Integrating Cytogenetics and Population Genomics: Allopatry and Neo-Sex Chromosomes May Have Shaped the Genetic Divergence in the Erythrinus erythrinus Species Complex (Teleostei, Characiformes).

Fernando H S De Souza,Thomas Liehr,Marcelo B Cioffi,Francisco De M C Sassi,Luiz A C Bertollo,Tariq Ezaz,Pedro H N Ferreira,Manolo F Perez

doi:10.3390/biology11020315

Fernando H S De Souza, Thomas Liehr + Show 6 more

Open Access

https://doi.org/10.3390/biology11020315

Copy DOI

Abstract

Simple SummaryFish present astonishing diversity, comprising more species than the combined total of all other vertebrates. Here, we integrated cytogenetic and genomic data to investigate how the evolution of multiple sex chromosomes together with allopatry is linked to genetic diversity and speciation in the fish species Erythrinus erythrinus. We hypothesized that the presence of multiple sex chromosomes has contributed to the genetic differentiation of populations, which could have potentially accelerated speciation.Diversity found in Neotropical freshwater fish is remarkable. It can even hinder a proper delimitation of many species, with the wolf fish Erythrinus erythrinus (Teleostei, Characiformes) being a notable example. This nominal species shows remarkable intra-specific variation, with extensive karyotype diversity found among populations in terms of different diploid chromosome numbers (2n), karyotype compositions and sex chromosome systems. Here, we analyzed three distinct populations (one of them cytogenetically investigated for the first time) that differed in terms of their chromosomal features (termed karyomorphs) and by the presence or absence of heteromorphic sex chromosomes. We combined cytogenetics with genomic approaches to investigate how the evolution of multiple sex chromosomes together with allopatry is linked to genetic diversity and speciation. The results indicated the presence of high genetic differentiation among populations both from cytogenetic and genomic aspects, with long-distance allopatry potentially being the main agent of genetic divergence. One population showed a neo-X1X2Y sexual chromosome system and we hypothesize that this system is associated with enhanced inter-population genetic differentiation which could have potentially accelerated speciation compared to the effect of allopatry alone.

Highlights

The biodiversity of Neotropical freshwater fish is remarkable, as they comprise at least5200 species [1]
Such cryptic diversity is at least partially explained by the high karyotypic diversity found in some species, such as E. erythrinus and H. malabaricus, in which many studies have shown the presence of intraspecific variants, with extensive differences observed in the diploid chromosome numbers (2n), karyotype compositions and different sex chromosome systems among populations [4]
We analyzed three distinct populations of E. erythrinus and used genomic approaches to investigate how the evolution of multiple sex chromosomes together with allopatry is linked to genetic diversity and speciation

Summary

Introduction

The biodiversity of Neotropical freshwater fish is remarkable, as they comprise at least5200 species [1]. The family currently contains 18 species that have been described, within three genera: Hoplias (13), Hoplerythrinus (3), and Erythrinus (2) [2]. Some authors have suggested a need for a taxonomic revision [3,4], as all genera display several undescribed morphotypes which are currently included in some nominal species [5]. Such cryptic diversity is at least partially explained by the high karyotypic diversity found in some species, such as E. erythrinus and H. malabaricus, in which many studies have shown the presence of intraspecific variants, with extensive differences observed in the diploid chromosome numbers (2n), karyotype compositions and different sex chromosome systems among populations [4].

Methods

Results

Discussion

Conclusion