Sunday, January 1, 2017

Artiodactyla: Even-toed Ungulates

Artiodactyla is the order of mammals which includes modern pigs, peccaries, hippos, deer, antelope, giraffes, and cattle. Members of this group are characterized by having limbs in which the main weight of the body is equally distributed through the third and fourth digits of each foot. As a result, these animals have a tendency to reduce the number of functional toes from five to just four or two. For this reason, artiodactyls are commonly referred to as the “even-toed ungulates”. Perissodactyls, the “odd-toed ungulates”, differ in that the main weight of the body is distributed through the third digit with the number of functional toes being reducd down to three or one. The name Artiodactyla was coined by the renowned English scientist Sir Richard Owen in 1848: derived from the Greek words artios, meaning “even”, and daktulos, meaning “finger”. Cetaceans (whales, dolphins, and porpoises) descended from early artiodactyls during the Eocene and are close relatives of hippos, leading some authors to combine the Cetacea and Artiodactyla into a common order known as “Cetartiodactyla”.

Illustration showing the foot anatomy of modern artiodactyls: (1) the foot with four
functional toes as demonstrated by the hippo, (2) the more common cloven-hoofed foot
in which there are always have two functional toes with reduced or absent lateral
toes, and (3) the padded foot which is found only among camels. In all cases,
the central third and fourth digits support the main body weight and the first
digits are always absent, resulting in an even number of toes.

The first artiodactyls are known to have lived in Europe during the early Eocene, a time when perissodactyls were the dominant terrestrial herbivores. The oldest known artiodactyl, Diacodexis (Dichoubunidae), was a rabbit-sized animal with bunodont dentition. Already, its limbs anatomy was highly modified for running with specializations that would be inherited by all later artiodactyls. The first cetaceans appear in the fossil record shortly thereafter, but these highly derived animals will be covered in a separate blog post. Disregarding their aquatic relatives, artiodactyls are among the most successful order of mammals, having diversified in the past 10 million years into a wide array of families, subfamilies, tribes, and genera, native to every continent except Antarctica and Australia. There are 10 modern families with 240 species between them. The order is subdivided into four suborders: Whippomorpha, Suina, Tylopoda, and Ruminata.

Whippomorpha- Whippomorpha is a group which contains the earliest artiodactyls and cetaceans. Traditionally, the families Hippopotamidae (hippos), Anthracotheriidae (anthracotheres), and Entelodontidae (entelodonts) were been placed within the Suina for morphological reasons. However, a 2009 study of artiodactyl phylogeny has since found that these three families, together with the middle Eocene predator Andrewsarchus mongoliensis, are much more closely related to Cetacea than they are to other artiodactyls. Barring the cetaceans, members of this group are the least derived among the artiodactyls with a history dating back to the early Eocene.

Representatives of the suborder Whippomorpha. This group
includes hippos (top-left), cetaceans (top-right), entelodonts
(bottom-left), and the middle Eocene predator Andrewsarchus
(bottom-right) among others.

Suina- The Suina, or “pig-like artiodactyls”, contains the modern families Suidae (pigs) and Tayassuidae (peccaries). These animals are characterized by having relatively robust heads with specialized nasals which support a distinctive snout which ends in a disc-shaped nose. Their bodies are typically robust, and cursorial adaptations are minimal. These animals first originated in the Northern Hemisphere during the early Oligocene. Members of this group may be either hypocarnivores or specialized herbivores.

Representatives of the suborder Suina: pigs (left) and peccaries (right).

Tylopoda- The Camelidae (camels) are the sole modern representatives of the group Tylopoda, a group which branched away from other artiodactyls during the middle Eocene. Extinct members of this group include the endemic European families Xiphodontidae and Cainotheriidae and the endemic North American families Protoceratidae and Merycoidodontidae. The latter family were once erroneously placed within the Suina due to their common, yet inaccurate description of “ruminating hogs”.

Representatives of the suborder Tylopoda. This group includes modern camels
(top-left), and the extinct protoceratids (top-right), oreodonts (bottom-left),
and cainotheres (bottom-right).

Ruminata- At present, the Ruminata (ruminants) are the most diverse group of ungulates, comprising nearly 200 modern species divided among the families Tragulidae (chevrotains), Moschidae (musk deer), Cervidae (deer), Antilocapridae (pronghorns), Giraffidae (giraffes), and Bovidae (antelopes and cattle). Extinct families include Hypertragulidae, Gelocidae, and Palaeomerycidae. The word ruminant is derived from the Latin word ruminare, meaning to chew over again, describing the unique method in which these animals digest their food. Rumination is a multi-step process which involves a complex, four-chambered stomach: 
  • First, food is consumed and stored in the first and largest chamber (rumen) where it mixes with saliva and microorganisms which begin to breakdown the tough cell walls of the plants.
  • After feeding, this stored food will gradually be regurgitated and rechewed over a period of time to allow further breakdown of plant fibers, as demonstrated here
  • The "cud" is then reswallowed and transferred to the second chamber (reticulum) where smaller, unwanted debris is trapped.
  • Food is then passed to the third chamber (omasum) where any large particles are broken up and moisture is absorbed.
  • Finally, the food travels to the fourth chamber (abomasum), or the "true stomach", where it is exposed to digestive enzymes and acids before it enters the small intestine. 
Click here for a more detailed description of the anatomy and function of the ruminant digestive tract. Through this process, ruminants are able to 1) quickly consume large quantities of food at a given time to be digested at a later period and 2) to extract nutrients from their food more efficiently than competing herbivores. 

Illustration showing the basic structure and organization
of the multi-chambered ruminant stomach. Wiki.

Most ruminants lack upper incisors, instead having a toughened pad which occludes with the lower incisors. The cuboid and navicular bones of the hindfoot have fused together, forming the cubonavicular bone. Additionally, many ruminant families have independently evolved paired head projections used for species identification, gender identification, and combat (horns, antlers, pronghorns, or ossicones). The first true ruminants appear in the fossil record at the end of the Eocene and underwent a gradual increase in diversity from the Miocene onward.

Representatives of the suborder Ruminata: pronghorns (top-left), deer (top-middle),
giraffes (top-right), chevrotains (bottom-left), musk deer (bottom-middle), and bovids

Defining Characteristics
All artiodactyls (including the earliest cetaceans) share a double-hinged astragalus* that features two symmetrical, pulley-shaped surfaces. This innovation has provided significant advantages for cursoriality: it restricts movement of the foot to the vertical plane and allows leverage to be altered as required. This adaptation is similar to the mechanism possessed by perissodactyls, albeit somewhat more sophisticated. Artiodactyls also share with perissodactyls a reduction or loss of the clavicle (collar bone) which allows them to maximize their stride length while running. The first digit (the equivalent of our thumbs and big toes) is absent in all species. Most artiodactyls have “cloven hooves”; having unguligrade feet in which the weight-bearing third and fourth digits are enlarged while the lateral digits are reduced or absent depending. Among modern species, only hippos have functional lateral digits that actively play a role in locomotion. Camels have a unique foot morphology in which the toes splay out and the body weight is supported by fatty pads, making them effectively digitigrade.

Astragali from the early whale Pakicetus (left), and a modern pig (middle)
and deer (right). Note that both ends of the astragali have a pulley-shaped
articular surface, a unique and defining feature of the order Artiodactyla.

  • Whippomorpha
    • Dichoubunidae: early Eocene to late Oligocene
    • Entelodontidae (entelodonts): late Eocene to middle Miocene
    • Anthracotheriidae: middle Eocene to late Pliocene
    • Hippopotamidae (hippos): middle Miocene to present
  • Suina
    •  Suidae (pigs): early Oligocene to present
    • Tayassuidae (peccaries): late Oligocene to present
  • Tylopoda
    • Protoceratidae: middle Eocene to early Pliocene
    • Camelidae (camels): middle Eocene to present
    • Xiphodontidae: late Eocene to late Oligocene
    • Cainotheriidae: Eocene to early Miocene
  • Ruminata
    • Hypertragulidae: middle Eocene to middle Miocene
    • Tragulidae (chevrotains): Oligocene to present
    • Gelocidae: Eocene to late Miocene
    • Moschidae (musk deer): early Miocene to present
    • Palaeomerycidae: Eocene to Miocene
    • Cervidae (deer): early Oligocene to present
    • Giraffidae (giraffes): early Miocene to present
    • Antilocapridae (pronghorns): early Miocene to present
    • Bovidae (antelopes): early Miocene to present

Astragalus: the ankle bone which connects the foot to the rest of the leg.

References & Further Reading
Spaulding M, O’Leary MA, Gatesy J (2009). “Relationships of Cetacea (Artiodactyla) among mammals: increased taxon sampling alters interpretations of key fossils and character evolution”. PLoS ONE 4(9): e7062 <Full Article>

Thewissen JGM, Cooper LN, Clementz MT, Bajpai S, Tiwari BN (2007). "Whales originated from aquatic artiodactyls in the Eocene epoch of India". Nature 450: 1190-1194 <Abstract>

Price SA, Bininda-Emonds O, Gittleman JL (2005). "A complete phylogeny of the whales, dolphins and even-toed hoofed mammals (Cetartiodactyla)". Biological Reviews 80(3): 445-73 <Full Article>

Gatesy J, Milinkovitch M, Waddell V, Stanhope M (1999). “Stability of cladistics relationships between Cetacea and higher-level artiodactyl taxa”. Systematic Biology 48(1): 6-20 <Full Article>

Montgelard C, Catzeflis FM, Douzery E (1997). “Phylogenetic relationships of artiodactyls and cetaceans as deduced from the comparison of cytochrome b and 12S rRNA mitochondrial sequences”. Molecular Biology and Evolution 14(5): 550-559 <Full Article>

Gatesy J, Hayashi C, Cronin MA, Arctander P (1996). "Evidence from milk casein genes that cetaceans are close relatives of hippopotamid artiodactyls" Molecular Biology and Evolution 13(7): 954-963 <Full Article>

Graur D, Higgins DG (1994). “Molecular evidence for the inclusion of cetaceans within the order Artiodactyla”. Molecular Biology and Evolution: 357-364 <Full Article>

Rose KD (ed). 2006. The Beginning of the Age of Mammals. The John Hopkins University Press, Baltimore, Maryland:243-257 <Book>

Macdonald DW (ed). 2006. The Princeton Encyclopedia of Mammals. Princeton University Press, Princeton, New Jersey <Book>

Augusti J, Anton M (2002). Mammoths, Sabertooths, and Hominids: 65 Million Years of Mammalian Evolution in Europe. Columbia University Press, New York: 36-37 <Book>

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