Karyotypic Evolution in African Fishes of the Genus Nothobranchius (Cyprinodontiformes)
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1
Severtsov Institute of Ecology and Evolution (RAS), Russia
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2
Department of Biology, Lomonosov Moscow State University, Russia
Species of the genus Nothobranchius live in ephemeral pools in savannah of Eastern Africa and have one of the shortest life cycles among vertebrates. Populations of Nothobranchius can be found in small isolated ponds (Reichard, 2016). This makes them an interesting model for speciation studies. Fishes of the genus Nothobranchius contains 76 valid species. An extremely high karyotype diversity in this genus was revealed. Phylogenetic data based on molecular markers from 46 species demonstrated that the genus Nothobranchius was a monophyletic assemblage and it included four clades (Dorn et al., 2014). In present study we revised phylogenetic tree and analysed cytogenetic data in the context of a phylogenetic reconstruction of the genus.
Individuals of Nothobranchius species were collected either from wild populations of East Africa or provided by killifish hobbyists. Chromosome preparations were made according to the method of Kligerman and Bloom (1977). The chromosome preparations were obtained from anterior kidney tissue. The slides were stained with 2% Giemsa solution. Chromosome morphology was determined according to Levan et al. (1964) and classified as metacentric (m), submetacentric (sm), subtelocentric (st) and acrocentric (a). To determine the fundamental number (NF), chromosomes of the m and sm groups were considered biarmed and those of group st/a uniarmed.
We generated a new phylogeny of Nothobranchius species using a partial sequence of the nuclear genes: glycin transporter 1 (GLYT1), myosin heavy chain 6 (MYH6), SH3 and PX domain containing 3 (SH3PX3), G-protein coupled receptor 85 (GPR85, also known as SREB2) and zic family member 1 (ZIC1). By combining the data from published Nothobranchius datasets (Dorn et al., 2014) with newly generated sequences for 19 species, we obtained a dataset that includes 64 species. Maximum likelihood and Bayesian phylogenetic trees were reconstructed.
Phylogenetic ancestral character state reconstruction of chromosome number was made using ChromEvol (Glick, Meyrose, 2014) and R packages. We estimated the strength of phylogenetic signal for the diploid number based on Pagel’s lambda statistic (Pagel, 1999) and Blomberg’s K statistic (Blomberg et al., 2003), using the “phylosig” function in the R package “phytools”. Correlation between genetic and karyotypic distances was calculated using Mantel test (Mantel, 1967).
We have analysed the karyotypes of 65 Nothobranchius species. The number and morphology of the chromosomes varied greatly. The diploid number of chromosomes ranged from 2n=16 in N. rachovii to 2n=49/50 in N. brieni (males/females). The most frequent diploid numbers were 2n=36 and 2n=38. The analysed karyotypes also had interspecific morphological differences. We have not detected heteromorphic sex chromosomes in the majority of the analysed species. However, in six species (N. guentheri, N. brieni, N. lourensi, N. janpapi, N. ditte, N. thierry) we found an X1X1X2X2/X1X2Y sex chromosome system where males had one chromosome less than females. We suggest that the system of multiple sex chromosomes emerged in these species independently, through the fusion of the Y chromosome and an autosome.
Phylogenetic tree topology confirmed genus Nothobranchius monophyly (Dorn et al., 2014). An ancestral chromosome number of 2n = 36 was reconstructed for all main nodes. Species with the highest diploid chromosome number and proportion of uniarmed chromosomes N. brieni (2n = 49/50) and N. malaissei (2n = 48) occupied positions deeply nested within Nothobranchius. Species with heteromorphic sex chromosomes didn’t closely relate to each other and belonged to two different clades.
We found a significant phylogenetic signal for diploid chromosome number and fundamental number. Values for Pagel’s lambda statistic (λ = 0.99, p< 0.01) and Blomberg’s K statistic (K = 0.23, p = 0.001) were significant. The correlation between genetic and karyotypic distances calculated was significant but weak (r = 0.2, p = 0.015). Thus, diploid chromosome numbers (2n) and fundamental numbers (NF) were significantly more similar for closely related species than for random ones.
Basing on the chromosome morphologies and the ancestral chromosome numbers, we propose the set of chromosome rearrangements involved in karyotype evolution of Nothobranchius. Interspecies differences in diploid chromosome number (2n) can result from both chromosome fusions for species with 2n = 16-34 and fissions events for species with 2n = 38-50. Some species share 2n values but they exhibit different chromosome morphology which can result from pericentric inversions or centromere shift events. Multiple sex chromosome system originated independently in species of different clades. Significant phylogenetic signal for chromosome number and morphology but a weak correlation between genetic and karyotypic distances can result from fast chromosome evolution of Nothobranchius.
Thus, the two main types of chromosomal rearrangements, chromosomal fusions/fissions and pericentric inversions (or centromeric shifts), and a high rate of chromosome evolution led to high karyotype diversity of genus Nothobranchius.
Acknowledgements
The reported study was funded by RFBR according to the research project 17-04-01899.
References
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Keywords:
Annual fish,
chromosome evolution,
Karyotype diversity,
chromosome rearrangements,
killifish
Conference:
XVI European Congress of Ichthyology, Lausanne, Switzerland, 2 Sep - 6 Sep, 2019.
Presentation Type:
Oral
Topic:
GENETICS, GENOMICS AND PHYSIOLOGY
Citation:
Demidova
TB,
Simanovsky
SA,
Raspopova
AA and
Krysanov
EY
(2019). Karyotypic Evolution in African Fishes of the Genus Nothobranchius (Cyprinodontiformes).
Front. Mar. Sci.
Conference Abstract:
XVI European Congress of Ichthyology.
doi: 10.3389/conf.fmars.2019.07.00051
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Received:
06 Jun 2019;
Published Online:
14 Aug 2019.
*
Correspondence:
Mx. Tatiana B Demidova, Severtsov Institute of Ecology and Evolution (RAS), Moscow, Russia, demidovatanya@mail.ru