Evolution of cetaceans

thumb|right|320px|Species of the infraorder Cetacea

thumb|right|320px|A [[phylogenetic tree showing the relationships among cetacean families. ]]

The evolution of cetaceans is thought to have proceeded in modern day Pakistan during the Eocene epoch (56–34 mya), the second epoch of the Paleogene period of the present-extending Cenozoic Era. Specifically, cetaceans are thought to have transitioned from land to water at the tailend of the Paleocene–Eocene transition about 56 Mya, which was marked by increased global temperatures of 5.6°C, warming the earths oceans.

Cetaceans are fully aquatic mammals belonging to the order Artiodactyla. Molecular and morphological analyses suggest that they share a relatively recent closest common ancestor with hippopotamuses – their sister group, diverging about 55.5 Mya. Cetacea completely branched off from other artiodactyls around 50 mya. Research conducted in the late 1970s in Pakistan revealed several stages in the transition of cetaceans from land to sea. Being mammals, they surface to breathe air; they have five finger bones (even-toed) in their fins; they nurse their young; and, despite their fully aquatic life style, they retain many skeletal features from their terrestrial ungulata ancestors.

The two modern parvorders of cetaceans – Mysticeti (baleen whales) and Odontoceti (toothed whales) – are thought to have separated from each other around 28–33 mya in a second cetacean radiation, the first occurring with the archaeocetes. The adaptation of animal echolocation in toothed whales distinguishes them from fully aquatic archaeocetes and early baleen whales. The presence of baleen in baleen whales occurred gradually, with earlier varieties having very little baleen, and their size is linked to baleen dependence (and subsequent increase in filter feeding).

Early evolution

thumb|upright|Cladogram showing the position of Cetacea within [[Artiodactylamorpha]]

The aquatic lifestyle of cetaceans first began in the Indian subcontinent from even-toed ungulates 50 million years ago, with this initial stage lasting approximately 4-15 million years. Archaeoceti is an extinct parvorder of Cetacea containing ancient whales. The traditional hypothesis of cetacean evolution, first proposed by Van Valen in 1966, was that whales were related to the mesonychians, an extinct order of carnivorous ungulates (hoofed animals) that resembled wolves with hooves and were a sister group of the artiodactyls (even-toed ungulates). This hypothesis was proposed due to similarities between the unusual triangular teeth of the mesonychians and those of early whales. However, molecular phylogeny data indicates that whales are very closely related to the artiodactyls, with hippopotamuses as their closest living relative. Because of this observation, cetaceans and hippopotamuses are placed in the same suborder, Whippomorpha. Cetartiodactyla (formed from the words Cetacea and Artiodactyla) is a proposed name for an order that includes both cetaceans and artiodactyls. However, the earliest anthracotheres, the ancestors of hippos, do not appear in the fossil record until the Middle Eocene, millions of years after Pakicetus, whereas the first known whale ancestor appeared during the Early Eocene; this difference in timing implies that the two groups diverged well before the Eocene. Molecular analysis identifies artiodactyls as being very closely related to cetaceans, so mesonychians are probably an offshoot from Artiodactyla, and cetaceans did not derive directly from mesonychians, but the two groups may share a common ancestor.

Raoellidae

Raoellidae (/reɪoʊˈɛlɪdeɪ/) is a family of extinct semiaquatic artiodactyls from the middle Eocene (about 48 million years ago) that were not cetaceans, but closely related to cetaceans. Raoellidae has been recovered as the family most closely related to Cetacea in multiple phylogenetic analyses. They are relatively small animals; on average, raoellids were the size of a red fox. However, Khirtharia major, at about twice the size of an average-sized raoellid, would have been approximately the size of a coyote. Meanwhile, the smallest raoellid, Metkatius, was roughly the size of a house cat. Raoellidae is of particular importance to the understanding of cetacean evolution due to representing a transitional form between fully-terrestrial artiodactyls and the semi-aquatic pakicetids. The raoellid that has been most thoroughly studied and most heavily contributed to the knowledge of Raoellidae is Indohyus. It showed signs of adaptations to aquatic life, including dense limb bones that reduce buoyancy so that they could stay underwater, which are similar to the adaptations found in modern aquatic mammals such as the hippopotamus. This suggests a similar survival strategy to the African chevrotain or water chevrotain which, when threatened by a bird of prey, dives into water and hides beneath the surface for up to four minutes.

thumb|left|300px|Possible relationships between cetaceans and other ungulate groups.<br>

Pakicetidae

The pakicetids were digitigrade hoofed mammals that are thought to be the earliest known cetaceans, with Raoellidae being the closest sister group. They lived in the early Eocene, around 50 million years ago. Their fossils were first discovered in North Pakistan in 1979, located at a river not far from the shores of the former Tethys Sea. After the initial discovery, more fossils were found, mainly in the early Eocene fluvial deposits in northern Pakistan and northwestern India. Based on this discovery, pakicetids most likely lived in an arid environment with ephemeral streams and moderately developed floodplains millions of years ago. Their diet probably included land animals that approached water for drinking or some freshwater aquatic organisms that lived in the river.

Pakicetids are classified as cetaceans mainly due to the structure of the auditory bulla (ear bone), which is formed only from the ectotympanic bone. The shape of the ear region in pakicetids is highly unusual and the skull is cetacean-like, although a blowhole is still absent at this stage. The jawbone of pakicetids also lacks the enlarged space (mandibular foramen) that is filled with fat or oil, which is used in receiving underwater sound in modern cetaceans. They have dorsal orbits (eye sockets facing up), which are similar to crocodiles. This eye placement helps submerged predators observe potential prey above the water.

It was initially thought that the ears of pakicetids were adapted for underwater hearing, but, as would be expected from the anatomy of the rest of this creature, the ears of pakicetids are specialized for hearing on land. However, pakicetids were able to listen underwater by using enhanced bone conduction, rather than depending on the tympanic membrane like other land mammals. This method of hearing did not give directional hearing underwater.

Ambulocetidae

Ambulocetus, which lived about 49 million years ago, was discovered in Pakistan in 1994. They were vaguely crocodile-like mammals, possessing large brevirostrine jaws. In the Eocene, ambulocetids inhabited the bays and estuaries of the Tethys Sea in northern Pakistan. The fossils of ambulocetids are always found in near-shore shallow marine deposits associated with abundant marine plant fossils and littoral mollusks. They probably swam by pelvic paddling (a way of swimming which mainly utilizes their hind limbs to generate propulsion in water) and caudal undulation (a way of swimming which uses the undulations of the vertebral column to generate force for movements), as otters, seals and modern cetaceans do. This is an intermediate stage in the evolution of cetacean locomotion, as modern cetaceans swim by caudal oscillation (a way of swimming similar to caudal undulation, but is more energy efficient).

Remingtonocetidae

Remingtonocetids lived in the Middle-Eocene in South Asia, about 49 to 43 million years ago. Compared to family Pakicetidae and Ambulocetidae, Remingtonocetidae was a diverse family found in north and central Pakistan and western India. Remingtonocetids were also found in shallow marine deposits, but they were obviously more aquatic than ambulocetidae. This is demonstrated by the recovery of their fossils from a variety of coastal marine environments, including near-shore and lagoonal deposits. This reduction in size had closely accompanied the cetacean radiation into marine environments. According to a 2002 study done by Spoor et al., this modification of the semicircular canal system may represent a crucial 'point of no return' event in early cetacean evolution, which excluded a prolonged semi-aquatic phase. and North America (e.g., Georgiacetus) also include open marine forms. Their amphibious nature is supported by the discovery of a pregnant Maiacetus, in which the fossilised fetus was positioned for a head-first delivery, suggesting that Maiacetus gave birth on land. If they gave birth in the water, the fetus would be positioned for a tail-first delivery to avoid drowning during birth.

Unlike remingtonocetids and ambulocetids, protocetids have large orbits which are oriented laterally. Increasingly lateral-facing eyes might be used to observe underwater prey, and are similar to the eyes of modern cetaceans. Furthermore, the nasal openings were large and were halfway up the snout. The great variety of teeth suggests diverse feeding modes in protocetids.

The foot structure of Rodhocetus shows that protocetids were predominantly aquatic. A 2001 study done by Gingerich et al. hypothesized that Rodhocetus locomoted in the oceanic environment similarly to how ambulocetids pelvic paddling, which was supplemented by caudal undulation. Terrestrial locomotion of Rodhocetus was very limited due to their hindlimb structure. It is thought that they moved in a way similar to how eared seals move on land, by rotating their hind flippers forward and underneath their body.

Basilosauridae

thumb|left|Archaeocetes (like this Basilosaurus) had a [[heterodont dentition]]

Basilosaurids and dorudontines lived together in the late Eocene around 41 to 33.9 million years ago, and are the oldest known obligate aquatic cetaceans. The large size of basilosaurids is due to the extreme elongation of their lumbar vertebrae. They had a tail fluke, but their body proportions suggest that they swam by caudal undulation and that the fluke was not used for propulsion. In contrast, dorudontines had a shorter but powerful vertebral column. They too had a fluke and, unlike basilosaurids, they probably swam similarly to modern cetaceans, by using caudal oscillations.

Both basilosaurids and dorudontines are relatively closely related to modern cetaceans, which belong to parvorders Odontoceti and Mysticeti. However, according to a 1994 study done by Fordyce and Barnes, the large size and elongated vertebral body of basilosaurids preclude them from being ancestral to extant forms. As for dorudontines, there are some species within the family that do not have elongated vertebral bodies, which might be the immediate ancestors of Odontoceti and Mysticeti. The other basilosaurids became extinct. The development of filter feeding may have been a result of worldwide environmental change and physical changes in the oceans. A large-scale change in ocean current and temperature could have contributed to the radiation of modern mysticetes. The earlier varieties of baleen whales, or "archaeomysticetes", such as Janjucetus and Mammalodon had very little baleen and relied mainly on their teeth.

There is also evidence of a genetic component of the evolution of toothless whales. Multiple mutations have been identified in genes related to the production of enamel in modern baleen whales. These are primarily insertion/deletion mutations that result in premature stop codons. Recent research has also indicated that the development of baleen and the loss of enamel-capped teeth both occurred once, and both occurred on the mysticete stem branch.

Generally it is speculated the four modern mysticete families have separate origins among the cetotheres. Modern baleen whales, Balaenopteridae (rorquals and humpback whale, Megaptera novaengliae), Balaenidae (right whales), Eschrichtiidae (gray whale, Eschrictius robustus), and Neobalaenidae (pygmy right whale, Caperea marginata) all have derived characteristics presently unknown in any cetothere and vice versa (such as a sagittal crest). Mysticetes are also known for their gigantism, as baleen whales are among the largest organisms to ever have lived; they reach lengths greater than 20 m and weigh more than 100,000 kg. This gigantism is directly related to their feeding mechanism – mysticete size has been found to be dependent on the amount of baleen a mysticete can use to filter its prey. Additionally, size is a positively selected trait that gives mysticetes a boost in fitness. Mysticete populations will therefore slowly become even more gigantic as whales with larger amounts of baleen are selected.

Toothed whales

The adaptation of echolocation occurred when toothed whales (Odontoceti) split apart from baleen whales, and distinguishes modern toothed whales from fully aquatic archaeocetes. This happened around 34 million years ago in a second cetacean radiation. Modern toothed whales do not rely on their sense of sight, but rather on their sonar to hunt prey. Echolocation also allowed toothed whales to dive deeper in search of food, with light no longer necessary for navigation, which opened up new food sources. Toothed whales echolocate by creating a series of clicks emitted at various frequencies. Sound pulses are emitted, reflected off objects, and retrieved through the lower jaw. Skulls of Squalodon show evidence for the first hypothesized appearance of echolocation. Squalodon lived from the early to middle Oligocene to the middle Miocene, around 33–14 million years ago. Squalodon featured several commonalities with modern toothed whales: the cranium was well compressed (to make room for the melon, a part of the nose), the rostrum telescoped outward into a beak, a characteristic of the modern toothed whales that gave Squalodon an appearance similar to them. However, it is thought unlikely that squalodontids are direct ancestors of modern toothed whales.

The first oceanic dolphins such as kentriodonts, evolved in the late Oligocene and diversified greatly during the mid-Miocene. The first fossil cetaceans near shallow seas (where porpoises inhabit) were found around the North Pacific; species like Semirostrum were found along California (in what were then estuaries). These animals spread to the European coasts and Southern Hemisphere only much later, during the Pliocene. The earliest known ancestor of arctic whales is Denebola brachycephala from the late Miocene around 9–10 million years ago. A single fossil from Baja California indicates the family once inhabited warmer waters.

thumb|left|[[Acrophyseter skull]]

Ancient sperm whales differ from modern sperm whales in tooth count and the shape of the face and jaws. For example, Scaldicetus had a tapered rostrum. Genera from the Oligocene and Miocene had teeth in their upper jaws. These anatomical differences suggest that these ancient species may not have necessarily been deep-sea squid hunters like the modern sperm whale, but that some genera mainly ate fish. Contrary to modern sperm whales, most ancient sperm whales were built to hunt whales. Livyatan had a short and wide rostrum measuring across, which gave the whale the ability to inflict major damage on large struggling prey, such as other early whales. Species like these are collectively known as killer sperm whales or macroraptorial sperm whales.

Beaked whales consist of over 20 genera. Earlier varieties were probably preyed upon by killer sperm whales and large sharks such as megalodon. In 2008, a large number of fossil ziphiids were discovered off the coast of South Africa, confirming the remaining ziphiid species might just be a remnant of a higher diversity that has since gone extinct. After studying numerous fossil skulls, researchers discovered the absence of functional maxillary teeth in all South African ziphiids, which is evidence that suction feeding had already developed in several beaked whale lineages during the Miocene. Extinct ziphiids also had robust skulls, suggesting that tusks were used for male-male interactions. Although they somewhat resembled a wolf, the fossils of pakicetids showed the eye sockets were much closer to the top of their head than that of other terrestrial mammals, but similar to the structure of the eyes in cetaceans. Their transition from land to water led to reshaping of the skull and food processing equipment because the eating habits were changing. The change in position of the eyes and limb bones is associated with the pakicetids becoming waders. The ambulocetids also began to develop long snouts, which is seen in current cetaceans. Their limbs (and hypothesized movement) were very similar to otters.

225px|thumb|left|The skeleton of a [[bowhead whale with the hind limb and pelvic bone structure circled in red. This bone structure stays internal during the entire life of the species.]]

Limblessness in cetaceans does not represent a regression of fully formed limbs nor the absence of limb bud initiation, but rather arrest of limb bud development. Limb buds develop normally in cetacean embryos. Occasionally, the genes that code for longer extremities cause a modern whale to develop miniature legs (atavism).

thumb|Pakicetus attocki skeleton

Pakicetus had a pelvic bone most similar to that of terrestrial mammals. In later species, such as Basilosaurus, the pelvic bone, no longer attached to the vertebrae and the ilium, was reduced. The pelvic girdle in modern cetaceans were once thought to be vestigial structures that served no purpose at all. The pelvic girdle in male cetaceans is different in size compared to females, and the size is thought to be a result of sexual dimorphism. The pelvic bones of modern male cetaceans are more massive, longer, and larger than those of females. Due to the sexual dimorphism displayed, they were most likely involved in supporting male genitalia that remain hidden behind abdominal walls until sexual reproduction occurs.

Early archaeocetes such as Pakicetus had the nasal openings at the end of the snout, but in later species such as Rodhocetus, the openings had begun to drift toward the top of the skull. This is known as nasal drift. The nostrils of modern cetaceans have become modified into blowholes that allow them to break to the surface, inhale, and submerge with convenience. The ears began to move inward as well, and, in the case of Basilosaurus, the middle ears began to receive vibrations from the lower jaw. Today's modern toothed whales use their melon organ, a pad of fat, for echolocation.

Genetics insights

The time of early cetacean evolution is consistent with dN/dS analysis estimates of cetacean UCP-1 gene inactivation, likely relaxing selection pressures against UCP-1, leading to pseudogenization. UCP-1 inactivation in cetaceans initiated the shift from heat production to heat conservation through blubber formation/thermal insulation as evidenced by a transgenic mouse model simulating cetacean-like UCP1 gene inactivation. While UCP1 pseudogenization initiated the development of these phenotypes, they weren't solidified until subsequent ADRB3 inactivation during the Eocene-Oligocene transition, which was marked by an estimated 4°C drop in benthic temperatures. ADRB3 is expressed primarily in adipocytes and functions primarily as a key regulator of lipolysis. Global cooling during the Eocene-Oligocene transition likely selected against ADRB3, favoring more robust thermal insulation provided by dense blubber formation and gigantism, and driving the modern cetacean phenotype.

Radiation events

There are three major radiation events that mark diversification and speciation in the evolutionary history of Cetacea. The first occurred around the middle Eocene (40 Mya) when these early cetaceans abandoned riverine and shallow coastal habitats, setting the scene for Protocetidae – the first fully marine cetacean. The timing of this second radiation event is not coincidental, as the following diversification of cetaceans was likely due to new ecological opportunities the change in oceans gave them. The final major radiation event, occurring throughout the middle Miocene and into the Pliocene (12 Mya to 2 Mya), was not due to a specific event but is associated with widespread generic expansion of odontocetes and mysticetes.]]

Culture is group-specific behavior transferred by social learning. Tool use to aid with foraging is one example. Whether or not a dolphin uses a tool affects its eating behavior, which causes differences in diet. Also, using a tool allows a new niche and new prey to open up for that particular dolphin. Due to these differences, fitness levels change within the dolphins of a population, which further causes evolution to occur in the long run. Culture and social networks have played a large role in the evolution of modern cetaceans, as concluded in studies showing dolphins preferring mates with the same socially learned behaviors, and humpback whales using songs between breeding areas. For dolphins particularly, the largest non-genetic effects on their evolution are due to culture and social structure.

Based on a 2014 study, the population of Indo-Pacific bottlenose dolphins (Tursiops sp.) around Shark Bay of Western Australia can be divided into spongers and nonspongers. Spongers put sea sponges on their snouts as protection against abrasions from sharp objects, stingray barbs, or toxic organisms. The sponges also help the dolphins target fish without swim bladders, since echolocation cannot detect these fish easily against a complex background. Spongers also specifically forage in deep channels, but nonspongers are found foraging in both deep and shallow channels. This foraging behavior is mainly passed on from mother to child. Therefore, since this is a group behavior being passed down by social learning, this tool use is considered a cultural trait. This suggests that juvenile males impose a social stress on their younger counterparts. In fact, it has been documented that juvenile males commonly perform acts of aggression, dominance, and intimidation against the male calves.

Genetic studies conducted on Clymene dolphins (Stenella clymene) focused on their natural histories, and the results show that the origin of the species was actually an outcome of hybrid speciation. Hybridization between spinner dolphins (Stenella longirostris) and striped dolphins (Stenella coeruleoalba) in the North Atlantic was caused by constant habitat sharing of the two species. Relationships between these three species had been speculated according to notable resemblances between anatomies of the Clymene and the spinner dolphins, resulting in the former being regarded as subspecies of the latter until 1981, and the possibility of the Clymene dolphin as a hybrid between the spinner and the striped dolphins have come to question based on anatomical and behavioral similarities between these two species.

Environmental factors

Genome sequences done in 2013 revealed that the Yangtze river dolphin, or "baiji" (Lipotes vexillifer), lacks single nucleotide polymorphisms in its genome. After reconstructing the history of the baiji genome for this dolphin species, researchers found that the major decrease in genetic diversity occurred most likely due to a bottleneck event during the last deglaciation event. During this time period, sea levels were rising while global temperatures were increasing. Other historical climate events can be correlated and matched with the genome history of the Yangtze river dolphin as well. This shows how global and local climate change can drastically affect a genome, leading to changes in fitness, survival, and evolution of a species.

The European population of common dolphins (Delphinus delphis) in the Mediterranean have differentiated into two types: eastern and western. According to a 2012 study, this seems to be due to a recent bottleneck as well, which drastically decreased the size of the eastern Mediterranean population. Also, the lack of population structure between the western and eastern regions seems contradictory of the distinct population structures between other regions of dolphins. Even though the dolphins in the Mediterranean area had no physical barrier between their regions, they still differentiated into two types due to ecology and biology. Therefore, the differences between the eastern and western dolphins most likely stems from highly specialized niche choice rather than just physical barriers. Through this, environment plays a large role in the differentiation and evolution of this dolphin species.

The divergence and speciation within bottlenose dolphins has been largely due to climate and environmental changes over history. According to research, the divisions within the genus correlate with periods of rapid climate change. For example, the changing temperatures could cause the coast landscape to change, niches to empty up, and opportunities for separation to appear. In the Northeast Atlantic, specifically, genetic evidence suggests that the bottlenose dolphins have differentiated into coastal and pelagic types. Divergence seems most likely due to a founding event where a large group separated. Following this event, the separate groups adapted accordingly and formed their own niche specializations and social structures. These differences caused the two groups to diverge and to remain separated.

Two endemic, distinctive types of short-finned pilot whale, Tappanaga (or Shiogondou) the larger, northern type and Magondou the smaller, southern type, can be found along the Japanese archipelago where distributions of these two types mostly do not overlap by the oceanic front border around the easternmost point of Honshu. It is thought that the local extinction of long-finned pilot whales in the North Pacific in the 12th century could have triggered the appearance of Tappanaga, causing short-finned pilot whales to colonize the colder ranges of the long-finned variant. Whales with similar characteristics to the Tappanaga can be found along Vancouver Island and northern US coasts as well.

References

External links

For a review of whale evolution, see

Timeline of Whale Evolution - Smithsonian Ocean Portal
Cetacean Paleobiology – University of Bristol
BBC: Whale's evolution
BBC: Whale Evolution – The Fossil Evidence
Hooking Leviathan by Its Past by Stephen Jay Gould
Research on the Origin and Early Evolution of Whales (Cetacea), Gingerich, P.D., University of Michigan
Pakicetus inachus, a new archaeocete (Mammalia, Cetacea) from the early-middle Eocene Kuldana Formation of Kohat (Pakistan). Gingerich, P.D., 1981, Museum of Paleontology, The University of Michigan
Skeletons of terrestrial cetaceans and the relationship of whales to artiodactyls, Nature 413, 277–281 (20 September 2001), J. G. M. Thewissen, E. M. Williams, L. J. Roe and S. T. Hussain
Evolution of Whales segment from the Whales Tohorā Exhibition Minisite of the Museum of New Zealand Te Papa Tongarewa