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Natural Epigenetic Variation Within and Among Six Subspecies of the House Sparrow, Passer Domesticus Sepand Riyahi1,*,‡, Roser Vilatersana2,*, Aaron W

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Natural Epigenetic Variation Within and Among Six Subspecies of the House Sparrow, Passer Domesticus Sepand Riyahi1,*,‡, Roser Vilatersana2,*, Aaron W © 2017. Published by The Company of Biologists Ltd | Journal of Experimental Biology (2017) 220, 4016-4023 doi:10.1242/jeb.169268 RESEARCH ARTICLE Natural epigenetic variation within and among six subspecies of the house sparrow, Passer domesticus Sepand Riyahi1,*,‡, Roser Vilatersana2,*, Aaron W. Schrey3, Hassan Ghorbani Node4,5, Mansour Aliabadian4,5 and Juan Carlos Senar1 ABSTRACT methylation is one of several epigenetic processes (such as histone Epigenetic modifications can respond rapidly to environmental modification and chromatin structure) that can influence an ’ changes and can shape phenotypic variation in accordance with individual s phenotype. Many recent studies show the relevance environmental stimuli. One of the most studied epigenetic marks is of DNA methylation in shaping phenotypic variation within an ’ DNA methylation. In the present study, we used the methylation- individual s lifetime (e.g. Herrera et al., 2012), such as the effect of sensitive amplified polymorphism (MSAP) technique to investigate larval diet on the methylation patterns and phenotype of social the natural variation in DNA methylation within and among insects (Kucharski et al., 2008). subspecies of the house sparrow, Passer domesticus. We focused DNA methylation is a crucial process in natural selection on five subspecies from the Middle East because they show great and evolution because it allows organisms to adapt rapidly to variation in many ecological traits and because this region is the environmental fluctuations by modifying phenotypic traits, either probable origin for the house sparrow’s commensal relationship with via phenotypic plasticity or through developmental flexibility humans. We analysed house sparrows from Spain as an outgroup. (Schlichting and Wund, 2014). These recent findings about the The level of variation in DNA methylation was similar among the five inheritance of environmentally induced DNA methylation marks house sparrow subspecies from the Middle East despite high over generations have changed our classical views of evolution and phenotypic and environmental variation, but the non-commensal natural selection (e.g. Champagne, 2008). Although the relevance subspecies was differentiated from the other four (commensal) of epigenetic processes in bird evolution is still under debate, the Middle Eastern subspecies. Further, the European subspecies was importance of DNA methylation in natural selection and ecology differentiated from all other subspecies in DNA methylation. Our has been reported in fungi and several other organisms (e.g. Herrera results indicate that variation in DNA methylation does not strictly et al., 2012; Schrey et al., 2013). follow subspecies designations. We detected a correlation between An ideal ecological process to study the role of DNA methylation methylation level and some morphological traits, such as in local adaptation is range expansion, either natural or standardized bill length, and we suggest that part of the high anthropogenic. Epigenetics could explain the success of some of morphological variation in the native populations of the house these expansions, as genetic variability is often decreased by sparrow is influenced by differentially methylated regions in specific bottleneck events and in many cases selection for genetic variants loci throughout the genome. We also detected 10 differentially is unlikely to be directly involved because of the short time scale of Passer methylated loci among subspecies and three loci that differentiated expansions (Schrey et al., 2014). The house sparrow, domesticus between commensal or non-commensal status. Therefore, the MSAP , is a remarkable bird species regarding range expansion technique detected larger scale differences among the European and and adaptation. The species probably originated in the Middle East non-commensal subspecies, but did not detect finer scale differences (e.g. Johnston and Klitz, 1977; Summers-Smith, 1988). Iran is a key among the other Middle Eastern subspecies. place of transition for this species (Vaurie, 1956), and several subspecies evolved in this area, probably because of the complex KEY WORDS: DNA methylation, Environmental adaptation, topographical features of the Iranian plateau (Misonne, 1959). As Commensalism, Phenotypic variation, MSAP several zones of intergradation have been described for the subspecies of house sparrow in this area (Vaurie and Koelz, 1949; Vaurie, 1956), INTRODUCTION the geographic distribution map of the species is approximate (Fig. 1). Epigenetic processes can regulate gene expression in response to The species extended naturally into Eurasia with the aid of human developmental and environmental stimuli (Richards, 2011). DNA commensalism (Summers-Smith, 1988; Anderson, 2006; Sætre et al., 2012). It was later introduced by humans into America, North Africa 1Evolutionary and Behavioural Ecology Research Unit, Natural History Museum of and Australia, now being one of the most broadly distributed Barcelona, Psg. Picasso s/n, 08003 Barcelona, Spain. 2Botanic Institute of vertebrate species (Anderson, 2006). Eleven subspecies have been Barcelona (IBB-CSIC-ICUB), Passeig de Migdia s/n, 08038 Barcelona, Spain. recognized, mainly on the basis of plumage coloration and body size 3Department of Biology, Armstrong State University, Savannah, GA 31419, USA. 4Department of Biology, Faculty of Science, Ferdowsi University of Mashhad, (Vaurie and Koelz, 1949; Vaurie, 1956; Summers-Smith, 1988). An Mashhad 9177 9489 74, Iran. 5Research Department of Zoological Innovations, earlier study on several mitochondrial and nuclear loci revealed that Institute of Applied Zoology, Faculty of Science, Ferdowsi University of Mashhad, human commensalism in the house sparrow has a single origin and Mashhad 9177 9489 74, Iran. *Joint first authors. evolved around 10,000 years ago after the advent of agriculture in the Middle East. According to this study, there is weak genetic ‡ Author for correspondence ([email protected]) structuring among house sparrow subspecies in the Middle East S.R., 0000-0003-3317-3576 (Sætre et al., 2012). In addition, another study which compared the native European population of house sparrow with introduced Received 31 March 2017; Accepted 1 September 2017 populations using microsatellite markers detected high Journal of Experimental Biology 4016 RESEARCH ARTICLE Journal of Experimental Biology (2017) 220, 4016-4023 doi:10.1242/jeb.169268 P. d. domesticus P. d. hyrcanus P. d. bactrianus P. d. biblicus P. d. persicus P. d. tingitanus P. d. indicus P. d. niloticus P. d. hufufae P. d. rufidorsalis Fig. 1. Sampling locations (black dots) and geographical distribution of 10 subspecies of house sparrow, Passer domesticus. Based on Vaurie and Koelz (1949), Vaurie (1956) and Summers-Smith (1988). An additional subspecies (P. d. parkini, from the Himalayas) is not shown on this map. differentiation among all studied native populations of house sparrow, deposited in two different museums. Of these 84 birds, 71 were from although genetic diversity appears to be higher in populations at lower 17 localities in Iran, and encompassed five of the 11 recognized latitudes (Schrey et al., 2011). subspecies: P. d. bactrianus Zarudny and Kudashev 1916 (N=10), The different native subspecies of house sparrow show a high level P. d. biblicus Hartert 1910 (N=17), P. d. hyrcanus Zarudny and of phenotypic variation (e.g. in plumage coloration, body size and Kudashev 1916 (N=4), P. d. indicus Jardine and Selby 1831 (N=16) wing length), which is considered to possibly be the result of and P. d. persicus Zarudny and Kudashev 1916 (N=24). All the adaptation to different environmental conditions (Vaurie, 1956; Iranian birds were collected during 2008–2009 for morphological Anderson, 2006). Outstanding phenotypic differences have also been and parasitological studies and were deposited at the Ferdowsi described between introduced and source house sparrow populations, University of Mashhad (Mashhad, Iran). The Iranian birds were shot supporting the adaptive capacity of the species to respond to novel or by local hunters (in some small cities of Iran, house sparrow is a changing environments (see, for example, Johnston and Selander, culinary delicacy). In addition, muscle tissue from 13 house sparrows 1964, 1973; Johnston and Klitz, 1977; Hamilton and Johnston, 1978; belonging to the P. d. domesticus (Linnaeus 1758) subspecies was Anderson, 2006). The role of epigenetic changes in shaping these obtained from the Natural History Museum of Barcelona (Catalonia, differences, however, remains unknown. Spain). Our study animals comprised 42 males, 33 females and 9 In this study, we estimated genome-wide methylation variation unknown sex, and encompassed different age categories. DNA was within and between five subspecies of house sparrow in the Middle extracted from muscle tissue preserved in pure ethanol at 4°C using East, within the Iranian plateau, to evaluate the role of epigenetic the MasterPure DNA Purification Kit (Epicenter, Madison, WI, variation in local adaptation and rapid expansion of the species in its USA). DNA quality and quantity were verified using a NanoDrop native range. Additionally, we used the subspecies from Spain as an 1000 v.3.7.1 spectrophotometer (Thermo Fisher Scientific, Waltham, outgroup. We searched for intraspecific methylation variation of MA, USA). DNA methylation differs among tissues as a result of house sparrows with the aid of a methylation-sensitive amplified different
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