Genomic Differences Between the Sexes in a Fish Species Seen Through Satellite DNAs

Neotropical fishes have highly diversified karyotypic and genomic characteristics and present many diverse sex chromosome systems, with various degrees of sex chromosome differentiation. Knowledge on their sex-specific composition and evolution, however, is still limited. Satellite DNAs (satDNAs) are tandemly repeated sequences with pervasive genomic distribution and distinctive evolutionary pathways, and investigating satDNA content might shed light into how genome architecture is organized in fishes and in their sex chromosomes. The present study investigated the satellitome of Megaleporinus elongatus, a freshwater fish with a proposed Z(1)Z(1)Z(2)Z(2)/Z(1)W(1)Z(2)W(2) multiple sex chromosome system that encompasses a highly heterochromatic and differentiated W-1 chromosome. The species satellitome comprises of 140 different satDNA families, including previously isolated sequences and new families found in this study. This diversity is remarkable considering the relatively low proportion that satDNAs generally account for the M. elongatus genome (around only 5%). Differences between the sexes in regards of satDNA content were also evidenced, as these sequences are 14% more abundant in the female genome. The occurrence of sex-biased signatures of satDNA evolution in the species is tightly linked to satellite enrichment associated with W-1 in females. Although both sexes share practically all satDNAs, the overall massive amplification of only a few of them accompanied the W-1 differentiation. We also investigated the expansion and diversification of the two most abundant satDNAs of M. elongatus, MelSat01-36 and MelSat02-26, both highly amplified sequences in W-1 and, in MelSat02-26's case, also harbored by Z(2) and W-2 chromosomes. We compared their occurrences in M. elongatus and the sister species M. macrocephalus (with a standard ZW sex chromosome system) and concluded that both satDNAs have led to the formation of highly amplified arrays in both species; however, they formed species-specific organization on female-restricted sex chromosomes. Our results show how satDNA composition is highly diversified in M. elongatus, in which their accumulation is significantly contributing to W-1 differentiation and not satDNA diversity per se. Also, the evolutionary behavior of these repeats may be associated with genome plasticity and satDNA variability between the sexes and between closely related species, influencing how seemingly homeologous heteromorphic sex chromosomes undergo independent satDNA evolution.

Automated summary

Neotropical fishes have highly diversified karyotypic and genomic characteristics, with varied sex chromosome systems. The study on the satellitome of Megaleporinus elongatus revealed 140 different satDNA families, showing gender-biased differences and significant contributions to sex chromosome differentiation. The highly diversified satDNA composition in M. elongatus influences genome plasticity and evolutionary behavior in sex chromosomes.