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RUNX2 Tandem Repeats and the Evolution of Facial Length in Placental Mammals Jason M

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RUNX2 Tandem Repeats and the Evolution of Facial Length in Placental Mammals Jason M University of Massachusetts Amherst ScholarWorks@UMass Amherst Anthropology Department Faculty Publication Anthropology Series 2012 RUNX2 tandem repeats and the evolution of facial length in placental mammals Jason M. Kamilar [email protected] Marie A. Pointer Vera Warmuth Stephen G.B. Chester Frédéric Delsuc See next page for additional authors Follow this and additional works at: https://scholarworks.umass.edu/anthro_faculty_pubs Part of the Animal Studies Commons, Anthropology Commons, and the Evolution Commons Recommended Citation Kamilar, Jason M.; Pointer, Marie A.; Warmuth, Vera; Chester, Stephen G.B.; Delsuc, Frédéric; Mundy, Nicholas I.; Asher, Robert J.; and Bradley, Brenda J., "RUNX2 tandem repeats and the evolution of facial length in placental mammals" (2012). BMC Evolutionary Biology. 332. https://scholarworks.umass.edu/anthro_faculty_pubs/332 This Article is brought to you for free and open access by the Anthropology at ScholarWorks@UMass Amherst. It has been accepted for inclusion in Anthropology Department Faculty Publication Series by an authorized administrator of ScholarWorks@UMass Amherst. For more information, please contact [email protected]. Authors Jason M. Kamilar, Marie A. Pointer, Vera Warmuth, Stephen G.B. Chester, Frédéric Delsuc, Nicholas I. Mundy, Robert J. Asher, and Brenda J. Bradley This article is available at ScholarWorks@UMass Amherst: https://scholarworks.umass.edu/anthro_faculty_pubs/332 Pointer et al. BMC Evolutionary Biology 2012, 12:103 http://www.biomedcentral.com/1471-2148/12/103 RESEARCH ARTICLE Open Access RUNX2 tandem repeats and the evolution of facial length in placental mammals Marie A Pointer1,2,3, Jason M Kamilar2,4,5, Vera Warmuth1, Stephen G B Chester2, Frédéric Delsuc6, Nicholas I Mundy1, Robert J Asher1* and Brenda J Bradley1,2* Abstract Background: When simple sequence repeats are integrated into functional genes, they can potentially act as evolutionary ‘tuning knobs’, supplying abundant genetic variation with minimal risk of pleiotropic deleterious effects. The genetic basis of variation in facial shape and length represents a possible example of this phenomenon. Runt-related transcription factor 2 (RUNX2), which is involved in osteoblast differentiation, contains a functionally- important tandem repeat of glutamine and alanine amino acids. The ratio of glutamines to alanines (the QA ratio) in this protein seemingly influences the regulation of bone development. Notably, in domestic breeds of dog, and in carnivorans in general, the ratio of glutamines to alanines is strongly correlated with facial length. Results: In this study we examine whether this correlation holds true across placental mammals, particularly those mammals for which facial length is highly variable and related to adaptive behavior and lifestyle (e.g., primates, afrotherians, xenarthrans). We obtained relative facial length measurements and RUNX2 sequences for 41 mammalian species representing 12 orders. Using both a phylogenetic generalized least squares model and a recently-developed Bayesian comparative method, we tested for a correlation between genetic and morphometric data while controlling for phylogeny, evolutionary rates, and divergence times. Non-carnivoran taxa generally had substantially lower glutamine-alanine ratios than carnivorans (primates and xenarthrans with means of 1.34 and 1.25, respectively, compared to a mean of 3.1 for carnivorans), and we found no correlation between RUNX2 sequence and face length across placental mammals. Conclusions: Results of our diverse comparative phylogenetic analyses indicate that QA ratio does not consistently correlate with face length across the 41 mammalian taxa considered. Thus, although RUNX2 might function as a ‘tuning knob’ modifying face length in carnivorans, this relationship is not conserved across mammals in general. Keywords: Mammalian evolution, Prognathism, Molecular evolution, Primates, Afrotheria, Xenarthra, Morphology Background expansions and contractions of poly-amino acid Work on the molecular basis of animal adaptation is stretches [7,8]. Moreover, proteins containing such providing ample evidence that small genetic changes can repeats are often involved in development [9,10]. Thus, underlie striking phenotypic differences, both within and the function of a protein can be easily modified via between species [1-4]. Of recent particular interest is the alterations in repeat tract length [8,10] and such modifi- role of short tandemly repeating DNA elements (i.e. cations may have less drastic pleiotropic effects than microsatellites) as evolutionary ‘tuning knobs’ [5]. other types of mutation [4]. Microsatellites are mutation-prone and often show sub- An example of this is the correlation between specific stantial length variation in repeat number [6]. These tandem repeats and variation in midfacial length (i.e., repeats are common in mammalian genomes, often oc- the degree of prognathism, or the jutting of the face and curring within coding exons, potentially translating into jaw) in carnivorans [11-13]. Variation in this striking morphological trait appears to be causatively associated * Correspondence: [email protected]; [email protected] with variation in coding sequence repeats within the 1Department of Zoology, University of Cambridge, Cambridge CB2 3EJ, UK Full list of author information is available at the end of the article gene RUNX2 (Runt-related transcription factor 2). © 2012 Pointer et al.; licensee BioMed Central Ltd. This is an Open Access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/2.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited. Pointer et al. BMC Evolutionary Biology 2012, 12:103 Page 2 of 11 http://www.biomedcentral.com/1471-2148/12/103 RUNX2 (also known as Cbfa1; Entrez Gene ID 860) Here we assess the extent to which the correlation be- codes for a transcription factor that plays an important tween skull shape and RUNX2 QA (Figure 1, Table 1) role in mediating osteoblast differentiation and activity ratio holds true across a variety of non-carnivoran pla- [14]. Its function is critical for building and repairing cental mammals. In particular, we focus on xenarthrans, bone. The activity of RUNX2 is mediated by a few func- afrotherians, and primates as these orders show marked tional domains, one of which consists of a stretch of glu- variations in face length, which are thought to be adap- tamines (abbreviated Q) followed by a stretch of tively associated with diet and ecology [23], and for these alanines (A) (reviewed in [15]). For RUNX2, the ratio of orders we have access to morphometric and genetic glutamines to alanines (QA ratio) appears to be posi- data. In analyzing data for 41 placental mammal species tively correlated with the transcriptional activity of the representing 12 orders (Table 1), we find no correlation protein [13,16]. between RUNX2 sequence and face length (Figures 2, RUNX2 mutations in humans cause the skeletal dis- and 3; Tables 2, and 3) across our sample as a whole. ease cleidocranial dysplasia (MIM 119600) and have been associated with a shortening or protruding of the Results face and other skeletodental pathologies [17,18], some of RUNX2 tandem repeat ratios which correspond to changes in certain clades of non- The translated amino acid sequences for the 41 species human mammals [19]. In general, work on RUNX2 in are provided in the Supplementary Material (Additional humans and mice indicates that when RUNX2 is up- File 1). The RUNX2 amino acid sequences flanking the regulated, bone development is accelerated [20]. In- tandem repeat region were generally conserved across terestingly, in comparisons of the modern human and taxa providing evidence that orthologous rather than Neanderthal genomes, RUNX2 is specifically highlighted paralogous sequences were successfully retrieved. In by Green et al. [21] as one of few genes showing a genetic signature of a selective sweep in the modern human lineage. Assuming the Neanderthal sequence data are valid, this would suggest a potentially important role for RUNX2 in human-specific cranial/skeletal features. The QA ratio of RUNX2 is correlated with facial length across breeds of dog (92 breeds of Canis lupus Oc-Pat familiaris; see [11] and across carnivorans in general CBL (30 species; [13]). Specifically, dog breeds and other car- nivoran species with a high QA ratio tend to have a relatively long rostrum or "face". Furthermore, Sears et al. [13] noted that the correlation was stronger among dogs, bears, raccoons and their relatives (i.e., caniforms) than among cats, civets, and mongooses (i.e., feliforms), related to the fact that the rostrum in cani- forms shows more positive allometry during growth than in feliforms. That is, compared to a cat, a dog shows more growth in the face relative to the braincase during its ontogeny. nose face The possibility that this correlation represents a gen- eral mechanism responsible for at least some aspects of skull growth across non-carnivoran mammals has not yet been thoroughly investigated. Facial shape and length are highly variable in many mammalian clades, including afrotherians (e.g., tenrecs), xenarthrans (e.g., anteaters) and euarchontoglires (e.g., primates). Morphometrically, the skull shows a tremendous amount of continuous Figure 1 Cranial measurements taken in this study. Macaque cranium in (A) ventral
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