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Evolution of Trans-Andean Endemic

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Evolution of Trans-Andean Endemic Soto et al. Revista Chilena de Historia Natural (2018) 91:8 Revista Chilena de https://doi.org/10.1186/s40693-018-0078-5 Historia Natural RESEARCH Open Access Evolution of trans-Andean endemic fishes of the genus Cheirodon (Teleostei: Characidae) are associated with chromosomal rearrangements Miguel Ángel Soto1, Jonathan Pena Castro2, Laura Ines Walker3, Luiz Roberto Malabarba4, Mateus Henrique Santos1, Mara Cristina de Almeida1, Orlando Moreira-Filho1,2 and Roberto Ferreira Artoni1,2* Abstract Background: Among Neotropical fishes, the family Characidae is highly diverse and speciose and its taxonomy is not completely resolved. In Chile, the family is represented by five species, all within the genus Cheirodon, of which C. pisciculus, C. galusdae, C. kiliani, and C. australe are endemic, while C. interruptus is introduced. We compared chromosomal markers in order to appreciate the taxonomy and evolution of these trans-Andean fishes. Results: The specimens were photographed in stereomicroscope to observe the ventral protrusive teeth and cusps for morphological analysis and species identification. All of the species analysed had equally diploid chromosome number 2n = 50, with karyotypes dominated by high number of acrocentric chromosomes as compared to those of other members of Cheirodontinae. The distribution of heterochromatin was inconspicuous and was similar in all the species. The number of active NORs (nucleolus organizer regions) was polymorphic, with the greater number of them in C. kiliani and C. galusdae. The location of 5S and 18S rDNA ranged in number and position, showing two sites in different chromosomes. The fluorescent in situ hybridization with telomeric probe did not reveal interstitial sites in all analysed species. Conclusions: The comparative analysis of karyotypes and morphological markers revealed a biogeographic pattern of distribution, with the species that occur in the southern region forming one group and those in central and northern Chile forming another. Keywords: Andean cordillera, Endemism, Freshwater fishes, Chromosome, Sea level, South America Background to distinguish [28]. Among the diverse fishes of the Although South America is typically megadiverse in Neotropical region, the family Characidae is one of the biodiversity, the hydrogeography of Chile and its natural most complex groups in terms of its taxonomy [13]. In isolation due to the Andean cordillera makes an exception. Chile, the family is represented by a single genus, namely These patterns have influenced the evolutionary history of Cheirodon [6, 27]. Its species are morphologically similar, its fish fauna, which is highly endemic and inconspicuous which makes it difficult to distinguish them [21]. in morphology and coloration what makes them difficult Five species of Cheirodon occur in Chile, they are distrib- uted allopatrically in a North to South direction: C. piscicu- * Correspondence: [email protected] lus (Girard, 1855), C. galusdae [4], C. kiliani [3], and C. 1Departamento de Biologia Estrutural, Molecular e Genética, Programa de Pós-Graduação em Biologia Evolutiva, Universidade Estadual de Ponta Grossa, australe (Campos, 1992) are endemic to Chile [3], whereas Avenida Carlos Cavalcanti 4748, Ponta Grossa, PR 84030-900, Brazil C. interruptus (Jenyns, 1842) is native to the Atlantic ba- 2 Departamento de Genética e Evolução, Programa de Pós-Graduação em sins of Argentina, Uruguay, and Brazil (Malabarba 2003). Biologia Evolutiva e Genética Molecular, Universidade Federal de São Carlos, Rodovia Washington Luis, Km 235, Monjolinho, São Carlos, SP 13565-905, It may have been introduced to Chile in the 1960s along Brazil with the larvae of Pejerrey, Odontesthes bonariensis Full list of author information is available at the end of the article © The Author(s). 2018 Open Access This article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated. Soto et al. Revista Chilena de Historia Natural (2018) 91:8 Page 2 of 8 (Valenciennes, 1835) [1, 3]. In fact, the first records of C. for taxonomic identification. The specimens were photo- interruptus in Chile were from Peñuelas Lake, an artificial graphed using a Leica M205C Stereomicroscope to ob- lake where O. bonariensis was likely first reared [20]. serve the ventral protrusive teeth and cusps. The The Chilean Cheirodon species have already been the analysed material was deposited in the Department of subject of morphological and molecular analyses [3, 14, Zoology of the Universidade Federal de Rio Grande do 21], to define their phylogenetic relationships. These Sul, Brazil, under vouchers UFRGS 22295 (Ch. interrup- analyses tended to group geographically distant species, tus), UFRGS 22296 (Ch. galusdae), UFRGS 22297 (Ch. such as Ch. australe and Ch. interruptus (the introduced pisciculus), UFRGS 22298 (Ch. kiliani), and UFRGS species) together [3, 14, 21]. In addition, some of the 22299 and UFRGS 22300 (Ch. australe). morphological characters used in those analyses can vary inter- and intra-specifically, which may lead to erroneous Chromosome preparations identification of Cheirodon populations [13]. Further- Chromosome preparations were obtained from fin tissue more, the DNA sequence analyses used in Chilean regenerated for three days for animals acclimated at 20 °C Cheirodon did not include Ch. pisciculus nor Ch. galus- in aquarium. The regeneration occurs in situ, therefore, dae, respectively, [14], so the phylogenetic relationships does not require special incubation conditions (20 °C), between the trans-Andean species remain unclear. more than those that do the fish to remain activefollowing Due to the difficulties in sampling as well as their the protocol of [29]. This technique was employed here due small size making difficult to obtain chromosomes, there to the small size of the animals (< 3.0 cm). To obtain the is no cytogenetic information about the Cheirodon ex- number, size, and morphology of chromosomes, the slides cept the 2n and karyotypes of the Cheirodontinae genera were stained with Giemsa diluted in 5% phosphate buffer Odontostilbe and Serrapinnus only [22, 25, 30]. These (KH2 PO4 +Na2 HPO4) pH 6.8 for 10 min and then washed data may be used to generate cytotaxonomic informa- in running water and air dried. To visualize heterochro- tion and detect evolutionary relationships to better matic regions, we used the C-band technique by Sumner understand the diversity of the genus Cheirodon [2]. Ac- [23], adaptated by Lui et al. [12]. The nucleolus organizer cordingly, in order to infer the taxonomy and evolution regions (Ag-NORs) were visualised according to [8]. of the trans-Andean Characidae, in the present work we Fluorescence in situ hybridisation (FISH) was utilised to elucidated the conventional and molecular cytogenetic detect chromosomal location of rDNA (18S and 5S) sites characteristics of its five species and contrast them with and telomeric sequences, according to the protocol of Pin- available morphological, molecular and cytogenetic data kel et al. [18], under high stringency (2.5 ng/μL probe, for the group. 50% formamide, 2× SSC, and 10% dextran sulphate). The 18S rDNA probe was amplified from the DNA of Prochi- Methods lodus argenteus (Spix & Agassiz, 1829) [7], using the Biological materials and sampling areas primers NS1 5′-GTAGT CATATGCTTGTCTC-3′ and A total of 15 individuals were collected for each one of the NS8 5’-TCCGCAGGTTC ACCTACGGA-3′ [31]. The 5S following species in different areas: Ch. interruptus (Estero probe was obtained from DNA amplification of Leporinus Marga-Marga, Viña del Mar, V region, Chile, coordinates elongatus (Valenciennes, 1850), using the primers A 19H 0263800.90 UTM E–6342166.09 UTM S), Ch. pisci- 5’-TACGCCCGATCTCGTCCGATC-3′ and B 5’-GCTG culus (Río Angostura, Hospital, Metropolitan region, GTATGGCCGTAGC-3′ [15]. The telomere probe Chile, coordinates 19H 0338122.17 UTM E–6250729.69 (TTAGGG) n was amplified using the primers (TTAG UTM S), Ch. galusdae (Río Andalién, Concepción, VIII GG)5 and (CCCTAA)5, in the absence of a DNA template, região, Chile, coordinates 18H 0682055.00 UTM according to [9]. The chromosome mapping of the 18S E–5925386.00 UTM S), Ch. kiliani (Rio Calle-Calle, Antil- probe was achieved using the Kit Biotin Nick Translation hue, XIV region, Chile, coordinates 18H 0674363.00 UTM (Roche), and the 5S and telomeric mappings were per- E–5592270.00 UTM S) and Ch. australe (Lagoa La Poza, formed using Kit Dig Nick Translation (Roche), following desembocadura Lago Llanquihue, Puerto Varas, X região, the manufacturer’s recommendations. Signal detection Chile, coordinates 18G 0679651.18 UTM E–5428179.56 was performed with digoxigenin conjugated to rhodamine UTM S). The capture of the specimens was authorised by (18S probe) and streptavidin conjugated to FITC (5S and the Subsecretaría de Pesca y Acuicultura del Gobierno de Telomeric probes) (Roche Applied Science). Chile (SUBPESCA) and by the Servicio Nacional de Pesca All analyses used mitotic chromosomes subjected to y Acuicultura del Gobierno de Chile (SERNAPESCA),
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