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Karyotypes and Sex Chromosomes in Two Australian Native Freshwater Fishes, Golden Perch (Macquaria Ambigua) and Murray Cod (Maccullochella Peelii) (Percichthyidae)

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Karyotypes and Sex Chromosomes in Two Australian Native Freshwater Fishes, Golden Perch (Macquaria Ambigua) and Murray Cod (Maccullochella Peelii) (Percichthyidae) International Journal of Molecular Sciences Article Karyotypes and Sex Chromosomes in Two Australian Native Freshwater Fishes, Golden Perch (Macquaria ambigua) and Murray Cod (Maccullochella peelii) (Percichthyidae) Foyez Shams 1,*, Fiona Dyer 1, Ross Thompson 1, Richard P. Duncan 1, Jason D. Thiem 2, Zuzana Majtánová 3 and Tariq Ezaz 1,* 1 Institute for Applied Ecology, Faculty of Science and Technology, University of Canberra, Canberra, Australian Capital Territory 2617, Australia 2 Department of Primary Industries, Narrandera Fisheries Centre, Narrandera, New South Wales 2700, Australia 3 Institute of Animal Physiology and Genetics, CAS, p.r.i., 277 21 Libˇechov, Czech Republic * Correspondence: [email protected] (F.S.); [email protected] (T.E.); Tel.: +61-2-6201-2872 (F.S.); +61-2-6201-2297 (T.E.) Received: 7 August 2019; Accepted: 28 August 2019; Published: 30 August 2019 Abstract: Karyotypic data from Australian native freshwater fishes are scarce, having been described from relatively few species. Golden perch (Macquaria ambigua) and Murray cod (Maccullochella peelii) are two large-bodied freshwater fish species native to Australia with significant indigenous, cultural, recreational and commercial value. The arid landscape over much of these fishes’ range, coupled with the boom and bust hydrology of their habitat, means that these species have potential to provide useful evolutionary insights, such as karyotypes and sex chromosome evolution in vertebrates. Here we applied standard and molecular cytogenetic techniques to characterise karyotypes for golden perch and Murray cod. Both species have a diploid chromosome number 2n = 48 and a male heterogametic sex chromosome system (XX/XY). While the karyotype of golden perch is composed exclusively of acrocentric chromosomes, the karyotype of Murray cod consists of two submetacentric and 46 subtelocentric/acrocentric chromosomes. We have identified variable accumulation of repetitive sequences (AAT)10 and (CGG)10 along with diverse methylation patterns, especially on the sex chromosomes in both species. Our study provides a baseline for future cytogenetic analyses of other Australian freshwater fishes, especially species from the family Percichthyidae, to better understand their genome and sex chromosome evolution. Keywords: sex determination; florescence in situ hybridisation (FISH); comparative genomic hybridisation (CGH); karyogram; DNA methylation 1. Introduction Morphological characteristics of chromosomes, like the size and number (including ploidy) may vary within taxonomic groups such as families, genera and even species [1]. Moreover, functional differences (e.g., accumulation of repetitive sequences, location of a certain gene or DNA methylation) often occur among species as well as among populations or among individuals of the same species [2–4]. Consequently, cytogenetic studies provide a useful tool for establishing phylogenetic and evolutionary relationships among species. Karyotype analysis can also facilitate the discovery of heteromorphic or heterochromatic sex chromosomes. Identification of sex chromosomes is important in dioecious species as it provides information on the evolution of sex determination and insights into the effect of environment in driving sex ratios Int. J. Mol. Sci. 2019, 20, 4244; doi:10.3390/ijms20174244 www.mdpi.com/journal/ijms Int. J. Mol. Sci. 2019, 20, x FOR PEER REVIEW 2 of 15 Int. J. Mol. Sci. 2019, 20, 4244 2 of 14 Identification of sex chromosomes is important in dioecious species as it provides information ofon populations the evolution through of sex upregulation determination and and downregulation insights into the of effect genes ofin environment gonadal development in driving sex [5, 6]. ratios of populations through upregulation and downregulation of genes in gonadal development The importance of understanding the sex chromosome systems in fish is heightened by the existence of [5,6]. The importance of understanding the sex chromosome systems in fish is heightened by the diverse genetic and epigenetic features such as genetic sex determination (GSD), environmental sex existence of diverse genetic and epigenetic features such as genetic sex determination (GSD), determination (ESD), mixed GSD–ESD and rapid sex reversal within this large group of animals [7]. environmental sex determination (ESD), mixed GSD–ESD and rapid sex reversal within this large Fish comprise more than fifty percent of extant vertebrate species [8], with around 32,500 species, group of animals [7]. includingFish more comprise than 15,000 more freshwaterthan fifty percent species [of9]. exta Freshwatersnt vertebrate are thusspecies hyperdiverse, [8], with around considering 32,500 this habitatspecies, constitutes including less more than than 0.3% 15,000 [10] of freshwater available global species water. [9]. Freshwaters Freshwater fishare arethus thus hyperdiverse, an important componentconsidering of this global habitat biodiversity constitutes and less evolutionary than 0.3% [10] studies. of available global water. Freshwater fish are thusThe an familyimportant Percichthyidae component of global (Order: biodiversity Centrarchiformes) and evolutionary or temperate studies. perches, consists of 22 freshwaterThe family and estuarinePercichthyidae species (Order: under Centrarchifo nine genera,rmes) distributed or temperate in Australia perches, and consists South Americaof 22 (Figurefreshwater1)[ 11 ].and The estuarine species investigatedspecies under here nine are gene goldenra, distributed perch (Macquaria in Australia ambigua and )South and Murray America cod (Maccullochella(Figure 1) [11]. peelii The), species two large-bodied investigated freshwaterhere are golden fish speciesperch (Macquaria native to ambigua the Murray) and DarlingMurray cod Basin (MDB)(Maccullochella in south-eastern peelii), Australiatwo large-bodied [12,13]. Goldenfreshwater perch fish also species occurs native in central to the Australia Murray Darling in the Lake Basin Eyre Basin(MDB) and in in south-eastern the central, coastal Australia Queensland [12,13]. Golden Fitzroy perch Basin, also although occurs in these central populations Australia are in consideredthe Lake toEyre be separate Basin and cryptic in the species central, [14 coastal]. Both Queenslan golden perchd Fitzroy and Murray Basin, although cod have these significant populations indigenous, are cultural,considered recreational to be separate and commercial cryptic species value. [14]. Moreover, Both golden both perch species and have Murray been bredcod have in hatcheries significant and extensivelyindigenous, stocked cultural, in catchmentsrecreational acrossand commercial the MDB forvalue. more Moreover, than 30 years.both species have been bred in hatcheries and extensively stocked in catchments across the MDB for more than 30 years. Figure 1 1.. DistributionDistribution of of nine nine genera genera of ofPercichthyidae Percichthyidae covering covering Australia, Australia, Chile Chile and andArgentina Argentina. SexSex chromosomes chromosomes in fishin fish have have been been studied studied since since theearly the early twentieth twentieth century, century, when thewhen presence the ofpresence heterogametic of heterogametic sex chromosome sex chromosome systems (either systems XY (either or WZ) XY was or describedWZ) was described [15–17]. Studies[15–17]. in fishesStudies have in identified fishes have diverse identified sex chromosomal diverse sex chromosomal systems (including systems XX (including/XY, XX/X0, XX/XY, ZZ/ZW, XX/X0, ZZ/Z0, XXZZ/ZW,/XY1Y2, ZZ/Z0, X1X1X2X2 XX/XY1Y2,/X1X2Y, ZZX1X1X2X2/X1X2Y,/ZW1W2, Z1Z1Z2Z2 ZZ/ZW1W2,/Z1Z2W), Z1Z1Z2Z2/Z1Z2W), with the XX/XY (male with heterogametic) the XX/XY and(male ZZ /heterogametic)ZW (female heterogametic) and ZZ/ZW (female systems heterogametic) being predominant systems being [18,19 predominant]. The ancestral [18,19]. fish The sex chromosomeancestral fish (sex-determining sex chromosome locus) (sex-determining has gone through locus) a complete has gone shift through of chromosome a complete pairs shift because of ofchromosome frequent chromosome pairs because rearrangements of frequent such chromosome as fusion andrearrangements translocation orsuch transposition as fusion [and20,21 ]. Suchtranslocation rearrangement or transposition events across [20,21]. the Such genome, rearrangement including events the sex across chromosomes, the genome, make including teleost the fish potentiallysex chromosomes, informative make for studiesteleost offish karyotype potentiall andy informative sex chromosome for studies evolution. of karyotype To date, thereand sex have beenchromosome no published evolution. studies onTo thedate, mode there of sexhave determination been no published in Australian studies freshwater on the mode fish. of sex determinationThe karyotype in Australian data for Australianfreshwater fish. freshwater fish fauna are scarce (Figure2)[ 22,23]. Prior to the current study, there have been no published accounts of karyotype data for any fish from the family Percichthyidae. Molecular characterisation of karyotypes is an important first step towards understanding genome evolution and organisation. In particular, mapping repetitive sequences Int. J. Mol. Sci. 2019, 20, x FOR PEER REVIEW 3 of 15 Int. J. Mol.The Sci. karyotype2019, 20, 4244 data for Australian freshwater fish fauna are scarce (Figure 2) [22,23]. Prior to the3 of 14 current study, there have been no published accounts of karyotype data for any fish from the family Percichthyidae.
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