46 | 46a | 46 |
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Eleotris muralis | 46 | 46a | 46 |
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Mogurnda mogurnda | 46 | 6sm+40st/a | 52 |
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Mogurnda obscura | 62 | - | - |
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Ophiocara porocephala | 48 | 48a | 48 |
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Oxyeleotris marmorata | 46 | 2m+2sm+42a | 50 |
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Gobiidae | Aboma latipes | 40 | 40a | 40 |
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Acanthogobius flavimanus | 44 | 44st/a | 44 |
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Acanthogobius flavimanus | 44 | 36st+8a | 80 | Arai and Kobayashi (1973) | |
Acanthogobius flavimanus | 44 | 10m/sm/st+34a | 54 |
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Acentrogobius pflaumi | 50 | 48m/sm+2st/a | 98 |
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Amblygobius albimaculatus | 44 | 2m+42st/a | 46 |
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Aphia minuta | 44 | 44a | 44 |
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Aphia minuta | 43 | 42a+1st | 42 |
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Aphia minuta | 42 | 1m+1st+40a | 44 |
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Aphia minuta | 42 | 1M+1m+40a | 44 |
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Aphia minuta | 41 | 2M+1st+38a | 44 |
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Apocryptes bato | 46 | 24m+10sm+12a | 80 |
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Apocryptes lanceolatus | 38 | 14m+22sm+2st | 76 |
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Awaous grammepomus | 46 | 46st/a | 46 |
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Awaous tajasica | 46 | 46a | 46 |
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Bathygobius fuscus | 48 | 48a | 48 |
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Bathygobius soporator | 48 | 2m+46a | 50 | Brum et al. (1996) | |
Bathygobius soporator | 48 | 2m/sm+46a | 50 | Cipriano et al. (2002) | |
Bathygobius soporator | 48 | 2m+6st+40a | 56 | Present study | |
Bathygobius stellatus | 46 | 2st+44a | 48 |
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Bathygobius stellatus | 47 | 1sm+2st+43a | 49 |
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Boleophthalmus boddaerty | 46 | 46m/sm | 92 | Subrahmanyan (1969) | |
Boleophthalmus glaucus | 46 | 12m+20sm+2st+12a | 80 |
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Boleophthalmus pectinirostrus | 46 | 46st/a | 46 |
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Bostrichthys sinensis | 48 | 4m/sm+44a | 52 |
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Chaenogobius annularis | 44 | 18sm+26st/a | 62 |
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Chaenogobius annularis | 44 | 36m/sm+8a | 80 |
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Chaenogobius annularis | 44 | 44a | 44 |
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Chaenogobius castaneus | 44 | 36m/sm/st+8a | 80 |
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Chaenogobius isaza | 44 | 12sm+32st/a | 56 |
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Chaenogobius urotaenia | 44 | - | - |
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Chaenogobius urotaenia | 42 | 14sm+28a | 56 |
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Chasmichthys dolichognatus | 44 | 44st/a | 44 |
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Chaenogobius gulosus | 44 | 44st/a | 44 |
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Chaenogobius gulosus | 44 | 16m/sm/st+28a | 60 |
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Ctenogobius criniger | 50 | 34m/sm+6st+10a | 90 |
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Gillichthys mirabilis | 44 | 12sm+32a | 56 |
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Gillichthys seta | 44 | 6m+14sm+24a | 64 |
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Glossogobius fasciatopunctatus | 44 | 10m+28sm+2st+4a | 84 |
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Glossogobius giuris | 46 | 46a | 46 |
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Gobiodon citrinus | 44 | 2m+42st/a | 46 |
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Gobiodon citrinus | 43 | 1m+42st/a | 44 |
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Gobiodon quinquestrigatus | 44 | 44a | 44 |
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Gobiodon rivulatus | 44 | 44a | 44 |
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Gobioides rubicundus | 46 | 2m+26sm+10st+8a | 84 |
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Gobionellus shufeldti | 48 | 48a (♀) | 48 |
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Gobionellus shufeldti | 47 | 46a+1m (♂) | 48 |
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Gobiosoma macrodon | 38 | 38a | 38 |
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Gobiosoma zebrella | 38 | 38a | 38 |
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Gobius abei | 46 | - | - |
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Gobius bucchichi | 44 | 2sm+42a | 46 |
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Gobius cobitis | 46 | 46a | 46 |
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Gobius cruentatus | 46 | 2st+44a | 48 |
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Gobius fallax | 38 | 8m/sm+30a | 46 |
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Gobius fallax | 39 | 7m/sm+32a | 46 |
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Gobius fallax | 40 | 6m/sm+34a | 46 |
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Gobius fallax | 40 | 7m/sm+33a | 47 |
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Gobius fallax | 41 | 5m/sm+36a | 46 |
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Gobius fallax | 42 | 4m/sm+38a | 46 |
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Gobius fallax | 43 | 3m/sm+40a | 46 |
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Gobius niger | 52 | 2m+4sm+16st+30a | 74 |
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Gobius niger | 51 | 3m+4sm+16st+28a | 74 |
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Gobius niger | 50 | 4m+4sm+16st+26a | 74 |
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Gobius niger | 49 | 5m+4sm+16st+24a | 74 |
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Gobius paganellus | 48 | 2sm+46a | 50 |
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Gobius similis | 44 | ? |
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Gobiusculus flavescens | 46 | 6m/sm+40a | 52 |
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Luciogobius grandis | 44 | ? |
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Luciogobius guttatus | 44 | ? | Arai and Kobayashi (1973) | ||
Mesogobius batrachocephalus | 30 | 16m+14a | 46 |
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Neogobius cephalarges | 46 | 46a | 46 |
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Neogobius constructor | 42 | 4m/sm+38a | 46 |
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Neogobius cyrius | 36 | structural polymorphism |
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Neogobius fluviatilis | 46 | 46a | 46 |
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Neogobius eurycephalus | 32 | 12m+2sm+18a | 46 |
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Neogobius eurycephalus | 31 | 13m+2sm+16a | 46 |
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Neogobius eurycephalus | 30 | 14m+2sm+14a | 46 |
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Neogobius gymnotrachelus | 46 | 46a | 46 |
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Neogobius kessleri | 46 | 46a | 46 |
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Neogobius melanostomus | 46 | 46a | 46 |
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Neogobius rhodionovi | 46 | 46a | 46 |
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Odontamblyops rubicundus | 46 | 4m+16sm+26st/a | 66 |
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Padogobius martensi | 46 | 1m+3sm+2st+40a | 52 |
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Parioglossus raoi | 46 | 46st/a | 46 |
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Periophthalmus cantonensis | 46 | 18m+12sm+16st/a | 76 |
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Pomatoschistus lozanoi | 37 | 3m+12sm+10st+12a | 62 | Webb (1980) | |
Pomatoschistus microps | 46 | 4m+16sm+20st+6a | 86 |
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Pomatoschistus minutus | 46 | 4m+16sm+16st+10a | 82 |
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Pomatoschistus minutus | 46 | 18sm+18st+10a | 82 |
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Pomatoschistus norvegicus | 32 | 10m+10sm+8st+4a | 60 | Webb (1980) | |
Pomatoschistus pictus | 46 | 22m/sm+12st+12a | 80 |
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Proterorhinus marmoratus | 46 | 46a | 46 |
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Pterogobius elapoides | 44 | 14sm+30st | 88 | Arai and Kobayashi (1973) | |
Pterogobius zonoleucus | 44 | 14sm+30st | 88 |
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Quietula guaymasiae | 42 | 6m+4sm+32a | 52 |
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Quietula y-cauda | 42 | 42a | 42 |
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Rhinogobius brunneus | 44 | 44a | 44 |
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Rhinogobius flumineus | 44 | 44a | 44 | Arai and Kobayashi (1973) | |
Rhinogobius giurinus | 44 | 44a | 44 |
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Rhodoniichthys laevis | 42 | 16m/sm+26st | 84 |
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Sicyopterus japonicus | 44 | 10m+10sm+24a | 64 |
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Synechogobius hasta | 44 | 2m+42st/a | 46 |
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Tridentiger obscurus | 44 | 10m/sm+34a | 54 |
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Tridentiger trigonocephalus | 44 | 28m/sm/st+16a | 72 |
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Tridentiger trigonocephalus | 46 | 16sm+6st+24a | 68 |
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Trypauchen vagina | 46 | 12m+6sm+10st+18a | 74 |
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Tukugobius flumineus | 44 | 44a | 44 |
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Zosterisessor ophiocephalus (= Gobius ophiocephalus) | 46 | 46a | 46 |
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Zosterisessor ophiocephalus (= Gobius ophiocephalus) | 45 | 1st+45a | 47 |
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Zosterisessor ophiocephalus | 46 | 2m/sm+44a | 48 |
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The present study focuses on the karyotypic characterization of some Atlantic species of the families Blenniidae, Ophioblennius trinitatis Miranda-Ribeiro, 1919 and Scartella cristata (Linnaeus, 1758), Labrisomidae, Labrisomus nuchipinnis (Quoy & Gaimard, 1824)and Gobiidae, Bathygobius soporator (Valenciennes, 1837), through conventional chromosomal analysis, characterization of nucleolar organizer regions (Ag-NORs) and the distribution pattern of C-positive heterochromatin (C-banding) in chromosomes, discussing evolutionary aspects.
Material and methodsA total of 25 specimens of Ophioblennius trinitatis (7♂, 4♀ and 14 indeterminate), 11 specimens of Scartella cristata (4♂, 5♀ and 2 indeterminate), 13 specimens of Labrisomus nuchipinnis (4♂, 4♀ and 5 indeterminate) and 12 specimens of Bathygobius soporator, (5♂, 5♀ and 2 indeterminate) were used for chromosome analysis. Ophioblennius trinitatis specimens came from the coast of Rio Grande do Norte (5°13'1.73"S; 35°9'57.85"W), northeastern Brazil (n=1), and the Saint Peter and Saint Paul (n=8) (00°55'02"N; 29°20'42"W) and Fernando de Noronha (n=16) (3°52'11"S; 32°26'13"W) archipelagos. The remaining specimens were collected on the coast of Rio Grande do Norte. Individuals were previously submitted to mitotic stimulation with compound attenuated antigens, for 24 to 48 hours (Molina 2001, Molina et al. 2010), anesthetized with clove oil (Eugenol) and sacrificed for the removal of anterior kidney fragments. Sexing of specimens was performed by macroscopic and microscopic examination of the gonads. Chromosome preparations were obtained from kidney cells (
Metaphase preparations were examined and photographed on an Olympus BX50 photomicroscope, using an Olympus DP70 digital camera system. Chromosomes were classified according to the position of the centromere in metacentrics (m), submetacentrics (sm), subtelocentrics (st) and acrocentrics (a) (
Ophioblennius trinitatisshowed 2n=46, with a chromosome formula equal to 6m+12st+28a (FN=64), irrespective of sex. Although chromosomes showed a gradual decline in size, the smallest acrocentric pairs corresponded to approximately one-third of the largest metacentric pairs. Nucleolar organizer regions are located in the terminal portions of the short arm on pair 9, the smallest subtelocentric pair. C-positive heterochromatin is discretely located in the centromeric/pericentromeric region of the chromosomes (Fig. 1a, b).
Karyotypes underGiemsa staining a, c, e, g and C-banding b, d, f, h of Ophioblenius trinitatis; a, b Scartella cristata; c, d Labrisomus nuchipinnis; e, f and Bathygobius soporator; g, h Ag-NOR-bearing chromosome pairs are highlighted.
Scartella cristata showed 2n=48 chromosomes, with a chromosome formula equal to 4st+44a (FN=52). The karyotype also displays a gradual reduction in chromosome size. However, the largest chromosome pair exhibits only double the size in relation to the smallest karyotype pair. Ribosomal sites are located on the terminal portions of the short arms on chromosome pair 1. C-positive heterochromatin is also reduced and located in the centromeric regions of chromosomes (Fig. 1c, d).
Cytogenetic analyses of Labrisomidae and Gobiidae species (Gobioidei)Labrisomus nuchipinnis (Labrisomidae) showed 2n=48 chromosomes with a chromosome formula of 2st+46a (FN=50), showing relatively more differentiated size between the largest and smallest chromosomes of the karyotype. Nucleolar organizer regions are in the terminal portions of the long arms on pair 2, corresponding to the largest pair of acrocentric chromosomes. C-positive heterochromatin was showed in the centromeric/pericentromeric region of all chromosome pairs, in relatively conspicuous blocks (Fig. 1e, f).
Bathygobius soporator (Gobiidae) also displayed the karyotype composed of 2n=48 chromosomes, but with the chromosome formula distinct from that of Labrisomus nuchipinnis, specifically, 2m+6st+40a (FN=56). Size difference between the largest and smallest chromosomes of the karyotype was far less pronounced. Ribosomal sites were on the terminal portions of the short arms on chromosome pair 4. C-banding showed discrete heterochromatic regions in the centromeric regions of most chromosomes and telomeric regions of some acrocentric pairs (Fig. 1g, h).
DiscussionThough many perciform families display a conserved karyotype pattern, with 2n=48 acrocentric chromosomes, some groups demonstrate dynamic tendencies in relation to chromosome evolution (Molina 2007). Much of identifiable chromosome diversity is attributed to pericentric inversions, the most common mechanism of chromosome evolution in this order (
Representatives of the suborder Blennioidei (e.g.,
Within the Blennioidei, the Blenniidae, a monophyletic family, is divided into six tribes including Salariini and Parablenniini which, in turn, include the Atlantic species Ophioblennius trinitatis and Scartella cristata respectively (
In spite of displaying relative diversity in chromosome structure, only 18.5% of Blennioidei species exhibit differences in the basal diploid number, 2n=48 chromosomes. As shown in table 1, diploid numbers for representatives of this suborder vary between 2n=40, found in Dasson trossulus (Jordan & Snyder, 1902)(
In contrast to Blennioidei, suborder Gobioidei shows much more dynamic karyotype evolution, demonstrating highly variable karyotype patterns, where the diploid number ranges from 2n=30 for Neogobius eurycephalus (Kessler, 1874) (
Among chromosome rearrangements involved in karyotypic differentiation of Gobiidae, Robertsonian fusions stand out, and are likely the most common event in this group (
Location and frequency of Ag-NOR sites are efficient cytotaxonomic markers in many groups of fish (
Ag-NOR phenotypes a–f described in species of Gobiidae. Ag-NORs sites described in the karyotypes of Gobiidae species were found a in the telomeric region on the short arm of a single pair of acrocentric chromosomes b in the telomeric region on the long arm of a single pair of acrocentrics c in the interstitial/pericentromeric region on the long arm of a single pair of acrocentric chromosomes d in the telomeric region on the short arm of a single subtelocentric pair e in the interstitial/pericentromeric region on the long arm of a single metacentric pair and f in the telomeric regions on the short arms of two acrocentric chromosome pairs.
Few data are available on ribosomal sites for Labrisomidae. Ag-NORs in Labrisomus nuchipinnis exhibit the phenotype (b) described above, in addition to both species of Blenniidae, Ophioblennius trinitatis and Scartella cristata, which may suggest an ancestral condition for this location.
In contrast, other chromosome characteristics, such as C-positive heterochromatin distribution, may be more conserved. This occurs in several species of Percifomes where discrete blocks are preferentially located in the centromeric/pericentromeric regions of chromosomes (Molina 2007). This pattern is repeated in Scartella cristata, Ophioblennius trinitatis and Labrisomus nuchipinnis, as well as in some Gobiidae, such as Gobius cobitis, Zosterisessor ophiocephalus and Neogobius eurycephalus (e.g.
Moreover, karyotypic diversity present in Gobioidei is increased by the occurrence of chromosome polymorphisms frequently observed in this group. This is particularly evident in several examples of intraspecific karyotypic variability, as well as polymorphisms involving different types of chromosome rearrangements, such as in Gobius niger (
In fact, karyotypic diversity among Blennioidei and Gobioidei seems to accompany phyletic diversification of these groups. This is a result of vicariant factors (
We are grateful to the National Council of Technological and Scientific Development (CNPq) for its financial support (Project 556793/2009-9) and to José Garcia Júnior for taxonomic identification of species.