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RUNX2 Repeat Variation Does Not Drive Craniofacial Diversity in Marsupials Axel H

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RUNX2 Repeat Variation Does Not Drive Craniofacial Diversity in Marsupials Axel H Newton et al. BMC Evolutionary Biology (2017) 17:110 DOI 10.1186/s12862-017-0955-6 RESEARCH ARTICLE Open Access RUNX2 repeat variation does not drive craniofacial diversity in marsupials Axel H. Newton, Charles Y. Feigin and Andrew J. Pask* Abstract Background: Runt-related transcription factor 2 (RUNX2) is a transcription factor essential for skeletal development. Variation within the RUNX2 polyglutamine / polyalanine (QA) repeat is correlated with facial length within orders of placental mammals and is suggested to be a major driver of craniofacial diversity. However, it is not known if this correlation exists outside of the placental mammals. Results: Here we examined the correlation between the RUNX2 QA repeat ratio and facial length in the naturally evolving sister group to the placental mammals, the marsupials. Marsupials have a diverse range of facial lengths similar to that seen in placental mammals. Despite their diversity there was almost no variation seen in the RUNX2 QA repeat across individuals spanning the entire marsupial infraclass. The extreme conservation of the marsupial RUNX2 QA repeat indicates it is under strong purifying selection. Despite this, we observed an unexpectedly high level of repeat purity. Conclusions: Unlike within orders of placental mammals, RUNX2 repeat variation cannot drive craniofacial diversity in marsupials. We propose conservation of the marsupial RUNX2 QA repeat is driven by the constraint of accelerated ossification of the anterior skeleton to facilitate life in the pouch. Thus, marsupials must utilize alternate pathways to placental mammals to drive craniofacial evolution. Keywords: Marsupial, Craniofacial, Evolution, RUNX2, CBFA1, Repeat variation, Repeat purity Background length and the ratio of polyglutamines (Q) to polyala- Mammals have evolved a diverse array of craniofacial nines (A) in the QA repeat domain of the Runt-related morphologies in response to their specialist diets. Exam- transcription factor 2 (RUNX2) gene [6]. ples of carnivores, omnivores and herbivores have RUNX2 is a transcription factor and master regulator of evolved independently in both the placental (eutherian) osteogenesis in the development of the mammalian skel- and marsupial (metatherian) lineages [1–3] with diet pla- eton [7, 8]. RUNX2 binds the osteoblast-specific cis-acting cing substantial selective pressures on craniofacial evolu- element (OSE-2) within the promoter of several key skel- tion. While there are many key developmental genes etal genes [9]. Mice deficient for Runx2 are unable to de- responsible for patterning the facial skeleton, the precise velop a bony skeleton [7]. In humans, mutations in mechanisms driving these morphological adaptations are RUNX2 cause cleidocranial dysplasia (CCD), with individ- not well defined [4]. One of the most remarkable exam- uals possessing craniofacial abnormalities with delayed ples of craniofacial diversity is between breeds of domes- closure of cranial sutures and dental anomalies [10]. Inter- tic dogs which have been subjected to strong artificial estingly, several of the skeletal abnormalities associated selection [5]. A comparative analysis of repeat variation with CCD patients are characteristic of the Neanderthal in developmental genes associated with skeletal and cra- skeleton, and it has been hypothesized that evolutionary niofacial development was performed across dog breeds changes to RUNX2 played a fundamental role in the with diverse craniofacial phenotypes [6]. A strong posi- phenotypic divergence of modern humans [11]. tive correlation was observed between craniofacial RUNX2 contains several functional domains, including a highly conserved RUNT DNA binding domain and, * Correspondence: [email protected] central to this study, a repetitive glutamine (Q), alanine The School of BioSciences, The University of Melbourne, Victoria 3010, Australia (A) domain [12]. Changes to the length, or ratio, of © The Author(s). 2017 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. Newton et al. BMC Evolutionary Biology (2017) 17:110 Page 2 of 9 sequential glutamines to alanines within RUNX2 alter radiated into a diverse range of terrestrial, aquatic its transactivational activity [13–17] providing a direct and aerial species (for example, rodents, cetaceans link between variation within this domain and cranio- and bats) with each group displaying highly variable facial length in dogs. Amino acid coding repeats are facial morphologies acquired along their own evolu- thought to provide a fast-acting mechanism for gener- tionary trajectories. Although the RUNX2 repeat may ating evolvability. Repeats promote replication slip- drive facial evolution within orders, other compensatory page, resulting in expansions and contractions which epistatic changes may act across larger evolutionary dis- can generate new alleles in rapid succession and pro- tances such that correlations cannot be detected. mote variation [18, 19]. The QA repeat in RUNX2 All studies on RUNX2 repeat length and facial di- provides a mechanism by which rapid morphological versity have been conducted in placental mammals. variation can arise. Such protein coding repeats have However, it is unknown whether a correlation be- been described as “evolutionary tuning knobs” where tween RUNX2 repeat length and facial length exists small, incremental changes can be associated with in their sister group, the marsupials. The marsupials rapid morphological evolution [20, 21]. are a naturally evolving infraclass that split from the Selective pressures over short evolutionary time- placental lineage ~160 million years ago [26] and ra- frames may favour changes in repeat length as a diated into 7 orders distributed through two superor- mechanism to generate rapid morphological change ders (the Australidelphia and Ameridelphia). Like [20, 21]. This may be especially true in the domestic their placental relatives, marsupials have evolved their dogs as they represent a single species that has been own distinct range of adaptive craniofacial morpholo- subjected to intense selective breeding over the past gies suited to their various specialized feeding ecol- century [6]. The RUNX2 QA repeat and facial length ogies (Fig. 1a-j, [1–3]). Marsupials occupy a diverse was investigated across distinct placental orders to de- range of facial lengths but show a reduced range of termine if repeat evolution correlates with facial overall craniofacial diversity when compared to pla- morphology in naturally evolving taxa over larger evo- cental mammals (Fig. 1m; [1]). Within marsupials lutionary timeframes. The QA-repeat and facial-length there are also several cases of convergent craniofacial was recorded across the carnivorans, the order in phenotypes with the placentals (Fig. 1i-l). The extinct thy- which the dogs and other canids are phylogenetically lacine and the canids represent one of the most extraor- distributed [14]. As seen in the domestic dogs (a sin- dinary examples of convergence in mammals especially in gle species), there was a positive correlation between their craniofacial morphology (C.Y. Feigin, A.J. Pask per- the RUNX2 QA repeat length and facial length within sonal communication). Here we test whether variation to this order, despite over 40 million years of evolution the RUNX2 repeat can explain facial length variation be- [14]. It was also noted that this correlation was stron- tween individuals throughout the various orders and fam- ger in members of the Caniformia who exhibit allo- ilies of marsupials, and across the marsupial infraclass. metric craniofacial development and higher overall Surprisingly, in contrast to the placental mammals, craniofacial diversity. In addition, the RUNX2 repeat marsupials possess almost no variability in the to facial length ratio was also examined across an- RUNX2 repeat length or composition across individ- other placental order, the Primates, who have been uals at the genus, family and order level. Despite their evolving for 55 million years [22]. Primates, like the diverse array of facial morphologies, marsupials have Carnivora, display a similar positive correlation be- not utilized evolutionary changes to the RUNX2 re- tween the RUNX2 repeat and facial length [23]. An peat to control their facial length development. analysis of the RUNX2 repeat to facial length was conducted across the three extant lineages of placen- Results tal mammals including the Afrotheria, Boreoeutheria Marsupials display a wide range of craniofacial diversity including Euarchontoglires (Primates, Rodents) and The marsupials display a wide range of adaptive cranio- Laurasiatherians (Ungulates, Carnivora), and the facial morphologies (Figs. 1 and 2), corresponding to Xenartha. While a correlation could be observed be- their various diets. As expected, the marsupials display tween the RUNX2 repeat and facial length within spe- a diverse range of facial lengths, which are consistent cific orders, this relationship did not hold true when with the range
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