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Revisiting the Karyotype Evolution of Neotropical Boid Snakes: a Puzzle Mediated by Chromosomal Fissions

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Revisiting the Karyotype Evolution of Neotropical Boid Snakes: a Puzzle Mediated by Chromosomal Fissions cells Article Revisiting the Karyotype Evolution of Neotropical Boid Snakes: A Puzzle Mediated by Chromosomal Fissions Patrik F. Viana 1 , Tariq Ezaz 2 , Marcelo de Bello Cioffi 3 , Thomas Liehr 4,* , Ahmed Al-Rikabi 4, Rodrigo Tavares-Pinheiro 5, Luiz Antônio Carlos Bertollo 3 and Eliana Feldberg 1 1 Laboratory of Animal Genetics, Instituto Nacional de Pesquisas da Amazônia, Coordenação de Biodiversidade, Av. André Araújo 2936, Petrópolis, Manaus 69067-375, AM, Brazil; [email protected] (P.F.V.); [email protected] (E.F.) 2 Institute for Applied Ecology, Faculty of Science and Technology, University of Canberra, Canberra 12 2616, ACT, Australia; [email protected] 3 Departamento de Genética e Evolução, Universidade Federal de São Carlos, São Carlos 13565-090, SP, Brazil; mbcioffi@ufscar.br (M.d.B.C.); [email protected] (L.A.C.B.) 4 Institute of Human Genetics, University Hospital Jena, Am Klinikum 1, 07747 Jena, Germany; [email protected] 5 Departamento de Ciências Biológicas e da Saúde, Laboratório de Herpetologia, Universidade Federal do Amapá, Macapá 68903-419, AP, Brazil; [email protected] * Correspondence: [email protected]; Tel.: +49-3641-9396850 Received: 17 September 2020; Accepted: 9 October 2020; Published: 10 October 2020 Abstract: The Boidae family is an ancient group of snakes widely distributed across the Neotropical region, where several biogeographic events contributed towards shaping their evolution and diversification. Most species of this family have a diploid number composed of 2n = 36; however, among Booidea families, the Boidae stands out by presenting the greatest chromosomal diversity, with 2n ranging between 36 and 44 chromosomes and an undifferentiated XY sex chromosome system. Here, we applied a comparative chromosome analysis using cross-species chromosome paintings in five species representing four Boidae genera, to decipher the evolutionary dynamics of some chromosomes in these Neotropical snakes. Our study included all diploid numbers (2n = 36, 40, and 44) known for this family and our comparative chromosomal mappings point to a strong evolutionary relationship among the genera Boa, Corallus, Eunectes, and Epicrates. The results also allowed us to propose the cytogenomic diversification that had occurred in this family: a process mediated by centric fissions, including fission events of the putative and undifferentiated XY sex chromosome system in the 2n = 44 karyotype, which is critical in solving the puzzle of the karyotype evolution of boid snakes. Keywords: chromosomal painting; evolution; neotropical region; Serpentes; Booidea 1. Introduction The modern boas (Booidea) and pythons (Pythonoidea) are an ancient group of snakes, often referred to as primitive snakes (Henophidia). Currently, comprising more than 220 valid species, the former diversified lineages of snakes, jointly with Scolecophidia and Caenophidia, represent the three main groups that make up the Serpentes suborder [1–4]. The Booidea superfamily is a monophyletic group [5,6], including six families, Calabariidae, Candoiidae, Sanziniidae, Charinidae, Erycidae, and Boidae, with over 66 species that are distinct both morphologically and Cells 2020, 9, 2268; doi:10.3390/cells9102268 www.mdpi.com/journal/cells Cells 2020, 9, 2268 2 of 11 biogeographicallyCells 2020, 9, x FOR [ 5PEER,7,8 ].REVIEW Calabariidae is restricted to West Africa, whereas Candoiidae is restricted2 of 11 to the Australasian countries, Sanziniidae to Madagascar, Charinidae to Central and North Americas single Colombian species), Erycidae to Europe, Middle East, North Africa, and Central and Southern (excepting for a single Colombian species), Erycidae to Europe, Middle East, North Africa, and Central Asia, and Boidae to the Neotropical region (Figure 1) [4–6,9]. This worldwide distribution is the result and Southern Asia, and Boidae to the Neotropical region (Figure1)[ 4–6,9]. This worldwide distribution of numerous biogeographic events associated with the Gondwana fragmentation [10–14]. is the result of numerous biogeographic events associated with the Gondwana fragmentation [10–14]. Figure 1. Estimated worldwide distribution pattern of Booidea species according to Reynolds and HendersonFigure [1.14 Estimated] and Uetz worldwide and Hosek distribution [4]. pattern of Booidea species according to Reynolds and Henderson [14] and Uetz and Hosek [4]. The Neotropical Boidae family stands out as an intriguing group due to its stunning and complex evolutionaryThe andNeotropical biogeographic Boidae family history stands dating out from as an the intriguing end of thegroup Cretaceous due to itsperiod stunning [12 ,13and,15 ,16]. Boidscomplex are viviparous evolutionary species and inhabiting biogeographic a wide hist rangeory dating of environments from the end andof the microhabitats, Cretaceous period including [12,13,15,16]. Boids are viviparous species inhabiting a wide range of environments and different forest landscapes that reflect their varied behaviors, such as generalist (Boa and Epicrates), microhabitats, including different forest landscapes that reflect their varied behaviors, such as aquatic (Eunectes), and arboreal (Corallus and Chilabothrus)[9,17,18]. Part of the diversification of generalist (Boa and Epicrates), aquatic (Eunectes), and arboreal (Corallus and Chilabothrus) [9,17,18]. thesePart snakes of the was diversification also mediated of these by vicariant snakes was events also (e.g.,mediated marine by vicariant incursions, events uplift (e.g. of, marine the Andes, and geologyincursions, of uplift the of Isthmus the Andes, of Panama)and geology [6 ,of16 the,19 –Isthmus21]. Boidae of Panama) is also [6,16, the19– most21]. Boidae speciose is also group insidethe the most Booidea speciose superfamily, group inside the comprising Booidea superfamily, more than comprising 30 species more allocated than 30 species in five allocated genera, Boa, Corallusin five, Eunectes genera,, EpicratesBoa, Corallus, and, EunectesChilabothrus, Epicrates[4,– and6], representing Chilabothrus [4 the–6], Neotropicalrepresenting radiationthe Neotropical from this superfamilyradiation [ 5from,9,15 ].this These superfamil snakesy [5,9,15 differ]. inThese biogeographic, snakes differ morphological, in biogeographic, molecular, morphological, and even chromosomalmolecular, characteristics and even chromosomal [5,6,22– 24characteristics]. [5,6,22–24]. MostMost of the of Serpentesthe Serpentes lineages lineages have have 2n 2n= = 3636 chromosomes (16 (16 macro macro + 20+ microchromosomes),20 microchromosomes), which is considered a plesiomorphic feature for the suborder [25–28]. However, Boidae differs from which is considered a plesiomorphic feature for the suborder [25–28]. However, Boidae differs other families by presenting the greatest chromosomal diversity among the Booidea families, with 2n from other families by presenting the greatest chromosomal diversity among the Booidea families, ranging from 36 to 44 chromosomes, including an undifferentiated XY sex chromosome system with[24,25, 2n ranging29]. Robertsonian from 36 to and 44 non chromosomes,-Robertsonian includingrearrangements, an undi includingfferentiated fission XYevents sex [26] chromosome, have systemoften [24 been,25,29 proposed]. Robertsonian to explain and this non-Robertsonian karyotype diversity. rearrangements, Furthermore, the including occurrence fission of interstitial events [26], havetelomeric often been sequences proposed (ITSs) to explain in most this karyotypeof the analyzed diversity. species Furthermore, strongly thesuggests occurrence that multiple of interstitial telomericchromosomal sequences rearrangements (ITSs) in most contributed of the analyzed to such species diversity strongly [24,30]. suggests that multiple chromosomal rearrangementsAlmost contributedsix decades toago, such the diversity first steps [24 towards,30]. understanding the cytotaxonomy of the AlmostNeotropical six decadessnakes were ago, thetaken first by steps Professor towards Willy understanding Beçak, a Brazilian the cytotaxonomy pioneer researcher of the trying Neotropical to snakesunravel were takentheir chromosome by Professor evolution. Willy Beçak, Beçak a Braziliandiscovered pioneer a remarkable researcher karyotype trying diversity to unravel for their Neotropical Boidae snakes, finding 2n = 36 chromosomes for three genera (Boa, Eunectes, and chromosome evolution. Beçak discovered a remarkable karyotype diversity for Neotropical Boidae Epicrates) and 2n = 44 chromosomes in the Corallus caninus species, whose karyotype was composed Boa Eunectes Epicrates snakes,only finding of subtelo/acrocentric 2n = 36 chromosomes like chromosomes. for three However, genera (the ,lack of refined, and taxonomic/molecular) and 2n = 44 Corallus caninus chromosomes in the species, whose karyotype was composed only of subtelo/acrocentric like chromosomes. However, the lack of refined taxonomic/molecular tools at the time led Beçak to Cells 2020, 9, 2268 3 of 11 conclude that 2n = 44 could represent the plesiomorphic condition for the Boidae family and that 2n = 36 would be a derived condition originating from chromosomal fusions. Years later, Gorman and Gress [26] added another key piece to this puzzle, by identifying the 2n = 40 for the species Corallus grenadensis from the West Indies, an intermediate 2n between the 36 as found in Boa, Eunectes, Epicrates, and Chilabothrus and 44, present in Corallus caninus. This intermediate 2n configuration led Gorman and Gress [26] to suggest that the evolution
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