Return.... to the world of sheep

My plan at the moment (in terms of blog-related writing) is to do nothing other than complete all those nearly-finished articles that I've been promising to do over the last weeks... or months... We begin with the second post on sheep, thereby completing what I started in the first sheep post (the first post is required reading before you launch into this one). As discussed back then, sheep are generally divided into three genetic groups: the Asian argaliforms, the mouflon-like moufloniforms, and the mostly American pachyceriforms. I covered the argaliforms last time and, of the pachyceriforms, got as far as introducing, and saying stuff about accidental falls and homosexuality, in Bighorn Ovis canadensis. The aim here is to finish dealing with pachyceriforms and to then get through the moufloniforms. Covering the latter group means including the confusing and complex story of sheep domestication... [in adjacent photo, the lamb skull at the front, and the big-horned ram, are Soay sheep; the other two are blackfaced sheep from Dartmoor. PS: note the small supraorbital foramina compared to McGowan's mystery bovid]

Given their wide distribution and habitat choice, bighorns are quite variable in size and morphology, and desert-dwelling forms are smaller, and with flatter, less widely spreading horns that mountain-dwelling populations. Though seven subspecies have been named, including four desert-dwelling forms and the extinct Audubon's bighorn O. c. auduboni, recent studies have indicated that only three can be supported: the Rocky Mountain bighorn O. c. canadensis, Sierra Nevada bighorn O. c. sierrae and Desert bighorn O. c. nelsoni (Wehausen & Ramey 1993, 2000, Wehausen et al. 2005). The idea that bighorns (and other sheep) are phenotypically 'plastic' is supported by data on how much sexual dimorphism occurs when populations become crowded. LeBlanc et al. (2001) showed that body mass in both sexes was depressed when population densities were high, leading to a decline in sexual size dimorphism between 2-yr-olds. While males were unable to 'catch up' with the disadvantaged growth rate they experienced as lambs, females underwent compensatory growth, so the population ended up with relatively large females compared to relatively small males.

Closely related to the bighorns is O. dalli, a species often known as Dall's sheep. However, the 'correct' name for O. dalli is actually Thinhorn sheep and, within this species, Dall's sheep is a subspecies (O. d. dalli) [shown in adjacent image]. The other subspecies is the slightly larger and more robust Stone sheep O. d. stonei, named for Montana naturalist A. J. Stone (and not for small rocks). The validity of the Stone sheep has been controversial and it and Dall's sheep grade into one another in NW British Columbia and central Yukon. Most recently, Stone and Dall's sheep were supported as valid taxa by Worley et al. (2004). Thinhorn sheep are northern specialists of British Columbia, the Yukon Territory and Alaska. While Dall's sheep is white, Stone sheep range from off-white in the north to grey and blackish further south.

Snow sheep

Bighorns and thinhorns share a number of genetic and morphological characters and form the pachyceriform clade, and they've also been given their own subgenus within Ovis, Pachyceros. Though sometimes called American sheep, there is in fact an Asian species that also seems to be part of the group: the Snow sheep O. nivicola of Siberia, sometimes called the Siberian or Asiatic bighorn and even included by some workers in the same species as the bighorn. It's true that Snow sheep are highly similar to Alaskan bighorns, but while bighorns have 54 chromosomes, Snow sheep have 52 (though read on), so they are now thought quite distinct. It's been suggested that bighorn and thinhorn sheep descend from a snow sheep-like ancestor that invaded Beringia and then moved south into North America, though some workers think that things likely occurred the other way round, with Asian snow sheep descended from a bighorn-like pachyceriform that re-invaded Asia.

Bunch et al. (2006) presented data suggesting that O. nivicola is not a clade, as while some snow sheep formed a sister-group to bighorns and thinhorns, others were at the base of the clade that includes argaliforms and moufloniforms. Geist (1991) and Bunch et al. (2006) speculated that the Kamchatka sheep O. n. nivicola [shown in adjacent image] might share 54 chromosomes with bighorns and thinhorns, and hence prove particularly close to these American species. Some of this data might mean that one or some snow sheep populations deserve recognition as distinct species-level taxa.

And on that note, snow sheep are polytypic, with between two and six subspecies being recognised by different researchers. I just know you want to see those listed, so: Kamchatka sheep O. n. nivicola, Koryak O. n. koryakorum, Okhotsk sheep O. n. alleni, Yablonov sheep O. n. potanini, Putorian sheep O. n. borealis and Yakut sheep O. n. lydekkeri. If we ever do get to the stage where people decide that the 'subspecies' concept is useless and that any such taxa should be classified as species, we're clearly going to see a massive surge in the recognised number of extant sheep taxa. Like, from seven or eight species to over 30 or something. Yikes.

The mouflons

Finally, we come to the moufloniforms. This group is named for the Mouflon O. musimon Blyth, 1811 or O. gmelini Blyth, 1841*, the smallest of wild sheep (c. 25-55 kg), of Iran, Iraq, Turkey, Corsica, Sardinia and Cyprus [captive individual shown in adjacent image]. Six subspecies have been named. Closely related, and sometimes regarded as conspecific with O. gmelini/musimon, is the Asian mouflon O. orientalis. While it used to be thought that the mouflons of Europe were truly wild sheep, it now seems that most or all of them are Neolithic ferals descended from O. orientalis, though note that this does not apply to all mouflon populations and that those of Turkey, Iran and elsewhere might be truly wild. The mouflons on Corsica and Sardinia appear to have been introduced to the islands about 6000 years ago. There is a huge amount of disagreement as to the taxonomy and relationships of these sheep - for fear of adding another 1000 words to the post I am going to avoid it.

* Though O. musimon is older, many sheep experts now seem to prefer O. gmelini. I think this is because the type for the latter name is more clearly linked to a potentially wild mouflon population (rather than a feral or hybrid population), though I'm not sure.

Domestic sheep: confusing multiple origins

How do domestic sheep O. aries fit into all this? Archaeological evidence suggests that sheep were first domesticated in the Fertile Crescent somewhere around 9000 years ago (though some workers suggest an origin about 11,000 years ago) and, while it is generally agreed that domestic sheep are moufloniforms, beyond that there this is some controversy as to their origins. It's been proposed that Asiatic mouflon or urial might have been their ancestors, and/or that argali genes had been introduced into domesticated urial (for discussion of argali and urial, see the first sheep post). Stefan Hiendleder and colleagues found that the domestic sheep of Europe and Asia differ in mtDNA, with European domestic sheep being close to European mouflon while Asian domestic sheep were not only strongly divergent from mouflon, but also from urial and argalis, and thus must have been domesticated from as an-yet-unknown wild ancestor (Hiendleder et al. 1998, 2002). These two well-separated mitochondrial lineages (dubbed Group A and Group B) had become distinct well prior to 11,000 years ago. Group B is the one that shares haplotypes with mouflon, with wild populations present in Turkey and Iran being regarded as the most likely sources for origination of Group B domestic sheep [adjacent photo shows Soay sheep, one of the most primitive living breeds of European sheep].

By 2005, a third distinct domestic sheep lineage - Group C - was reported in Chinese and Turkish sheep (Guo et al. 2005, Pedrosa et al. 2005). Tapio et al. (2006) looked at mitochondrial variation in domestic sheep across Europe, the Caucasian region and central Asia, and found another distinct lineage - Group D - in a sheep from the north Caucasus. Meadows et al. (2007) further complicated this story by documenting a fifth distinct ovine mitochondrial lineage: Group E.

Paralleling studies of domestic cattle, goat, pig, horse, donkey and chicken, it now seems that sheep were domesticated on multiple occasions from several different wild populations, and that domestic sheep ancestry involves as-yet-unidentified wild ancestral populations. In fact perhaps the single most significant discovery from recent genetic studies of domestic animals is that domestic 'species' have arisen from multiple different local domestication events, and only rarely from single events (though the latter have been documented: in yaks for example (Guo et al. 2006).

While Group B sheep (the group that includes most European domestic sheep breeds) are tied to European mouflon, and hence most likely share an ancestor that was a sort of wild, proto-mouflon, the wild ancestors of Group A, C, D and E sheep all remain unknown, and genetic distances show that these wild ancestors were not urial or argali as used to be thought. The most likely hypothesis is that these distinct domestic sheep matrilines descended from wild moufloniform populations that are now extinct. The good news is that the evidence for these populations hasn't necessarily disappeared, as there is a vast amount of unsampled archaeological sheep specimens: as Meadows et al. (2007) suggested, 'perhaps the next phase in mtDNA discovery should be aimed at ancient DNA from the Fertile Crescent' (p. 1378) [another Soay sheep shown in adjacent image].

Sheep taxonomy, ancestry and phylogeny is far from resolved, and we have much to learn about the relationships between living species, and huge holes remain in our understanding of the history of domestic breeds. That might be surprising in such a ubiquitous and familiar group of animals - or does it highlight how much we have yet to learn about even the most mundane of beasts?

Incidentally, for those who follow various of the discussions that we have here at Tet Zoo, keep an eye on Picture of the day # 14 for more on the maximum authenticated size of Crocodylus porosus. I have recently added a few new bits of information to the post on Peter Hocking's big cats (including a mention of the alleged African tiger Panthera tigris senegalensis), and Marc van Roosmalen has recently sent me a new, very long piece of text on his new Amazonian mammals that I will adapt and publish on the blog soon.

Refs - -

Bunch, T. D., Wu, C., Zhang, Y.-P. & Wang, S. 2006. Phylogenetic analysis of snow sheep (Ovis nivicola) and closely related taxa. Journal of Heredity 97, 21-30.

Geist, V. 1991. On the taxonomy of giant sheep (Ovis ammon Linnaeus, 1766). Canadian Journal of Zoology 69, 706-723.

Guo, J., Du, L. X., Ma, Y. H., Guan, W. J. & Li, H. B., Zhao, Q.-J., Li, X & Rao, S.-Q. 2005. A novel maternal lineage revealed in sheep (Ovis aries). Animal Genetics 36, 331-336.

- ., Savolainen, P., Su, J., Zhang, Q., Qi, D., Zhou, J., Zhong, Y., Zhao, X. & Liu, J. 2006. Origin of mitochondrial DNA diversity of domestic yaks. BMC Evolutionary Biology 2006, 6: 73.

Hiendleder, S., Kaupe, B., Wassmuth, R. & Janke, A. 2002. Molecular analysis of wild and domestic sheep questions current nomenclature and provides evidence for domestication from two different subspecies. Proceedings of the Royal Society of London B 269, 893-904.

- ., Mainz, K., Plante, Y. & Lewalski, H. 1998. Analysis of mitochondrial DNA indicates that domestic sheep and derived from two different ancestral maternal sources: no evidence for contributions from Urial and Argali sheep. The Journal of Heredity 89, 113-120.

LeBlanc, M., Festa-Bianchet, M. & Jorgenson, J. T. 2001. Sexual size dimorphism in bighorn sheep (Ovis canadensis): effects of population density. Canadian Journal of Zoology 79, 1661-1670.

Meadows, J. R. S., Cemal, I., Karaca, O., Gootwine, E. & Kijas, J. W. 2007. Five ovine mitochondrial lineages from sheep breeds of the near east. Genetics 175, 1371-1379.

Pedrosa, S., Uzun, M, Arranz, J.-J., Gutiérrez-Gil, B., San Primitivo, F. & Bayón, Y. 2005. Evidence of three maternal lineages in near eastern sheep supporting multiple domestication events. Proceedings of the Royal Society of London B 272, 2211-2217.

Tapio, M., Marzanov, N., Ozerov, M., Cinkulov, M., Gonzarenko, G., Kiselyova, T., Murawski, M., Viinalass, H. & Kantanen, J. 2006. Sheep mitochondrial DNA variation in European, Caucasian, and central Asian areas. Molecular Biology and Evolution 23, 1776-1783.

Wehausen, J. D., Bleich, V. C. & Ramey, R. R. 2005. Correct nomenclature for Sierra Nevada bighorn sheep. California Fish and Game 91, 216-218.

- . & Ramey, R. R. 1993. A morphometric reevaluation of the Peninsular bighorn subpecies. Transactions of the Desert Bighorn Council 37, 1-10.

Worley, K., Strobeck, C., Arthur, S., Carey, J., Schwantje, H., Veitch, A. & Coltman, D. W. 2004. Population genetic structure of North American thinhorn sheep (Ovis dalli). Molecular Ecology 13, 2545-2556.