Water Deer Taxonomy - Korean Cousins?

A single paragraph to the French journal Comptes rendus de l'Académie des Sciences in 1884 by an anonymous author told how, in a letter to renowned French mammologist Alphonse Milne-Edwards, French Jesuit missionary and zoologist Pierre Marie Heude announced to him that he'd received various specimens of a water deer from Korea.

These specimens differed in skull morphology and fur colour to such an extent from Swinhoe's description 14 years earlier that Heude advocated this Korean water deer be considered a new species, proposing the binomen Hydropotes argyropus. There's no information in this short note from where this binomen originates, although it seems plausible it's derived from the Greek argyreios meaning "silvery" and pous meaning "foot" – implying the specimens exhibited lighter coloured feet/legs.

In his Catalogue of Ungulate Mammals, published in 1913, Richard Lydekker synonymised argyropus with inermis, effectively treating the two as a single species, but in a short note in his 1922 paper on the mammals of Korea and Manchuria, Tamezo Mori argued that it should stand as a separate species, as Heude had originally suggested. Later in the 1920s, however, the US National Museum acquired 13 specimens of water deer from China and 11 from Korea. The zoologist Alfred Howell compared these as part of his project to reassess the museum's mammal collection, and was ultimately led to assign the Chinese and Korean samples subspecific standing. Chinese water deer thus became Hydropotes inermis inermis and Korean water deer Hydropotes inermis argyropus – a division still commonly used today. In his paper to the Proceedings of the United States National Museum during 1929, he noted:

"This fine series shows that there is much individual variation in color, and in size of skull, within this genus [sic]."

Nonetheless, it seems that the chief separator here was the colour of the coat, and Howell went on to describe how:

"The form is recognized on the basis of average darker and richer coloration, with more reddish about the head. The skull exhibits no consistent differences."

Much more recently, Yung Kun Kim and colleagues carried out univariate and multivariate analyses of the cranial morphology of 50 Chinese and 45 Korean water deer. The results, published in the Journal of Veterinary Medical Science in 2015, show that the two groups were very similar, with at least 75% overlap, leading them to conclude:

"… these 2 subspecies are not well-differentiated, suggesting that individuals of the 2 populations share common morphological traits".

In 2009, Hung Sun Koh and colleagues at Chungbuk University in South Korea published their genetic analysis of 75 water deer specimens, 30 from three sites in China and 45 samples from five sites in South Korea. The mtDNA control region and cyt b data suggest two distinct forms distributed in two populations: a major group that includes individuals in both China and Korea, and a minor clade that appears unique to Korea. In other words, this sample set implies that Chinese water deer are found in both China and Korea, while "Korean water deer" are found only in Korea. It's important to recognise that these data suggest only that there has been genetic divergence between some populations of water deer in Korea; they don't support the classification of these lineages as separate subspecies. Indeed, in their paper to Biochemical Genetics, Koh and colleagues note that a cyt b genetic distance below 2% falls within the range typically expected for intraspecific variation, and the distance between their major and minor lineages was only 1.3%.

The findings of Koh and his team were substantiated by a team led by Baek-Jun Kim at South Korea's National Institute of Ecology using different genetic markers (D-loop haplotype and median-joining network data). These data, published in Genes and Genetic Systems during 2014, also indicate two water deer lineages: A, which is present in both China and Korea; and B, which is present only in Korea, where it presumably originated. Molecular clock analysis carried out as part of the investigation suggests these lineages separated at some point in the early Pleistocene (around 1.8 mya), when the Korean peninsula was connected with China and undergoing a period of significant climatological fluctuation. The peninsula was cut off from China by the Yellow Sea about 10,000 years ago, preventing further gene flow between the lineages. Again, the genetic distance of these lineages calculated in this study was less than 2%. Subsequently, in their 2015 short communication to Animal Systematics, Evolution and Diversity, Hye Ri Kim and colleagues reported on their mitochondrial cytochrome haplotype analysis of tissues collected from 18 road-killed individuals from two northern forests and one southern forest in South Korea. The analysis clearly separated Korean water deer into two phylogroups, one of which clustered with deer from China, leading the researchers to conclude that both the Chinese and Korean water deer are distributed across South Korea.

Baek-Jun Kim and Hye Ri Kim's findings -- that one Korean phylogroup clusters with Chinese lineages while the other appears Korea-specific, with both present in some sites in South Korea -- seems consistent with colonisation from the south, via the now-submerged land bridge that once connected China to the south-west of the peninsula. This also chimes with observations made by British travel journalist and naturalist Geoffrey Vyvyan Hett in a lecture given to the Royal Central Asian Society in February 1936. Hett, who travelled widely on the peninsula on hunting trips and spoke with locals about the animals they encountered, noted that there were only water deer in the south of Korea, replaced in the north by Siberian roe deer (Capreolus pygargus) and the musk deer (Moschus moschiferus). Based on his analysis of topographical maps, Hett considered this distribution reflected that there was once a land connection between China and the south-west Korean peninsula "by which the southern types of animals could have migrated, while the northern forms entered from Manchuria and the maritime province of East Siberia". Unfortunately, no data exist for populations in what's now North Korea, so it isn't possible to confirm genetically whether a once-distinct northern population (colonised by a different route, as Hett proposed) ever existed there, or how it might relate to the southern lineages.

Whatever the colonisation history of water deer on the peninsula, it's worth distinguishing between the ability of genetic markers to detect a lineage split and whether that split reflects meaningful structure in nature. Data from the 2009 and 2014 studies, along with microsatellite analysis published by Yun-Sun Lee and co-workers at Seoul National University in 2011 -- which found no significant regional or genetic structure differences between the mid-eastern and southwestern populations in South Korea -- and the genomic analysis of Rory Putman and his team published in 2021, suggest that despite the identifiable mitochondrial lineages, there's little pronounced population structure among water deer within Korea – the two lineages are not confined to separate ranges, and gene flow appears to continue between them.

Water deer from China and Korea cannot be confidently distinguished by morphology, and the available genetic data suggest they are best considered a single species. There are some data indicating that water deer in South Korea show lower genetic diversity than those in China, which may hint at early divergence, but this falls well short of justifying subspecific separation.

References

Anon. (1884). Note sur une nouvelle espece d'Hydropotes, par le pere Heude. Comptes rendus de l'Académie des Sciences. t98(16): 1017.

Hett, G.V. (1936). In Korea, 1935. Journal of The Royal Central Asian Society. 23(2): 236-250.

Howell, A.B. (1929). Mammals from China in the Collections of the United States National Museum. Proceedings of the United States National Museum. 75: 1-158.

Kim, B.J. et al. (2014). Mitochondrial genetic diversity, phylogeny and population structure of Hydropotes inermis in South Korea. Genes and Genetic Systems. 89(5): 227-235.

Kim, H.R. et al. (2015). Intraspecific phylogeny of the Korean water deer, Hydropotes inermis argyropus (Artiodactyla, Cervidae). Animal Systematics, Evolution and Diversity. 31(2): 118-121.

Kim, Y.K. et al. (2015). Cranial morphological homogeneity in two subspecies of water deer in China and Korea. Journal of Veterinary Medical Science. 77(11): 1427-1435.

Koh, H.S. et al. (2009). Two sympatric phylogroups of the Chinese water deer (Hydropotes inermis) identified by mitochondrial DNA control region and Cytochrome b gene analyses. Biochemical Genetics. 47: 860.

Lee, Y-S. et al. (2011). Isolation and characterization of 12 microsatellite loci from Korean water deer (Hydropotes inermis argyropus) for population structure analysis in South Korea. Genes & Genomics. 33: 535-540.

Lydekker, R. (1913). Catalogue of Ungulate Mammals - Vol. 4. British Museum.

Mori, T. (1922). LXIV.–On some new mammals from Korea and Manchuria. Annals and Magazine of Natural History. 10(60): 607-614.

Putman, R. et al. (2021). Conservation genetics of native and European-introduced Chinese water deer (Hydropotes inermis). Zoological Journal of the Linnean Society. 191(4): 1181-1191.