Proboscidea

Proboscidea (from the Ancient Greek proboskis, "front-feeder" or "trunk," coined by Carl Illiger in 1811) is the order of placental mammals (Afrotheria, Mammalia) that comprises the largest living terrestrial animals on Earth: the three extant species of elephants in family Elephantidae—the African savanna (bush) elephant (Loxodonta africana), the African forest elephant (Loxodonta cyclotis, proven by nuclear genomics to be a distinct species that diverged ~2.6–5.6 million years ago; Roca et al., 2001; Rohland et al., 2010), and the Asian elephant (Elephas maximus)—together with more than 180 extinct Cenozoic species of woolly and Columbian mammoths (Mammuthus)†, straight-tusked elephants (Palaeoloxodon)†, mastodons (Mammut)†, gomphotheres†, and deinotheres†.

Within the placental mammal tree, Proboscidea belongs to the ancient Gondwanan superorder Afrotheria, nested inside the clade Paenungulata ("near-ungulates") as the sister order to Sirenia (manatees and dugongs) and Hyracoidea (rock hyraxes, Procavia capensis)—meaning that a 4-kilogram rabbit-sized rock hyrax and an aquatic manatee are the closest living evolutionary relatives of a 6,000-kilogram African elephant!

1. The Prehensile Muscular-Hydrostat Proboscis (Trunk): Formed by the developmental fusion and extreme elongation of the nose and upper lip (while the external bony nostrils are retracted high onto the forehead), the elephant trunk is the most versatile boneless prehensile organ in the vertebrate kingdom. Containing zero bones and zero cartilage along its length, the trunk operates as a constant-volume muscular hydrostat (William M. Kier & Kathleen K. Smith, 1985; Dagenais et al., 2021) composed of ~90,000 to 150,000 muscle fascicles arranged across longitudinal, radial, and opposingly wound helical layers, innervated by a facial (VII) and trigeminal (V) infraorbital nerve bundle thicker than the elephant's entire spinal cord! Capable of uprooting a 250-kg tree, sucking up 8–10 liters of water at inhalation velocities of 150 m/s, or picking up a single tortilla chip without cracking it (using two opposable finger-like projections on the trunk tip in Loxodonta vs. a single dorsal finger in Elephas), the trunk also houses ~2,000 functional olfactory receptor (OR) genes—the largest olfactory receptor gene repertoire ever sequenced in any animal (Niimura et al., 2014, >5× that of humans and >2× that of bloodhound dogs!).
2. Hypertrophied Second Upper Incisor Ivory Tusks (Schreger Lines): Contrary to popular belief, elephant tusks are not canine teeth—they are ever-growing (hypselodont) second upper incisors (I²) (while all canines, lower incisors, and other upper incisors were lost in modern elephants!). Once a small deciduous milk tusk is shed at age 1, the permanent tusk grows continuously at ~15–18 cm per year from an open vascular pulp cavity and is composed of dentine (ivory) reinforced by a microscopic, three-dimensional crisscrossing weave of collagen fibrils and dentinal tubules that create a diagnostic checkerboard pattern of intersecting chevrons in cross-section (Schreger lines, whose outer intersection angles exceed >115° in extant Loxodonta and Elephas ivory vs. <90° in extinct Mammuthus mammoth ivory, used by forensic wildlife customs officers to distinguish illegal elephant ivory from fossil mammoth ivory!). Under intense selective pressure from 20th-century ivory poaching during the Mozambican Civil War (1977–1992), Shane Campbell-Staton and colleagues (Science, 2021) demonstrated that female African savanna elephants in Gorongosa National Park underwent a rapid evolutionary sweep increasing natural congenital tusklessness from 18.5% to 50.9%, driven by an X-linked dominant, male-lethal mutation in the dental ameloblast/odontoblast gene AMELX!
3. Horizontal "Conveyor-Belt" Molar Replacement (Mesial Drift): Whereas nearly all other mammals replace their milk teeth vertically from underneath (vertical replacement) and then must make one permanent set of adult molars last their entire lifespan, elephants, mammoths, and manatees evolved horizontal conveyor-belt molar progression:
   • At any given moment, an elephant has only one (or parts of two) massive, brick-sized grinding molars in use in each jaw quadrant!
   • Each elephantidae molar is a lamellate composite built from 12 to 30 transverse plates of hard enamel filled with dentine and embedded in a block of cementum (acting like a giant cheese grater to shred coarse fibrous grass and bark).
   • As the front molar is worn down to its roots by chewing 150–200 kg of vegetation per day, a new, larger molar forms at the very back of the jaw and pushes slowly forward (mesial drift) like a grocery-store conveyor belt, spitting out the worn front stub! Over a 60- to 70-year lifespan, an elephant cycles through six successive sets of four molars (M1 → M2 → M3 → M4 → M5 → M6): once the sixth and final set (M6, weighing 4–5 kg each) wears flat around age 60–65, wild elephants can no longer chew tough forage and die of malnutrition.
4. Graviportal Limbs, Obliterated Pleural Cavity, and Seismic Rayleigh-Wave Communication:
   • Obliterated Pleural Space: Unique among mammals, elephants obliterate their pleural cavity before birth—fusing the visceral and parietal pleura of the lungs directly to the chest wall and diaphragm with dense elastic connective tissue! As shown by John B. West (2001), this prevents the high negative hydrostatic pressure generated when an elephant snorkels underwater with its trunk held 2 meters above the surface from rupturing pulmonary pleural capillaries into fatal pleural effusion!
   • Infrasonic and Seismic Communication: In addition to airborne infrasound rumbles (14–35 Hz) discovered by Katharine B. Payne (1986) that travel 5–10 km through the savanna boundary layer, Caitlin E. O'Connell-Rodwell (2000–2007) proved that vocalizing and foot-stamping elephants couple seismic Rayleigh waves (10–40 Hz) into the ground that travel 16 to 32 km through soil and are detected by distant herds via bone conduction (through enlarged middle-ear ossicles) and dense Pacinian corpuscles embedded around the cushioned fat pad of the elephant's feet!

A 5,000-kilogram elephant has ~100 times more cells than a human and lives for 60 to 70 years—yet lifetime cancer mortality in elephants is estimated at <5% (compared to ~17–25% in humans)! In 2015 and 2018, Joshua D. Schiffman, Carlo C. Maley, Lisa M. Abegglen, and Vincent J. Lynch, Juan Manuel Vazquez, and colleagues discovered how Proboscidea evolved reinforced tumor suppression as body size expanded from 5 kg in Eocene Eritherium to 5,000+ kg in modern elephants:

1. 20 Copies (40 Alleles) of the TP53 ("Guardian of the Genome") Tumor-Suppressor Gene: Whereas humans, mice, and rock hyraxes have only 1 copy (2 alleles) of the TP53 gene, African and Asian elephants carry 20 copies (40 alleles) of TP53—1 ancestral canonical gene plus 19 retrotransposed pseudogene/retrogene copies (TP53RTG1–19) that accumulated step-by-step across the Cenozoic in direct lockstep with fossil proboscidean body-size expansion! When an elephant cell suffers ionizing-radiation or chemical DNA damage, these TP53RTG decoys bind and inhibit the negative regulator MDM2, sensitizing the canonical p53 protein so the damaged elephant cell immediately executes programmed cell death (apoptosis) at 2- to 5-fold higher rates than human cells rather than risking mutagenic DNA repair (Abegglen et al., 2015; Sulak et al., 2016)!
2. Resurrection of the "Zombie Gene" LIF6: In 2018, Vazquez, Sulak, Chigurupati, and Lynch discovered that elephants also duplicated the Leukemia Inhibitory Factor (LIF) locus 7–11 times: one duplicate copy, LIF6, had been a dead, un-transcribed pseudogene in ancestral Paenungulates until the proboscidean lineage evolved a new p53-binding response element upstream of LIF6—re-awakening LIF6 as a p53-inducible "zombie gene" whose protein translocates straight to the outer mitochondrial membrane to trigger Bax/Bak pore formation and apoptosis whenever DNA is damaged!

How did dwarf elephants no bigger than a calf or golden retriever evolve on Mediterranean and Indonesian islands?

During the Pleistocene, elephants (Palaeoloxodon and Stegodon) repeatedly swam across narrow sea straits (modern elephants are superb distance swimmers, using their buoyant lungs and snorkel trunks to swim up to 48 km at a time!) to colonize isolated islands in the Mediterranean (Sicily, Malta, Cyprus, Crete, and Tilos) and Indonesia (Flores). On islands lacking large predators and with limited total forage, Insular Dwarfism (Foster's Rule) selected rapidly for extreme body-size reduction: on Sicily and Malta, the giant 10-ton continental straight-tusked elephant (Palaeoloxodon antiquus) shrank over just a few hundred thousand years into the Sicilian dwarf elephant (Palaeoloxodon falconeri)—which stood only 90 centimeters (3 feet) tall at the shoulder and weighed ~100–200 kg (1% of its ancestor's mass!)!

1. Payne, K. B., Langbauer, W. R., Jr., & Thomas, E. M. (1986). Infrasonic calls of the Asian elephant (Elephas maximus). Behavioral Ecology and Sociobiology, 18(4), 297–301. doi:10.1007/BF00300007
2. Roca, A. L., Georgiadis, N., Pecon-Slattery, J., & O'Brien, S. J. (2001). Genetic evidence for two species of elephant in Africa. Science, 293(5534), 1473–1477. doi:10.1126/science.1059936
3. Rohland, N., Reich, D., Mallick, S., Meyer, M., Green, R. E., Georgiadis, N. J., ... & Hofreiter, M. (2010). Genomic DNA sequences from mastodon and woolly mammoth reveal deep speciation of forest and savanna elephants. PLOS Biology, 8(12), e1000564. doi:10.1371/journal.pbio.1000564
4. Abegglen, L. M., Caulin, A. F., Chan, A., Lee, K., Robinson, R., Campbell, M. S., ... & Schiffman, J. D. (2015). Potential mechanisms for cancer resistance in elephants and comparative cellular response to DNA damage in humans. JAMA, 314(17), 1850–1860. doi:10.1001/jama.2015.13134
5. Vazquez, J. M., Sulak, M., Chigurupati, S., & Lynch, V. J. (2018). A zombie LIF gene in elephants is upregulated by TP53 to induce apoptosis in response to DNA damage. Cell Reports, 24(7), 1765–1776. doi:10.1016/j.celrep.2018.07.042
6. Campbell-Staton, S. C., Arnold, B. J., Gonçalves, D., Granli, P., Poole, J., Long, R. A., & Pringle, R. M. (2021). Ivory poaching and the rapid evolution of tusklessness in African elephants. Science, 374(6566), 483–487. doi:10.1126/science.abe7389