Wider ranges correlate with conserved chromosomes in pelagic jack fish

A comparative cytogenetic study of pelagic jack fishes found that wider geographic distributions were associated with more conservative chromosome structures. Researchers combined new chromosome analyses of four Carangidae species with cytogenetic records for the family and estimates of species’ maximum linear distribution and total occupied area. The authors interpret the pattern as consistent with gene flow among widely connected populations limiting the fixation of chromosomal rearrangements, although the study was comparative and did not directly measure migration or gene flow.

The new cytogenetic data covered the rainbow runner, Elagatis bipinnulata ; greater amberjack, Seriola rivoliana ; golden trevally, Gnathanodon speciosus ; and Florida pompano, Trachinotus carolinus . The rainbow runner and greater amberjack were collected off the São Pedro and São Paulo archipelago in the Meso-Atlantic region, while juvenile golden trevally came from Pacific and Indo-Pacific sources obtained through ornamental-fish traders. Florida pompano were from cultured stock on the coast of Florida.

The four-species sample therefore represented differing origins and sampling conditions rather than a uniform population-level survey across their full ranges. Chromosomes were prepared from anterior kidney tissue after in vivo mitotic stimulation and short-term culture. At least 30 metaphase spreads per individual were examined to establish chromosome number, karyotype structure and fluorescence in situ hybridization results.

Conventional and molecular methods included Giemsa staining, C-banding and Ag-NOR analysis for heterochromatin and nucleolus organizer regions, mithramycin fluorescence with DAPI counterstaining for GC-rich sites, and double-FISH with 18S and 5S ribosomal DNA probes. Chromosome morphology was classified as metacentric, submetacentric, subtelocentric or acrocentric, and the fundamental number, or NF, counted the arms of two-armed chromosomes plus one arm for acrocentric elements. All four species had a diploid chromosome number of 2n = 48, but they differed in chromosome structure.

The rainbow runner and golden trevally each had a karyotype of two subtelocentric and 46 acrocentric chromosomes, giving an NF of 50. Greater amberjack had two submetacentric, two subtelocentric and 44 acrocentric chromosomes, for an NF of 52. Florida pompano had four metacentric, four submetacentric and 40 acrocentric chromosomes and the highest NF among the four, at 56.

The investigators found no differentiated sex chromosomes in the analyzed specimens. These observations show that a conserved chromosome count can coexist with marked variation in centromere position and chromosome-arm structure. The ribosomal DNA patterns were comparatively conserved.

Each species had one prominent Ag-NOR site positioned in heterochromatic and GC-rich regions, and these sites corresponded to 18S rDNA hybridization signals. In the rainbow runner and golden trevally, the regions occurred at the end of the short arms of the large subtelocentric chromosome pair. Greater amberjack had a similarly placed site on its subtelocentric pair, while Florida pompano carried it on a large acrocentric pair.

Each species also had a single 5S rDNA locus that was not syntenic with the 18S site. Its position varied among species, ranging from interstitial or terminal locations to a pericentromeric site on the smallest chromosome pair in golden trevally. The broader literature comparison showed that chromosome number is far more conserved than chromosome morphology across Carangidae.

The assembled database covered 22% of the family’s recognized species and included data published from 1974 through 2021. A diploid number of 48 occurred in 88% of species with available data, while fundamental numbers ranged from 48 to 78. Most differences from that baseline were associated with pericentric inversions, while centric fissions and fusions were comparatively uncommon.

Exceptions included three Carangini species with diploid numbers above 48 and rare Robertsonian fusion states reported in Seriola dumerili and Selene setapinnis . Grouping the available data by tribe revealed a geographic gradient in average chromosome-arm number. Naucratini had an average NF of 51.7, close to the presumed family baseline, and the largest mean distribution measures among the four tribes: 60% of the family’s maximum linear distance and 50% of its maximum occupied area.

Scomberoidini averaged an NF of 52, with corresponding distribution values of 40% and 30%. Carangini averaged 53.4, although that result was strongly influenced by the relatively localized and chromosomally divergent Trachurus species; removing that genus reduced the tribal average to 51.3. Trachinotini had the highest average NF, 54.4, but the lowest mean geographic measures, both 20% of the family maximum.

Statistical analysis supported a negative association between geographic reach and chromosome-arm number. Maximum linear geographic distribution and total occupied area were strongly correlated with one another, with a Pearson coefficient of r = 0.829. NF had a moderate negative correlation with maximum linear distance, r = −0.419, and a stronger negative correlation with occupied area, reported as r = −0.876.

The study noted that occupied area may be less precisely defined than maximum linear distance because its ecological boundaries are less straightforward, whereas the maximum axis offers a simpler measure of potential dispersal. These results describe an association across species and tribes; they do not demonstrate that broader range directly caused chromosome conservation, and the compiled dataset includes heterogeneous cytogenetic and geographic sources. The authors connect the pattern to the population biology of large pelagic fishes, which may combine migratory behavior, planktonic larval stages, broadcast spawning and strong swimming capacity.

Such life histories can sustain movement and gene flow across large oceanic areas, reducing opportunities for chromosome rearrangements to become fixed in separated populations. The new samples also showed gross karyotypic similarity between Caribbean Florida pompano and populations previously reported from southeastern and northeastern Brazil, despite the Amazon and Orinoco river barriers identified in the western Atlantic distribution of Trachinotus . Overall, the study presents preliminary evidence consistent with broad oceanic connectivity being associated with conservative karyotypes in Carangidae, while noting that the family contains many monotypic genera and genera represented by only a few species.

Subject of Research: Comparative cytogenetic diversity and geographic distribution in pelagic Carangidae fishes

Article Title: Comparative cytogenetic patterns in Carangidae fishes in association with their distribution range

Article References: Soares, R. X., Motta Neto, C. C. D., Costa, G. W. W. F. D., Cioffi, M. D. B., Bertollo, L. A. C., Borges, A. T., & Molina, W. F. (2021). Comparative cytogenetic patterns in Carangidae fishes in association with their distribution range. Comparative Cytogenetics, 15(4), 429-445. https://doi.org/10.3897/compcytogen.v15.i4.69638

Image Credits: AI Generated

DOI: 10.3897/CompCytogen.v15.i4.69638

Keywords: Carangidae, pelagic fishes, cytogenetics, chromosome rearrangements, geographic distribution, karyotype evolution, marine biology, ribosomal DNA, gene flow, biogeography, Comparative, cytogenetic