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Gene 628 (2017) 275–280 Gene 628 (2017) 275–280 Contents lists available at ScienceDirect Gene journal homepage: www.elsevier.com/locate/gene Research paper Molecular adaptive convergence in the α-globin gene in subterranean MARK octodontid rodents ⁎ Ivanna H. Tomascoa, , Nicolás Boullosaa, Federico G. Hoffmannb,c, Enrique P. Lessaa a Departamento de Ecología y Evolución, Facultad de Ciencias, Universidad de la República, Iguá 4225, Montevideo, 11400, Uruguay b Department of Biochemistry and Molecular Biology, Mississippi State University, MS, USA c Institute for Genomics, Biocomputing and Biotechnology, Mississippi State University, MS, USA ARTICLE INFO ABSTRACT Keywords: Tuco-tucos (Ctenomys) and related coruros (Spalacopus) are South American subterranean rodents. An en- Molecular evolution ergetically demanding lifestyle within the hypoxic/hypercapnic underground atmosphere may change the se- Caviomorphs lective regime on genes involved in O2 transport in blood. In addition, some species of tuco-tucos may be found Fossoriality at high altitude, thus facing additional reductions in changes O2 availabily. We examined sequence variation in Hemoglobine the alpha globin subunit gene of hemoglobine in these lineages, within a robust phylogenetic context. Using different approaches (classical and Bayesian maximum likelihood (PAML/Datamonkey) and alternatives methods (TreeSAAP)) we found at least 2 sites with evidence of positive selection in the basal branch of Octodontidae, but not in tuco-tucos. These results suggest some adaptive changes associated to fossoriality, but not strictly to life underground. 1. Introduction environment (Darden, 1972; Arieli, 1990; Shams et al., 2005). Maximal CO2 levels (6.1%) and minimal O2 levels (7.2%) were recorded in Assessing the predictability of evolution is a central question in mounds of Spalax carmeli in Israel (Shams et al., 2005). Models of dif- current evolutionary research. In a macroevolutionary framework, fusion gas exchange (Withers, 1978) and experimental data (MacLean, phylogenetically independent invasions of specialized niches by sets of 1981) show that burrow atmospheres are generally hypoxic and hy- relatively closely related species have proven to be powerful study percapnic (Buffenstein, 2000). systems. Among vertebrates, the independent invasion of high-altitude Under low O2 partial pressure in the burrow atmosphere and facing environments by multiple birds, the evolution of diving in multiple the potential CO2 perturbation of their blood acid-base balance, sub- mammalian taxa or the independent invasion of the subterranean niche terranean mammals are expected to avoid excessive energy expenditure by rodents represent natural study systems to address these type of in respiratory work. The mechanisms by which this is achieved are not questions (see Lacey et al., 2000). fully understood, but apparently include several physiological adjust- Subterranean rodents live most of their lives underground in their ments in relation to the predicted values of mammals of similar body usually closed burrows, which are dark, hypoxic, hypercapnic, and mass (predicted by Stahl, 1967) and at different levels (reviewed by thermally stable relative to their above-ground counterparts. From a Boggs et al., 1984, Buffenstein, 2000, Nevo et al., 1999). For example, biological standpoint, life underground imposes particular challenges, oxygen carrying capacity is increased, facilitated by elevated he- which have driven subterranean rodents to develop convergent mor- moglobin concentrations, high intrinsic affinity for oxygen and more phological and physiological features (Nevo et al., 1999). An important red blood cells (reviewed by Buffenstein, 2000). constraint faced by subterranean mammals is the low availability of O2 There have been at least eight independent invasions of the sub- (hypoxia) and the excess of CO2 (hypercapnia) in the subterranean terranean niche by rodents. Among them, comparisons between the Abbreviations: O2, oxygen; CO2, carbon dioxide; Hb, hemoglobine; Cl, cloride; α-globine, alpha-globine subunit gene of hemoglobine; β-globine, beta-globine subunit gene of he- moglobine; PAML, phylogenetic analysis by maximum likelihood (software); TreeSAAP, selection on amino acid properties using phylogenetic trees (software); MEME, mixed effects model of evolution (software); REL, random effects branch-site model (software); Mya, millon years ago; M asl., metres above sea level; SDS, sodium dodecyl sulfate; NaCl, sodium chloride; DNA, deoxyribonucleic acid; dNTP, deoxyribonucleoside triphosphate; MgCl2, magnesium chloride; Ala, alanine; Gly, glycine; Asp, aspartic acid; Glu, glutamic acid; Asn, aspargine; Ser, serine; Thr, threonine; Leu, leucine ⁎ Corresponding author at: Departamento de Ecología y Evolución, Facultad de Ciencias, Universidad de la República, Iguá 4225, Montevideo 11400, Uruguay. E-mail addresses: [email protected], [email protected] (I.H. Tomasco), [email protected] (N. Boullosa), federico.g.hoff[email protected] (F.G. Hoffmann), [email protected] (E.P. Lessa). http://dx.doi.org/10.1016/j.gene.2017.07.057 Received 16 May 2017; Received in revised form 21 June 2017; Accepted 19 July 2017 Available online 21 July 2017 0378-1119/ © 2017 Elsevier B.V. All rights reserved. I.H. Tomasco et al. Gene 628 (2017) 275–280 Changes in sites/branches positively selected by 12 Ctenomys rionegrensis PAML MEME TreeSAAP Ctenomys leucodon Ctenomys sociabilis Ctenomyidae Ctenomyidae 71 subterranean Spalacopus cyanus Aconaemys fuscus 57 71 1 Octodon degus 111 Tympanoctomys barrerae Octodontidae 130 12 71 Proechimys longicaudatus Cavia porcellus Cavia aperea Fig. 1. Phylogenetic relationship among caviomorph rodents included in this study. Numbers are amino acid sites of α-globin gene identified to be under natural selection by different methods. Red, blue and gray circles, show sites identified as positively selected by PAML, MEME and TreeSAAP, respectively. (For interpretation of the references to color in this figure legend, the reader is referred to the web version of this article.) South American sibling families Octodontidae (degus, coruros and al- Specifically, the goal of this study is to look for convergent or parallel lies) and Ctenomyidae (tuco-tucos) provide a unique opportunity to changes in the α-globin genes of subterranean lineages relative to their trace the evolution of adaptations related to life underground because fossorial counterparts, and explore whether these changes were driven of their phylogenetic affinities and their relatively recent occupation of by natural selection. the subterranean niche (Lessa et al., 2008). Burrowing for shelter and rearing young (fossoriality) are shared characteristics among these two 2. Materials and methods families of rodents, but only two extant genera, Ctenomys (tuco-tucos) and Spalacopus (coruros) have acquired fully subterranean lifestyles and 2.1. Specimens examined their associated anatomical and physiological adaptations (Fig. 1). These two South American genera of subterranean rodents are analo- We selected 2 specimens from 10 caviomorph rodent species, in- gous to North American pocket gophers but have entered the sub- cluding representatives of two related but independent subterranean terranean niche more recently. Moreover, the sister groups of most lineages. Among these subterranean lineages were three species of tuco- other subterranean rodent lineages, if at all known, tend to be very tucos (Ctenomys) and the coruro (Spalacopus cyanus). Fossorial, but non- divergent from the subterranean groups, but this is not the case with subterranean relatives were three Octodontid rodents (Aconaemys Octodontidae and Ctenomyidae which have diverged between 14 and fuscus, Octodon degus and Tympanoctomys barrerae). We also add a non- 23 Mya (reviewed in Patton et al., 2015). Within Octodontidae, the fossorial spiny rat (Proechimys longicaudatus), and finally two species of coruro has evolved a fully subterranean life and acquired numerous Cavia (C. porcellus and C. aperea) which were used as outgroup. Because morphological changes within the last 2 to 3 Mya (Lessa et al., 2008; tuco-tucos comprise >63 species and were considered one of the most Opazo, 2005). The family Ctenomyidae accumulated changes asso- rapidly speciating mammalian lineages (Patton et al., 2015), we chose a ciated to subterranean life in a mosaic fashion along several lineages, in sample of 3 species from this group, in an attempt to capture the di- a longer process that has taken at least 8 Mya; the extant diversity of versity of lifestyles and molecular differentiation and habitat features tuco-tucos includes >63 nominal species (Patton et al., 2015) that following Tomasco and Lessa (2011): C. sociabilis, C. rionegrensis and C. diversified in the last 3.5 Mya (Verzi et al., 2010). In addition, phylo- leucodon. First two species live on lowland, about 0 m asl, but C. leu- genetic relationships among the genera are well-established (e.g., codon occurs between 3800 and 4500 m asl. We also included se- Opazo, 2005; Upham and Patterson, 2012 and references therein), quences of O. degus and C. porcellus taken from GenBank (XM_ which facilitates the tracing of changes associated with the acquisition 003478407.2 and XM_004627947.1 respectively). Table 1 summarizes of subterranean adaptations onto an established phylogeny, enabling us information about specimen voucher numbers and sampling localities to identify and discriminate adaptations restricted to subterranean of samples. lineages from
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