- Email: [email protected]
Cetacean Evolution
180
C
Cetacean Evolution
Cetaceans are also important consumers. Their large body sizes, high metabolic rates, and positions as apex or near-apex predators mean that they take tons of prey with implications for the structure of marine ecosystems themselves. The “krill surplus hypothesis” (Laws, 1977) proposed that the removal of large whales from the Southern Ocean released up to 150 million tons of krill per year from whale predation, a prey base that was theoretically then available to other krill predators. Subsequent growth in penguin and pinniped populations was attributed to this competitive release (reviewed in Ballance et al., 2006b). Killer whale predation may drive population dynamics of their prey, sea otters, elephant seals, gray whales, and humpback whales among them, with the potential for cascading effects. For example, killer whale predation was proposed to explain apparently sequential declines in pinniped populations in the north Pacific, as killer whales depleted these prey, and subsequently shifted to unexploited species (Springer et al., 2003). These ideas have been hotly debated and research attempting to clarify them is confounded by spatial and/or temporal mismatch between datasets, disagreement regarding the extent to which killer whales can (or do) switch between different prey types, and massive anthropogenic influences on marine ecosystems (e.g., commercial exploitation and subsequent recovery of protected species, climate change and its bottom-up influences). Nevertheless, there is intriguing and strong evidence that top-down forcing through cetacean predation is an important structuring force for marine ecosystems. Particularly as large whales recover from commercial exploitation, the appearance of killer whale predation on them is increasingly being documented, providing an opportunity for ecologists to document ecosystem change in our lifetimes (Pitman et al., 2014). The role that cetaceans play in marine ecosystems is an active and exciting focus of research in cetacean ecology.
See Also the Following Articles Biogeography n Distribution n Ecology n Variation n Ocean Environments n Pinniped Ecology
Geographic
References Ballance, L.T., Pitman, R.L., and Fiedler, P.C. (2006a). Oceanographic influences on seabirds and cetaceans of the eastern tropical Pacific: A review. Prog. Oceanogr. 69, 360–390. Ballance, L.T., Pitman, R.L., Hewitt, R., Siniff, D., Trivelpiece, W., Clapham, P., and Brownell Jr., R.L. (2006b). The removal of large whales from the Southern Ocean. Evidence for long-term ecosystem eff ects? In “Whales, Whaling, and Ocean Ecosystems”, (J.A. Estes, D.P. DeMaster, D.F. Doak, T.M. Williams, and R.L. Brownell Jr., Eds), pp. 215–230. University of California Press, Berkeley, CA. Becker, E.A., Foley, D.G., Forney, K.A., Barlow, J., Redfern, J.V., and Gentemann, C.L. (2012). Forecasting cetacean abundance patterns to enhance management decisions. Endang. Species Res. 16, 97–112. Corkeron, P.J., and Connor, R.C. (1999). Why do baleen whales migrate? Mar. Mamm. Sci. 15, 1228–1245. Durban, J.W., and Pitman, R.L. (2011). Antarctic killer whales make rapid, round-trip movements to subtropical waters: evidence for physiological maintenance migrations? Biol. Lett. doi:10.1098/ rsbl.2011.0875. Estes, J.A. (2006). Whales, Whaling, and Ocean Ecosystems. University of California Press. Heyning, J.E., and Mead, J.G. (1996). Suction Feeding in Beaked Whales: Morphological and Observational Evidence. Natural History Museum of Los Angeles County. Laws, R.M. (1977). Seals and whales of the Southern Ocean. Philos. Trans. R. Soc. Lond. B 27, 81–96.
Melville, H. (1851). Moby Dick, or, The Whale. Harper and Brothers, New York, NY Norris, K.S., and Møhl, B. (1983). Can odontocetes debilitate prey with sound? Am. Nat. 122, 85–104. Obst Jr., B.S., and Hunt, G.L. (1990). Marine birds feed at gray whale mud plumes in the Bering Sea. Auk 107, 678–688. Perrin, W.F. (1991). Why are there so many kinds of whales and dolphins? BioScience 41, 460–461. Pitman, R.L., Ballance, L.T., Mesnick, S.I., and Chivers, S.J. (2001). Killer whale predation on sperm whales: observations and implications. Mar. Mamm. Sci. 17(3), 494–507. Pitman, R.L., and Stinchcomb, C. (2002). Rough-toothed dolphins (Steno bredanensis) as predators of mahimahi (Coryphaena hippurus). Pac. Sci. 56, 447–450. Pitman, R.L., Durban, J.W., Greenfelder, M., Guinet, C., Jorgensen, M., Olson, P.A., Plana, J., Tixier, P., and Towers, J.R. (2011). Observations of a distinctive morphotype of killer whale (Orcinus orca), type D, from subantarctic waters. Polar Biol. 34(2), 303–306. Pitman, R.L., and Durban, J.W. (2012). Cooperative hunting behavior, prey selectivity and prey handling by pack ice killer whales (Orcinus orca), type B, in Antarctic Peninsula waters. Mar. Mamm. Sci. 31, 16–36. Pitman, R.L., Totterdell, J.A., Fearnbach, H., Ballance, L.T., Durban, J.W., and Kemps, H. (2014). Whale killers: Prevalence and ecological implications of killer whale predation on humpback whale calves off Western Australia. Mar. Mamm. Sci. doi:10.1111/mms.12182. Redfern, J.V., et al. (19 authors) (2006). Techniques for cetacean–habitat modeling. Mar. Ecol. Prog. Ser. 310, 271–295. Roman, J., Estes, J.A., Morissette, L., Smith, C., Costa, D., McCarthy, J., Nation, J.B., Nicol, S., Pershing, A., and Smetacek, V. (2014). Whales as marine ecosystem engineers. Front. Ecol. Environ. 12(7), 377–385. Santora, J.A., Reiss, C.S., Loeb, V.J., and Veit, R.R. (2010). Spatial association between hotspots of baleen whales and demographic patterns of Antarctic krill Euphausia superba suggests size-dependent predation. Mar. Ecol. Prog. Ser. 405, 255–269. Schakner, Z.A., Lunsford, C., Straley, J., Eguchi, T., and Mesnick, S.L. (2014). Using models of social transmission to examine the spread of longline depredation behavior among sperm whales in the Gulf of Alaska. PLoS One 9(10), e109079. Springer, A.M., Estes, J.A., Van Vliet, G.B., Williams, T.M., Doak, D.F., Danner, E.M., and Pfister, B. (2003). Sequential megafaunal collapse in the North Pacific Ocean: An ongoing legacy of industrial whaling. Proc. Natl. Acad. Sci. 100(21), 12223–12228. Tittensor, D.P., Mora, C., Jetz, W., Lotze, H.K., Ricard, D., Berghe, E.V., and Worm, B. (2010). Global patterns and predictors of marine biodiversity across taxa. Nature 466(7310), 1098–1101.
CETACEAN EVOLUTION R. Ewan Fordyce I. Patterns of Evolution Anatomists of the 1600s–1700s, such as Ray and Hunter, showed that cetaceans share many structures with hoofed mammals: an ungulate-like larynx, stomach, reproductive organs, and fetal membranes (Flower, 1883). An early serological study (Boyden and Gemeroy, 1950) showed cetaceans close to ungulates, foreshadowing molecular approaches. Modern studies place the clade Cetacea in the Cetartiodactyla—hoofed mammals (artiodactyls, ruminants). Fossils reveal shared skeletal structures with artiodactyls, and show that cetaceans appeared more than 50 million years ago. Cetaceans
REF 08/16
50
Delphinidae
Monodontidae
Phocoenidae
Radiation of delphinoids
Radiation of Neoceti
?
Ultrasonic hearing Origin of neoceti Radiation of toothed mysticeti Radiation of oceanic cetacea including polar species High frequency hearing
†Odobenocetopsidae
Pontoporiidae
Iniidae †Albireonidae
Platanistidae Ziphiidae Lipotidae †Kentriodontidae
†Squalodelphinidae
†Eurhinodelphinidae †Allodelphinidae
Kogiidae †Eoplatanistidae
†Squalodontidae
†Waipatiidae
†Patriocetidae
†Mirocetidae †Agorophiidae
Extinction of many archaic neocete groups
†Simocetidae
Radiation of basal balaenopteroids Baleen-assisted filter feeding
Physeteridae
Balaenopteridae includes Eschrichtiinae
Basal balaenopteridae
†Pelocetus group
181
Odontoceti
†Xenorophidae †Ashleycetidae
†Mauicetus group
Neobalaeninae
†Llanocetidae
†Eomysticetidae
†Mammalodontidae †Aetiocetidae
Late Middle
†Mesonychia
Early Late Early
Archaeoceti †Raoellidae †Pakicetidae †Ambulocetidae †Remingtonocetidae †Protocetidae †Basilosauridae †Kekenodontidae
40
E O C E N E
Late
30
O L I G O
Middle
20
Early
Millions of years before present
10
M I O C E N E
†Parietobalaena group
Balaenidae
PLEIS P L I
Cetotheriidae
Mysticeti
EL
0
Hippopotamidae
Cetacean Evolution
Key to groups, age ranges, symbols Extant (crown) clade Extinct (stem) clade Extinct paraphyletic group Extinct taxon Freshwater habits obligate or occasional Pleistocene Pleis Pliocene Plio
†
Radiation of riverine to shallow coastal Cetacea
Figure 1 Phylogeny of living and fossil Cetacea, with families calibrated against time. Some key ecological/behavioral shifts are shown. This composite is based on Uhen (2010) for Archaeoceti, Marx and Fordyce (2015) for Mysticeti, and Churchill et al. (2016) for Odontoceti. Other phylogenies show different patterns. are the most diverse clade of modern marine mammals in terms of species, ecology, and range. Cetaceans have a sparse fossil record, lacking a close succession of ancestors to descendants that might show evolution. Hennig’s methodology of cladistic analysis suits the high “information content” of cetaceans. It has produced phylogenies that integrate morphology and molecules from living and/or fossil species. Cladistic methods reveal clades united by common ancestry (Fig. 1). Clades are the foundation for formal taxonomic names (Committee on Taxonomy, 2016), including the two major groups, Odontoceti and Mysticeti. Fossils provide the only direct evidence of extinct species and structures; they indicate clades and ecologies not seen today. The third division of Cetacea is the Archaeoceti, a grade (paraphyletic taxon) including the basal or stem cetaceans. Patterns from modern and fossil species have, since 2000, hugely expanded understanding of evolution, although high-level/deep time phylogenies (Fig. 1) show limited agreement. Discussion of evolution depends on agreed phylogenetic approaches. Concepts of crown and stem group help to compare fossil versus molecular evidence for deep-time events. A crown group comprises all living species in a clade, and all descendants of their latest common ancestor. The stem group comprises those species, all extinct, that are closer to the crown group than to any other clade.
Evolutionary rates, modes, and mechanisms of cetacean ancestor-to-descendant transitions are poorly understood (Quental and Marshall, 2010). Evolutionary processes at the species level might include natural selection, sexual selection, coevolution, dispersal, founder effects, vicariance, and hybridization, discussed further below.
II. Ecology Past and Present Structure is the link between genome and ecology. Structure involves functional complexes linked to ecology—to interactions between species and biological, physical, and chemical environment. Musculoskeletal systems in living species help to reveal function and biology (Rommel et al., 2006). But, how do subtle differences between related species help to separate niches? How do family-level functional complexes (e.g., acoustic sinuses in Delphinidae) link to lifestyle, habitat, and species diversity? Numerical methods, e.g., geometric morphometrics, may quantify and elucidate structural patterns in ontogeny and ecology. On geological timescales, evolution and paleoecology are inextricably linked, for evolution occurs through natural selection and adaptation to the environment. Ecological phenomena—including feeding and predator–prey interactions, migration, nutrient cycling, thermal adaptations, habitat shifts, and strandings and burial— strongly inform evolution.
C
Cetacean Evolution
182
Geographic patterns important in cetacean evolution
Habitat shift: polar monodontids had temperate-tropical relatives 4–6 Ma m
†Parapontoporia
f
Lipotes f
C
f f Platanista
K
Berardius bairdii, Lissodelphis borealis
an origins Tethy †Prolipotes
K
†Pomatodelphis m
P. sinus
K
f
m
Fossils reflect past links - Atlantic/Pacific Kentriodon
spp and Central American Seaway K
f
Antitropical patterns -
†Ziphiidae f
Sotalia Inia f f †Platanistinae
sister-taxa separated by tropical waters
Major habitat shift:
m
tropical origins >50 Ma, to polar south 40–45 Ma
Founder effects -
†Platanistoidea?
Phocoena sinus evolved from P. spinipinnis
f
Cosmopolitan Physeter macrocephalus
Winter tropical breeding
Rorqual migration
C. heavisidii C. hectori
Symbols f Freshwater dolphin location f Freshwater fossil cetacean location Representative fossil location m Monodontid location K Kentriodon location
C. commersonii
Berardius arnuxii, Lissodelphis peronii
f
Pontoporia
C. eutropia
Circum-polar pattern -
Cephalorhynchus speciation around Southern Ocean
Summer polar feeding
C. commersonii
Figure 2 Distribution patterns and cetacean evolution: key fossil localities, antitropical and circum-Antarctic distributions, allopatric species pairs between oceans, founder effects, convergent origins for various freshwater dolphins, habitat expansion from tropical ranges involving rise of pelagic habits and occupation of polar waters, and geologically recent changes in habitat. Ancient lifestyles can be inferred by “taxonomic uniformitarianism,” using modern ecology to understand fossils: the present is the key to the past. For example, fossil beaked whales may have been deep divers. However, fossils show that cetacean evolution involves structural change, in turn implying change in ecology. How far back might we “push” modern ecology? Past lifestyle may be inferred by analogy and functional morphology, using known modern correlations of muscle, nerve, and vessels to bone. The extinct Peruvian Odobenocetops “walrus whales” have no structural equivalents among living Cetacea. Rather, their jaws are similar to those of the unrelated walrus, Odobenus, implying comparable suction feeding on molluscs. Extant phylogenetic bracketing predicts that a fossil in a crown (living) clade would have the same attributes as the living species. For example, extinct species within the crown Odontoceti can be inferred to have echolocated because phylogenetically adjacent living species echolocate.
III. Major Radiations Molecular phylogenies show relationships among living cetaceans (e.g., McGowen et al., 2009), but lack the extinct lineages which helped shape cetacean evolution. Fossil-based phylogenies are limited by the patchy fossil record, but they do anchor lineages in time and space, and do show changes in structure and diversity. Family patterns help to recognize three major radiations—times of functional, ecological, and taxonomic diversification—in cetacean history (Fig. 1).
Cetaceans evolved on the margins of the former tropical Tethys seaway, between India and Asia, early in the Eocene, about 53–45 million years before present (Ma) (Fig. 2). The early small, amphibious species of Pakicetidae probably arose from terrestrial ancestors such as the mesonychids or, more favored, the raoellids. Pakicetids occur in freshwater strata but possibly used near-coastal habitats. Perhaps rivers were a refuge from predators (Thewissen et al., 2007) and a source of food. Two other short-ranged Tethyan amphibious clades are the Ambulocetidae and Remingtonocetidae. The diverse Protocetidae includes 19+ genera (pbdb.org) of Archaeoceti that were more specialized for marine life than pakicetids, ambulocetids, and remingtonocetids (Bajpai and Thewissen, 2014). Concurrent changes in locomotory and hearing mechanisms allowed dispersal beyond the Tethys, foreshadowing fully oceanic habits. Species in the Middle to Late Eocene family Basilosauridae were pelagic, judging from their spread to temperate and Antarctic latitudes by 39–40 Ma (Buono et al., 2016). In terms of disparity and presumably, ecology, basilosaurids were more comparable with living mysticetes than with odontocetes. Taxa varied in body size, hind-limb reduction, skull and jaw proportions, tooth form and number, and aspects of the hearing apparatus. Archaeocete diversity dropped late in Eocene times (Uhen, 2010), foreshadowing the rise of Neoceti. The second major radiation, involving the Neoceti or crown-Cetacea, started late in the Eocene, and continued in the Oligocene (Marx and Fordyce, 2015) (Fig. 1). The two living clades, Mysticeti and Odontoceti, appeared, and diversified rapidly in about 5 Ma,
Cetacean Evolution
183
after originating from Eocene archaeocetes which probably did not echolocate or filter-feed. Concurrent events included the final breakup of Gondwana, continued opening of the Southern Ocean, cooling and increased tropics-to-polar temperature gradients, and changes in ocean ecosystems and productivity. It is likely that cetaceans responded to new ecological opportunities in rapidly changing oceans (Lindberg and Pyenson, 2007; Marx and Fordyce, 2015). The most basal mysticetes were extinct toothed families, of latest Eocene to early Miocene age: Llanocetidae, Mammalodontidae, and Aetiocetidae. They were probably raptorial, perhaps using suction feeding. Toothless filter-feeding baleen whales evolved during the Oligocene, as shown by the extinct Eomysticetidae and by basal balaenopteroids on the lineage to rorquals. Fossil Balaenidae, Cetotheriidae, archaic balaenopteroids, and Balaenopteridae are widely known from Miocene strata, and phylogenies predict that many originated in the Oligocene (Marx and Fordyce, 2015). Oligocene odontocetes include diverse families that reflect a greater structural disparity and wider geographic range than for mysticetes. Examples include the Xenorophidae, Simocetidae, Agorophiidae, Waipatiidae, Squalodontidae, Patriocetidae, and Eurhinodelphinidae, all extinct, and a putative sperm whale, Physeteridae. Phylogenetic relationships between these groups, or with later lineages, are uncertain. Other families, some extant, appeared in the Miocene: Kogiidae, Ziphiidae, Allodelphinidae, Squalodelphinidae, and Platanistidae. Of note is the radiation of delphinoids including the Kentriodontidae, the “river dolphins” (Lipotidae, Iniidae, Pontoporiidae), Monodontidae, Phocoenidae, and Delphinidae (Fig. 1). Cetacean diversity peaked later in the Miocene (Uhen, 2010), marking the third major radiation. From the Middle Miocene (12 Ma) on, and especially during the Pliocene (2.5–5.3 Ma), “modern” mysticetes and odontocetes radiated while archaic groups disappeared, e.g., Eurhinodelphinidae and Squalodontidae. Cetotheres declined into the Pleistocene, leaving only Caperea. Crown balaenopterids and delphinoids radiated to become major components of fossil assemblages. Ocean dolphins (Delphinidae) radiated from Late Miocene onward (McGowen et al., 2009, Bianucci, 2013), to dominate Pliocene to modern oceans. Monodontids are rare beyond their modern Arctic range (Vélez-Juarbe and Pyenson, 2012); the related Odobenocetopsidae occur only in Peruvian-Chilean strata. Many extant genera appeared by the Pleistocene, 2.5 Ma, but history is uncertain for the following ice ages because of a patchy fossil record generated by fluctuating sea levels. It has been suggested that many north–south species pairs evolved in the later Pleistocene, but molecular studies point to earlier divergences.
Darwin’s sexual selection may account for sexual dimorphism, particularly involving display structures, and has been linked with polygamous mating systems. Examples of possible sexually selected structures in male Cetacea include the large dorsal fin in Orcinus orca, conspicuous mandibular teeth in many ziphiids, and the prominent tusks in Monodon monoceros. Sexual selection could explain size dimorphism in, e.g., male Physeter macrocephalus—with its huge forehead—and female Balaenoptera species. There are no convincing cases for cetacean speciation by hybridization. Cetacean hybrids are known, for example, in Balaenoptera, between Phocoenoides and Phocoena, and between genera of Delphinidae (Crossman et al., 2016). Coevolution, especially involving mimicry, predator–prey, and host–parasite interactions, is an important phenomenon. Cetacean mimicry occurs in pygmy sperm whales (Kogia), with a remarkably shark-like form, underslung jaw, and pigmented false gill slit. Presumably, looking like a predator will lessen the chance of being eaten. The evolution of macropredators, e.g., killer whale, Orcinus, might produce adaptive responses in potential prey, such as changed habitat preferences and sound communication frequencies. Convergent evolution involves structural or ecological similarities not inherited from a recent common ancestor. The long-jawed “river dolphins” encompass four species in four different families (Fig. 1). One, Platanista, is convergent in its riverine habits, small body size, and long rostrum with the three closely related delphinidans Inia, Pontoporia, and Lipotes. The southern delphinid Cephalorhynchus hectori is similar, in body form and aspects of lifestyle, to the unrelated porpoise Phocoena phocoena (Phocoenidae). Unrelated groups have convergently reduced and lost teeth, as seen in living Mesoplodon (Ziphiidae) and the Pliocene ziphiid-mimic delphinid Australodelphis. Developmental mechanisms underlie evolution. One, heterochrony, involves change in timing or rate of development of structures relative to the situation in an ancestor. Juvenile structures may persist into adult stages (pedomorphosis), whereas other structures develop “beyond” that of the ancestral adult stage (peramorphosis) (Tsai and Fordyce, 2014). Possible pedomorphic features include the shortened intertemporal region, the rounded cranium and persistent interparietal bone on the skull of Delphinidae and Phocoenidae, and the down-turned rostrum and relatively symmetrical skull in Phocoenidae. Possible peramorphic features include extra body parts, e.g., increase in number of vertebrae, as in Dalls porpoise, Phocoenoides dalli, or extra phalanges generated through a delayed halt in development.
IV. Evolutionary Processes
V. Evolution and Geography
Darwin’s original evolutionary process, natural selection, adapts organisms to their environment by “fine-tuning” structure and behavior. The result is differential reproductive success. Competition for limited resources, especially food, is axiomatic for natural selection. Baleen whales and other plankton-eating vertebrates might compete, but the structure of the feeding apparatus of sympatric baleen whales, feeding mode, and geographic distribution indicate limited niche overlap between mysticete species (Pastene et al., 2007). Fossil platanistoid dolphins declined in diversity as delphinoids diversified later in the Miocene; extinction in one group and radiation in another could indicate that delphinoids outcompeted platanistoids. However, differences in skeletal structure imply little ecological overlap between the two groups. Perhaps changing oceanic circulation and climate caused the extinction of platanistoids, while delphinoids radiated coincidentally.
Darwin linked speciation to geography. A species range may be split by a change in physical habitat (split by a vicariant event), or be expanded by dispersal beyond normal limits. Geographically isolated populations may then diverge and speciate. During 50 Ma of cetacean history, geographic changes have included the closure or opening of straits and ocean basins, swings in continental shelf habitat area through sea level fluctuations, and major shifts in current systems, upwellings, and latitudinal water masses. Oceanic temperature regimes changed in parallel. This physical evolution of the oceans probably influenced cetacean evolution at many levels. The distributions of modern and fossil Cetacea suggest an important role for geography in evolution (Fig. 2). Some living cetaceans have closely related north–south species pairs, but do not occur in the tropics. Such antitropical distributions probably arose
C
184
C
Cetacean Evolution
allopatrically when populations were separated by tropical sea temperatures or current regimes, leading to speciation. Antitropical distributions occur in rorquals (Balaenoptera), right whales (Eubalaena), beaked whales (Berardius, Hyperoodon, and Mesoplodon), and dolphins (Delphinidae, e.g., Lissodelphis) (Rice, 1998). Molecular studies reveal that six antitropical and/or circum-Antarctic species of Lagenorhynchus dolphins split at varying times, not only during the recent (~2.5 Ma) ice ages, and that these species represent two or more lineages (Harlin-Cognato, 2010). Cephalorhynchus probably speciated around the Southern Ocean, with four distinctly circum-Antarctic/species. There is some fossil evidence for allopatric speciation: related species of the small Miocene dolphin Kentriodon from California and Maryland presumably evolved from an ancestor that ranged through the Central American Seaway before the uplift of Panama. The endangered vaquita, Phocoena sinus, from the Gulf of Mexico, probably originated when a few Burmeisters porpoises, Phocoena spinipinnis, dispersed across the equator probably during the Pleistocene. The vaquita, with its limited distribution and low genetic variability, illustrates founder effects: a new species, in an isolated region beyond normal range limits, may arise from a few original founders which are not genetically representative of the original population. Rapid sea level fluctuations changed continental shelf habitats during many glacial cycles since 2.5 Ma. During the last glacial maximum 17,000–19,000 years ago, sea level was 120 m lower than today, reducing shelf habitat for short intervals (Ludt and Rocha, 2015). Such change could affect normal ranges and habitats (Pyenson and Lindberg, 2011), perhaps causing habitat shift or extinctions. However, if species durations typically exceed 100,000 years, then most living cetacean species have survived many such fluctuations. Late Pliocene and early Pleistocene Cetacea include a few species from shallow-water habitats (e.g., the cetothere Herpetocetus, and dolphin Parapontoporia) that might have later disappeared because of Pleistocene climate changes and/or habitat loss (Boessenecker and Poust, 2015). Some cetacean groups have changed their range over time. Archaeocetes originated in the (sub)tropics, but later spread to temperate regions which have remained the region of peak (modern) cetacean diversity. The beluga and narwhal (Monodontidae) are now Arctic, but during warmer Pliocene times (4 Ma), monodontids occurred far south in subtropical waters (Vélez-Juarbe and Pyenson, 2012). New species might evolve by anagenesis, transforming from an ancestral to descendant species without lineage splitting, particularly in geographically wide-ranged species. Among living Cetacea, the sperm whale Physeter macrocephalus represents a genus with a single abundant and widely distributed species with no close relatives (sister species), and anagenesis might explain its history. Freshwater settings were important in the early transition of cetaceans from land to sea in the Tethys. Early archaeocetes were amphibious, with well-developed hindlimbs. Freshwater habits for some archaeocetes are indicated by oxygen isotopes from teeth. Fossil Neoceti show several much later reinvasions of freshwaters. For example, an unnamed possible platanistoid dolphin occurs in Late Oligocene lake sediments of central Australia. The presence of several specimens suggests long-term occupation of the habitat. Other fossil odontocetes from freshwater sediments include a large ziphiid from Kenya, and dolphins from China, California, and several locations in South America. All modern “river dolphins” had marine ancestors, some known from fossils, which invaded freshwaters in Asia and South America in several separate events. Modern mysticetes may range into rivers, but are not reported as fossil from freshwater settings.
VI. Life History Traits Cetaceans are K strategists in terms of life history (Estes, 1979): large animals that reproduce slowly, produce one offspring, show significant parental care of young, have long reproductive lives, and have relatively low mortality rates. This reproductive strategy has been linked evolutionarily to the nutritional requirements of the young and parents, and thus to food availability. Cetaceans show major evolutionary patterns linked to oceanic change, supporting the idea that food resources have helped to drive cetacean history. The exact roles of physical versus biological effects, viz., bottom-up or top-down drivers, in cetacean evolution are contentious.
VII. Taxonomic Longevity How long do species and genera persist? Few fossil species, if any, have ranges longer than one geological stage (stage: a time unit commonly 4–5 Ma). Among extinct Cetacea, the close-spaced succession of Eocene archaeocetes suggests species durations of 1–2 Ma. Living species range back into the Pleistocene, also implying durations of ~2 Ma. For living Balaenoptera species, molecular estimates for lineage splits range from 6–10 Ma to possibly 20 Ma, older than indicated by fossils. Consider other complications: a single lineage might contain a succession of species ending with a geologically young living species, there are negligible fossil records for living species, and the stratigraphic record for balaenopterids since 20 Ma is generally sparse (Marx and Fordyce, 2015). Extinct fossil species in crown Balaenoptera are of Pliocene to Late Miocene age. For odontocetes, a fossil-calibrated molecular phylogeny indicates that some living delphinid species lineages split only 1–2 Ma (McGowen et al., 2009). Little is known about quantified rates of evolution in Cetacea. A phylogeny for fossil and living Mysticeti shows a rapid Oligocene radiation, but no later peaks (Marx and Fordyce, 2015). Unlike the situation for some fossil land mammals, the cetacean record is too sparse to quantify change in structure over time. For living species, no speciation event has been dated reliably enough to clearly reveal evolutionary rate.
VIII. Diversity and Disparity Diversity is the number of species within a taxon (e.g., a genus or family), whereas disparity involves variation in structure within a taxon. Diversity is easily assessed, because advances in the philosophy and practice of systematics have produced an accepted classification of living cetaceans, but the study of disparity is still developing. The two living clades Odontoceti and Mysticeti differ markedly in diversity (Committee on Taxonomy, 2016). Mysticetes include 14 species in four families. The Balaenopteridae is most speciose, with eight species in two genera. Balaenoptera species vary in size, distribution, behavior, and especially aspects of the feeding apparatus (baleen size and spacing, size and shape of the upper jaw). Skeletal differences are rather minor, and disparity appears low. The gray whale, Eschrichtius robustus, is structurally quite different (disparate) from other mysticetes and is generally placed in its own family, but some phylogenies place it in the Balaenopteridae. Fossils show that gray whales lived in the Pliocene, ~4 Ma, with a predicted lineage origin of ~10 Ma. Odontocetes include at least 75 species in 10 families. With 37 species, Delphinidae is the most diverse family of cetaceans, and disparity seems higher than, e.g., within Balaenopteridae. Delphinids vary markedly in body size and proportion, skull form, proportions of the feeding apparatus and teeth, and distribution of air sinuses in the skull base. Among beaked whales (Ziphiidae; 22 species), Mesoplodon has 15 rather similar species in which only adult males are separated easily. Disparity here appears low and awaits
Cetacean Evolution explanation in terms of evolutionary ecology. Each of the four species of small long-beaked “river dolphins” represents a single family: Lipotidae, Iniidae, Pontoporiidae, and Platanistidae. These superficially similar dolphins differ markedly in skull form—hence the common separation into four families. The most intriguing is Platanista gangetica (Platanistidae), which is the last of the ancient and once diverse superfamily Platanistoidea. For crown Platanista, crown Platanistidae, and crown Platanistoidea, diversity is low (one or two living species of Platanista), with no fossil record, but stem platanistoids include diverse species ranging back to 29–28 Ma. Odontocetes are structurally disparate. Variation in the skull involves the shape, size, and composition of the feeding apparatus and teeth, facial region, including bony origin for nasofacial muscles implicated in echolocation, nasal passages, acoustic system, and air sinuses in the skull base. Disparity suggests specialization in many directions, but we struggle to understand the evolution of structural diversity. Future study of odontocete structural patterns could involve constructional morphology, three-dimensional geometric morphometrics, and finite element analysis.
IX. Extinction Extinction, the disappearance of lineages, is the fundamental natural complement to evolution. A species goes extinct when the number of individuals and geographic range drops to zero. The fossil record reveals that extinction is inevitable and usually terminal; few species go extinct by evolving into descendants. For most fossil cetacean species, the record comprises one or a few specimens that are rarely complete or in an obvious stratigraphic succession. Accordingly, we are uncertain whether the latest known individual is indeed the last of a species, or how to explain the cause of extinction. Among different styles of extinction, there is no evidence that cetaceans have been involved in a short, dramatic, mass extinctions comparable to that affecting nonavian dinosaurs. Taxonomic extinction involves the better documented disappearance of clades like the Squalodontidae and Aetiocetidae. Single-species extinction probably accounts for most of the record: piecemeal disappearance for uncertain reason. Many causes are possible (change in habitat, climate, or prey distribution, predation or pandemic) but we have little clue. Human impact may drive cetacean extinction (e.g., Lipotes) in the Anthropocene. Species susceptible to extinction are those in low-diversity clades (e.g., one or two species in a genus), with no close relatives, localized in physical settings that are unstable over geological time. For Cetacea, this means particularly the “river dolphins.” Conversely, widely distributed oceanic species would seem at less risk. Extinction begs the question: are there vacant modern niches that formerly were occupied by Cetacea? For example, long-jawed stem-Platanistidae lived in shallow marine settings until about 10 Ma, but Platanista now occurs only in freshwaters. Similarly, species of Squalodontidae and Eurhinodelphinidae were widely distributed before their demise in the later Miocene. Judging from the functional complexes seen in the latter fossils, there are no modern equivalents to these groups: some morphotypes and lifestyles have disappeared.
See Also the Following Articles Archaeocetes, Archaic n Basilosaurids and Kekenodontids
References Bajpai, S., and Thewissen, J.G.M. (2014). Protocetid cetaceans (Mammalia) from the Eocene of India. Palaeont. Elec. 17(34A), 1–19. Bianucci, G. (2013). Septidelphis morii, n. gen. et sp., from the Pliocene of Italy: new evidence of the explosive radiation of true dolphins (Odontoceti, Delphinidae). J. Vert. Paleo. 33, 722–740.
185
Boessenecker, R.W., and Poust, A.W. (2015). Freshwater occurrence of the extinct dolphin Parapontoporia (Cetacea: Lipotidae) from the upper Pliocene nonmarine Tulare Formation of California. Palaeontology 58, 489–496. Boyden, A., and Gemeroy, D. (1950). The relative position of the Cetacea among the orders of Mammalia as indicated by precipitin tests. Zoologica 35, 145–151. Buono, M.R., Fernández, M.S., Reguero, M.A., Marenssi, S.A., Santillana, S.N., and Mörs, T. (2016). Eocene basilosaurid whales from the La Meseta Formation, Marambio (Seymour) Island, Antarctica. Ameghiniana 53, 296–315. Churchill, M., Martinez-Caceres, M., de Muizon, C., Mnieckowski, J., and Geisler, J.H. (2016). The origin of high-frequency hearing in whales. Curr. Biol. doi:10.1016/j.cub.2016.06.004. Committee on Taxonomy (2016). List of marine mammal species and subspecies. Society for Marine Mammalogy, www.marinemammalscience.org. Crossman, C.A., Taylor, E.B., and Barrett‐Lennard, L.G. (2016). Hybridization in the Cetacea: widespread occurrence and associated morphological, behavioral, and ecological factors. Ecol. Evol. 6, 1293–1303. Estes, J.A. (1979). Exploitation of marine mammals: r-selection of K-strategists? J. Fish. Res. Bd. Can. 36, 1009–1017. Flower, W.H. (1883). On whales, past and present, and their probable origin. II. Nature 28, 226–230. Harlin-Cognato, A.D. (2010). The Dusky Dolphins’ place in the delphinid family tree. In “Dusky Dolphin: Master Acrobat off Different Shores”, (B. Wursig, and M. Wursig, Eds), pp. 1–20. Academic Press, Amsterdam. Lindberg, D.R., and Pyenson, N.D. (2007). Things that go bump in the night: evolutionary between cephalopods and cetaceans in the Tertiary. Lethaia 40, 335–343. Ludt, W.B., and Rocha, L.A. (2015). Shifting seas: the impacts of Pleistocene sea-level fluctuations on the evolution of tropical marine taxa. J. Biogeog. 42, 25–38. Marx, F.G., and Fordyce, R.E. (2015). Baleen boom and bust: a synthesis of mysticete phylogeny, diversity and disparity. R. Soc. Open Sci. 2. doi:10.1098/rsos.140434. McGowen, M.R., Spaulding, M., and Gatesy, J. (2009). Divergence date estimation and a comprehensive molecular tree of extant cetaceans. Mol. Phylogenet. Evol. 53, 891–906. Pastene, L.A., Goto, M., Kanda, N., Zerbini, A.N., Kerem, D.A.N., Watanabe, K.B.Y., Hasegawa, M., Nielsen, R., Larsen, F., and Palsboll, P.J. (2007). Radiation and speciation of pelagic organisms during periods of global warming: the case of the common minke whale, Balaenoptera acutorostrata. Mol. Ecol. 16, 1481–1495. Pyenson, N.D., and Lindberg, D.R. (2011). What happened to Gray Whales during the Pleistocene? The ecological impact of sea-level change on benthic feeding areas in the North Pacific Ocean. PLoS One 6. doi:10.1371/journal.pone.0021295. Quental, T.B., and Marshall, C.R. (2010). Diversity dynamics: molecular phylogenies need the fossil record. Tr. Ecol. Evol. 25, 434–441. Rice, D.W. (1998). Marine Mammals of the World. Systematics and Distribution. Society for Marine Mammalogy, Lawrence, KS. Rommel, S.A., Costidis, A.M., Fernandez, A., Jepsono, P.D., Pabst, D.A., McLellan, W.A., et al. (2006). Elements of beaked whale anatomy and diving physiology and some hypothetical causes of sonar-related stranding. J. Cet. Res. Manag. 7, 189–209. Thewissen, J.G.M., Cooper, L.N., Clementz, M.T., Bajpai, S., and Tiwari, B.N. (2007). Whales originated from aquatic artiodactyls in the Eocene epoch of India. Nature 450, 1190–1194. Tsai, C.-H., and Fordyce, R.E. (2014). Disparate heterochronic processes in baleen whale evolution. Evol. Biol. doi:10.1007/ s11692-11014-19269-11694. Uhen, M.D. (2010). The origin(s) of whales. Ann. Rev. Earth Planet. Sci. 38, 189–219. Vélez-Juarbe, J., and Pyenson, N.D. (2012). Bohaskaia monodontoides, a new monodontid (Cetacea, Odontoceti, Delphinoidea) from the Pliocene of the western North Atlantic Ocean. J. Vert. Paleo. 32, 476–484.
C
C
Cetacean Evolution
Cetaceans are also important consumers. Their large body sizes, high metabolic rates, and positions as apex or near-apex predators mean that they take tons of prey with implications for the structure of marine ecosystems themselves. The “krill surplus hypothesis” (Laws, 1977) proposed that the removal of large whales from the Southern Ocean released up to 150 million tons of krill per year from whale predation, a prey base that was theoretically then available to other krill predators. Subsequent growth in penguin and pinniped populations was attributed to this competitive release (reviewed in Ballance et al., 2006b). Killer whale predation may drive population dynamics of their prey, sea otters, elephant seals, gray whales, and humpback whales among them, with the potential for cascading effects. For example, killer whale predation was proposed to explain apparently sequential declines in pinniped populations in the north Pacific, as killer whales depleted these prey, and subsequently shifted to unexploited species (Springer et al., 2003). These ideas have been hotly debated and research attempting to clarify them is confounded by spatial and/or temporal mismatch between datasets, disagreement regarding the extent to which killer whales can (or do) switch between different prey types, and massive anthropogenic influences on marine ecosystems (e.g., commercial exploitation and subsequent recovery of protected species, climate change and its bottom-up influences). Nevertheless, there is intriguing and strong evidence that top-down forcing through cetacean predation is an important structuring force for marine ecosystems. Particularly as large whales recover from commercial exploitation, the appearance of killer whale predation on them is increasingly being documented, providing an opportunity for ecologists to document ecosystem change in our lifetimes (Pitman et al., 2014). The role that cetaceans play in marine ecosystems is an active and exciting focus of research in cetacean ecology.
See Also the Following Articles Biogeography n Distribution n Ecology n Variation n Ocean Environments n Pinniped Ecology
Geographic
References Ballance, L.T., Pitman, R.L., and Fiedler, P.C. (2006a). Oceanographic influences on seabirds and cetaceans of the eastern tropical Pacific: A review. Prog. Oceanogr. 69, 360–390. Ballance, L.T., Pitman, R.L., Hewitt, R., Siniff, D., Trivelpiece, W., Clapham, P., and Brownell Jr., R.L. (2006b). The removal of large whales from the Southern Ocean. Evidence for long-term ecosystem eff ects? In “Whales, Whaling, and Ocean Ecosystems”, (J.A. Estes, D.P. DeMaster, D.F. Doak, T.M. Williams, and R.L. Brownell Jr., Eds), pp. 215–230. University of California Press, Berkeley, CA. Becker, E.A., Foley, D.G., Forney, K.A., Barlow, J., Redfern, J.V., and Gentemann, C.L. (2012). Forecasting cetacean abundance patterns to enhance management decisions. Endang. Species Res. 16, 97–112. Corkeron, P.J., and Connor, R.C. (1999). Why do baleen whales migrate? Mar. Mamm. Sci. 15, 1228–1245. Durban, J.W., and Pitman, R.L. (2011). Antarctic killer whales make rapid, round-trip movements to subtropical waters: evidence for physiological maintenance migrations? Biol. Lett. doi:10.1098/ rsbl.2011.0875. Estes, J.A. (2006). Whales, Whaling, and Ocean Ecosystems. University of California Press. Heyning, J.E., and Mead, J.G. (1996). Suction Feeding in Beaked Whales: Morphological and Observational Evidence. Natural History Museum of Los Angeles County. Laws, R.M. (1977). Seals and whales of the Southern Ocean. Philos. Trans. R. Soc. Lond. B 27, 81–96.
Melville, H. (1851). Moby Dick, or, The Whale. Harper and Brothers, New York, NY Norris, K.S., and Møhl, B. (1983). Can odontocetes debilitate prey with sound? Am. Nat. 122, 85–104. Obst Jr., B.S., and Hunt, G.L. (1990). Marine birds feed at gray whale mud plumes in the Bering Sea. Auk 107, 678–688. Perrin, W.F. (1991). Why are there so many kinds of whales and dolphins? BioScience 41, 460–461. Pitman, R.L., Ballance, L.T., Mesnick, S.I., and Chivers, S.J. (2001). Killer whale predation on sperm whales: observations and implications. Mar. Mamm. Sci. 17(3), 494–507. Pitman, R.L., and Stinchcomb, C. (2002). Rough-toothed dolphins (Steno bredanensis) as predators of mahimahi (Coryphaena hippurus). Pac. Sci. 56, 447–450. Pitman, R.L., Durban, J.W., Greenfelder, M., Guinet, C., Jorgensen, M., Olson, P.A., Plana, J., Tixier, P., and Towers, J.R. (2011). Observations of a distinctive morphotype of killer whale (Orcinus orca), type D, from subantarctic waters. Polar Biol. 34(2), 303–306. Pitman, R.L., and Durban, J.W. (2012). Cooperative hunting behavior, prey selectivity and prey handling by pack ice killer whales (Orcinus orca), type B, in Antarctic Peninsula waters. Mar. Mamm. Sci. 31, 16–36. Pitman, R.L., Totterdell, J.A., Fearnbach, H., Ballance, L.T., Durban, J.W., and Kemps, H. (2014). Whale killers: Prevalence and ecological implications of killer whale predation on humpback whale calves off Western Australia. Mar. Mamm. Sci. doi:10.1111/mms.12182. Redfern, J.V., et al. (19 authors) (2006). Techniques for cetacean–habitat modeling. Mar. Ecol. Prog. Ser. 310, 271–295. Roman, J., Estes, J.A., Morissette, L., Smith, C., Costa, D., McCarthy, J., Nation, J.B., Nicol, S., Pershing, A., and Smetacek, V. (2014). Whales as marine ecosystem engineers. Front. Ecol. Environ. 12(7), 377–385. Santora, J.A., Reiss, C.S., Loeb, V.J., and Veit, R.R. (2010). Spatial association between hotspots of baleen whales and demographic patterns of Antarctic krill Euphausia superba suggests size-dependent predation. Mar. Ecol. Prog. Ser. 405, 255–269. Schakner, Z.A., Lunsford, C., Straley, J., Eguchi, T., and Mesnick, S.L. (2014). Using models of social transmission to examine the spread of longline depredation behavior among sperm whales in the Gulf of Alaska. PLoS One 9(10), e109079. Springer, A.M., Estes, J.A., Van Vliet, G.B., Williams, T.M., Doak, D.F., Danner, E.M., and Pfister, B. (2003). Sequential megafaunal collapse in the North Pacific Ocean: An ongoing legacy of industrial whaling. Proc. Natl. Acad. Sci. 100(21), 12223–12228. Tittensor, D.P., Mora, C., Jetz, W., Lotze, H.K., Ricard, D., Berghe, E.V., and Worm, B. (2010). Global patterns and predictors of marine biodiversity across taxa. Nature 466(7310), 1098–1101.
CETACEAN EVOLUTION R. Ewan Fordyce I. Patterns of Evolution Anatomists of the 1600s–1700s, such as Ray and Hunter, showed that cetaceans share many structures with hoofed mammals: an ungulate-like larynx, stomach, reproductive organs, and fetal membranes (Flower, 1883). An early serological study (Boyden and Gemeroy, 1950) showed cetaceans close to ungulates, foreshadowing molecular approaches. Modern studies place the clade Cetacea in the Cetartiodactyla—hoofed mammals (artiodactyls, ruminants). Fossils reveal shared skeletal structures with artiodactyls, and show that cetaceans appeared more than 50 million years ago. Cetaceans
REF 08/16
50
Delphinidae
Monodontidae
Phocoenidae
Radiation of delphinoids
Radiation of Neoceti
?
Ultrasonic hearing Origin of neoceti Radiation of toothed mysticeti Radiation of oceanic cetacea including polar species High frequency hearing
†Odobenocetopsidae
Pontoporiidae
Iniidae †Albireonidae
Platanistidae Ziphiidae Lipotidae †Kentriodontidae
†Squalodelphinidae
†Eurhinodelphinidae †Allodelphinidae
Kogiidae †Eoplatanistidae
†Squalodontidae
†Waipatiidae
†Patriocetidae
†Mirocetidae †Agorophiidae
Extinction of many archaic neocete groups
†Simocetidae
Radiation of basal balaenopteroids Baleen-assisted filter feeding
Physeteridae
Balaenopteridae includes Eschrichtiinae
Basal balaenopteridae
†Pelocetus group
181
Odontoceti
†Xenorophidae †Ashleycetidae
†Mauicetus group
Neobalaeninae
†Llanocetidae
†Eomysticetidae
†Mammalodontidae †Aetiocetidae
Late Middle
†Mesonychia
Early Late Early
Archaeoceti †Raoellidae †Pakicetidae †Ambulocetidae †Remingtonocetidae †Protocetidae †Basilosauridae †Kekenodontidae
40
E O C E N E
Late
30
O L I G O
Middle
20
Early
Millions of years before present
10
M I O C E N E
†Parietobalaena group
Balaenidae
PLEIS P L I
Cetotheriidae
Mysticeti
EL
0
Hippopotamidae
Cetacean Evolution
Key to groups, age ranges, symbols Extant (crown) clade Extinct (stem) clade Extinct paraphyletic group Extinct taxon Freshwater habits obligate or occasional Pleistocene Pleis Pliocene Plio
†
Radiation of riverine to shallow coastal Cetacea
Figure 1 Phylogeny of living and fossil Cetacea, with families calibrated against time. Some key ecological/behavioral shifts are shown. This composite is based on Uhen (2010) for Archaeoceti, Marx and Fordyce (2015) for Mysticeti, and Churchill et al. (2016) for Odontoceti. Other phylogenies show different patterns. are the most diverse clade of modern marine mammals in terms of species, ecology, and range. Cetaceans have a sparse fossil record, lacking a close succession of ancestors to descendants that might show evolution. Hennig’s methodology of cladistic analysis suits the high “information content” of cetaceans. It has produced phylogenies that integrate morphology and molecules from living and/or fossil species. Cladistic methods reveal clades united by common ancestry (Fig. 1). Clades are the foundation for formal taxonomic names (Committee on Taxonomy, 2016), including the two major groups, Odontoceti and Mysticeti. Fossils provide the only direct evidence of extinct species and structures; they indicate clades and ecologies not seen today. The third division of Cetacea is the Archaeoceti, a grade (paraphyletic taxon) including the basal or stem cetaceans. Patterns from modern and fossil species have, since 2000, hugely expanded understanding of evolution, although high-level/deep time phylogenies (Fig. 1) show limited agreement. Discussion of evolution depends on agreed phylogenetic approaches. Concepts of crown and stem group help to compare fossil versus molecular evidence for deep-time events. A crown group comprises all living species in a clade, and all descendants of their latest common ancestor. The stem group comprises those species, all extinct, that are closer to the crown group than to any other clade.
Evolutionary rates, modes, and mechanisms of cetacean ancestor-to-descendant transitions are poorly understood (Quental and Marshall, 2010). Evolutionary processes at the species level might include natural selection, sexual selection, coevolution, dispersal, founder effects, vicariance, and hybridization, discussed further below.
II. Ecology Past and Present Structure is the link between genome and ecology. Structure involves functional complexes linked to ecology—to interactions between species and biological, physical, and chemical environment. Musculoskeletal systems in living species help to reveal function and biology (Rommel et al., 2006). But, how do subtle differences between related species help to separate niches? How do family-level functional complexes (e.g., acoustic sinuses in Delphinidae) link to lifestyle, habitat, and species diversity? Numerical methods, e.g., geometric morphometrics, may quantify and elucidate structural patterns in ontogeny and ecology. On geological timescales, evolution and paleoecology are inextricably linked, for evolution occurs through natural selection and adaptation to the environment. Ecological phenomena—including feeding and predator–prey interactions, migration, nutrient cycling, thermal adaptations, habitat shifts, and strandings and burial— strongly inform evolution.
C
Cetacean Evolution
182
Geographic patterns important in cetacean evolution
Habitat shift: polar monodontids had temperate-tropical relatives 4–6 Ma m
†Parapontoporia
f
Lipotes f
C
f f Platanista
K
Berardius bairdii, Lissodelphis borealis
an origins Tethy †Prolipotes
K
†Pomatodelphis m
P. sinus
K
f
m
Fossils reflect past links - Atlantic/Pacific Kentriodon
spp and Central American Seaway K
f
Antitropical patterns -
†Ziphiidae f
Sotalia Inia f f †Platanistinae
sister-taxa separated by tropical waters
Major habitat shift:
m
tropical origins >50 Ma, to polar south 40–45 Ma
Founder effects -
†Platanistoidea?
Phocoena sinus evolved from P. spinipinnis
f
Cosmopolitan Physeter macrocephalus
Winter tropical breeding
Rorqual migration
C. heavisidii C. hectori
Symbols f Freshwater dolphin location f Freshwater fossil cetacean location Representative fossil location m Monodontid location K Kentriodon location
C. commersonii
Berardius arnuxii, Lissodelphis peronii
f
Pontoporia
C. eutropia
Circum-polar pattern -
Cephalorhynchus speciation around Southern Ocean
Summer polar feeding
C. commersonii
Figure 2 Distribution patterns and cetacean evolution: key fossil localities, antitropical and circum-Antarctic distributions, allopatric species pairs between oceans, founder effects, convergent origins for various freshwater dolphins, habitat expansion from tropical ranges involving rise of pelagic habits and occupation of polar waters, and geologically recent changes in habitat. Ancient lifestyles can be inferred by “taxonomic uniformitarianism,” using modern ecology to understand fossils: the present is the key to the past. For example, fossil beaked whales may have been deep divers. However, fossils show that cetacean evolution involves structural change, in turn implying change in ecology. How far back might we “push” modern ecology? Past lifestyle may be inferred by analogy and functional morphology, using known modern correlations of muscle, nerve, and vessels to bone. The extinct Peruvian Odobenocetops “walrus whales” have no structural equivalents among living Cetacea. Rather, their jaws are similar to those of the unrelated walrus, Odobenus, implying comparable suction feeding on molluscs. Extant phylogenetic bracketing predicts that a fossil in a crown (living) clade would have the same attributes as the living species. For example, extinct species within the crown Odontoceti can be inferred to have echolocated because phylogenetically adjacent living species echolocate.
III. Major Radiations Molecular phylogenies show relationships among living cetaceans (e.g., McGowen et al., 2009), but lack the extinct lineages which helped shape cetacean evolution. Fossil-based phylogenies are limited by the patchy fossil record, but they do anchor lineages in time and space, and do show changes in structure and diversity. Family patterns help to recognize three major radiations—times of functional, ecological, and taxonomic diversification—in cetacean history (Fig. 1).
Cetaceans evolved on the margins of the former tropical Tethys seaway, between India and Asia, early in the Eocene, about 53–45 million years before present (Ma) (Fig. 2). The early small, amphibious species of Pakicetidae probably arose from terrestrial ancestors such as the mesonychids or, more favored, the raoellids. Pakicetids occur in freshwater strata but possibly used near-coastal habitats. Perhaps rivers were a refuge from predators (Thewissen et al., 2007) and a source of food. Two other short-ranged Tethyan amphibious clades are the Ambulocetidae and Remingtonocetidae. The diverse Protocetidae includes 19+ genera (pbdb.org) of Archaeoceti that were more specialized for marine life than pakicetids, ambulocetids, and remingtonocetids (Bajpai and Thewissen, 2014). Concurrent changes in locomotory and hearing mechanisms allowed dispersal beyond the Tethys, foreshadowing fully oceanic habits. Species in the Middle to Late Eocene family Basilosauridae were pelagic, judging from their spread to temperate and Antarctic latitudes by 39–40 Ma (Buono et al., 2016). In terms of disparity and presumably, ecology, basilosaurids were more comparable with living mysticetes than with odontocetes. Taxa varied in body size, hind-limb reduction, skull and jaw proportions, tooth form and number, and aspects of the hearing apparatus. Archaeocete diversity dropped late in Eocene times (Uhen, 2010), foreshadowing the rise of Neoceti. The second major radiation, involving the Neoceti or crown-Cetacea, started late in the Eocene, and continued in the Oligocene (Marx and Fordyce, 2015) (Fig. 1). The two living clades, Mysticeti and Odontoceti, appeared, and diversified rapidly in about 5 Ma,
Cetacean Evolution
183
after originating from Eocene archaeocetes which probably did not echolocate or filter-feed. Concurrent events included the final breakup of Gondwana, continued opening of the Southern Ocean, cooling and increased tropics-to-polar temperature gradients, and changes in ocean ecosystems and productivity. It is likely that cetaceans responded to new ecological opportunities in rapidly changing oceans (Lindberg and Pyenson, 2007; Marx and Fordyce, 2015). The most basal mysticetes were extinct toothed families, of latest Eocene to early Miocene age: Llanocetidae, Mammalodontidae, and Aetiocetidae. They were probably raptorial, perhaps using suction feeding. Toothless filter-feeding baleen whales evolved during the Oligocene, as shown by the extinct Eomysticetidae and by basal balaenopteroids on the lineage to rorquals. Fossil Balaenidae, Cetotheriidae, archaic balaenopteroids, and Balaenopteridae are widely known from Miocene strata, and phylogenies predict that many originated in the Oligocene (Marx and Fordyce, 2015). Oligocene odontocetes include diverse families that reflect a greater structural disparity and wider geographic range than for mysticetes. Examples include the Xenorophidae, Simocetidae, Agorophiidae, Waipatiidae, Squalodontidae, Patriocetidae, and Eurhinodelphinidae, all extinct, and a putative sperm whale, Physeteridae. Phylogenetic relationships between these groups, or with later lineages, are uncertain. Other families, some extant, appeared in the Miocene: Kogiidae, Ziphiidae, Allodelphinidae, Squalodelphinidae, and Platanistidae. Of note is the radiation of delphinoids including the Kentriodontidae, the “river dolphins” (Lipotidae, Iniidae, Pontoporiidae), Monodontidae, Phocoenidae, and Delphinidae (Fig. 1). Cetacean diversity peaked later in the Miocene (Uhen, 2010), marking the third major radiation. From the Middle Miocene (12 Ma) on, and especially during the Pliocene (2.5–5.3 Ma), “modern” mysticetes and odontocetes radiated while archaic groups disappeared, e.g., Eurhinodelphinidae and Squalodontidae. Cetotheres declined into the Pleistocene, leaving only Caperea. Crown balaenopterids and delphinoids radiated to become major components of fossil assemblages. Ocean dolphins (Delphinidae) radiated from Late Miocene onward (McGowen et al., 2009, Bianucci, 2013), to dominate Pliocene to modern oceans. Monodontids are rare beyond their modern Arctic range (Vélez-Juarbe and Pyenson, 2012); the related Odobenocetopsidae occur only in Peruvian-Chilean strata. Many extant genera appeared by the Pleistocene, 2.5 Ma, but history is uncertain for the following ice ages because of a patchy fossil record generated by fluctuating sea levels. It has been suggested that many north–south species pairs evolved in the later Pleistocene, but molecular studies point to earlier divergences.
Darwin’s sexual selection may account for sexual dimorphism, particularly involving display structures, and has been linked with polygamous mating systems. Examples of possible sexually selected structures in male Cetacea include the large dorsal fin in Orcinus orca, conspicuous mandibular teeth in many ziphiids, and the prominent tusks in Monodon monoceros. Sexual selection could explain size dimorphism in, e.g., male Physeter macrocephalus—with its huge forehead—and female Balaenoptera species. There are no convincing cases for cetacean speciation by hybridization. Cetacean hybrids are known, for example, in Balaenoptera, between Phocoenoides and Phocoena, and between genera of Delphinidae (Crossman et al., 2016). Coevolution, especially involving mimicry, predator–prey, and host–parasite interactions, is an important phenomenon. Cetacean mimicry occurs in pygmy sperm whales (Kogia), with a remarkably shark-like form, underslung jaw, and pigmented false gill slit. Presumably, looking like a predator will lessen the chance of being eaten. The evolution of macropredators, e.g., killer whale, Orcinus, might produce adaptive responses in potential prey, such as changed habitat preferences and sound communication frequencies. Convergent evolution involves structural or ecological similarities not inherited from a recent common ancestor. The long-jawed “river dolphins” encompass four species in four different families (Fig. 1). One, Platanista, is convergent in its riverine habits, small body size, and long rostrum with the three closely related delphinidans Inia, Pontoporia, and Lipotes. The southern delphinid Cephalorhynchus hectori is similar, in body form and aspects of lifestyle, to the unrelated porpoise Phocoena phocoena (Phocoenidae). Unrelated groups have convergently reduced and lost teeth, as seen in living Mesoplodon (Ziphiidae) and the Pliocene ziphiid-mimic delphinid Australodelphis. Developmental mechanisms underlie evolution. One, heterochrony, involves change in timing or rate of development of structures relative to the situation in an ancestor. Juvenile structures may persist into adult stages (pedomorphosis), whereas other structures develop “beyond” that of the ancestral adult stage (peramorphosis) (Tsai and Fordyce, 2014). Possible pedomorphic features include the shortened intertemporal region, the rounded cranium and persistent interparietal bone on the skull of Delphinidae and Phocoenidae, and the down-turned rostrum and relatively symmetrical skull in Phocoenidae. Possible peramorphic features include extra body parts, e.g., increase in number of vertebrae, as in Dalls porpoise, Phocoenoides dalli, or extra phalanges generated through a delayed halt in development.
IV. Evolutionary Processes
V. Evolution and Geography
Darwin’s original evolutionary process, natural selection, adapts organisms to their environment by “fine-tuning” structure and behavior. The result is differential reproductive success. Competition for limited resources, especially food, is axiomatic for natural selection. Baleen whales and other plankton-eating vertebrates might compete, but the structure of the feeding apparatus of sympatric baleen whales, feeding mode, and geographic distribution indicate limited niche overlap between mysticete species (Pastene et al., 2007). Fossil platanistoid dolphins declined in diversity as delphinoids diversified later in the Miocene; extinction in one group and radiation in another could indicate that delphinoids outcompeted platanistoids. However, differences in skeletal structure imply little ecological overlap between the two groups. Perhaps changing oceanic circulation and climate caused the extinction of platanistoids, while delphinoids radiated coincidentally.
Darwin linked speciation to geography. A species range may be split by a change in physical habitat (split by a vicariant event), or be expanded by dispersal beyond normal limits. Geographically isolated populations may then diverge and speciate. During 50 Ma of cetacean history, geographic changes have included the closure or opening of straits and ocean basins, swings in continental shelf habitat area through sea level fluctuations, and major shifts in current systems, upwellings, and latitudinal water masses. Oceanic temperature regimes changed in parallel. This physical evolution of the oceans probably influenced cetacean evolution at many levels. The distributions of modern and fossil Cetacea suggest an important role for geography in evolution (Fig. 2). Some living cetaceans have closely related north–south species pairs, but do not occur in the tropics. Such antitropical distributions probably arose
C
184
C
Cetacean Evolution
allopatrically when populations were separated by tropical sea temperatures or current regimes, leading to speciation. Antitropical distributions occur in rorquals (Balaenoptera), right whales (Eubalaena), beaked whales (Berardius, Hyperoodon, and Mesoplodon), and dolphins (Delphinidae, e.g., Lissodelphis) (Rice, 1998). Molecular studies reveal that six antitropical and/or circum-Antarctic species of Lagenorhynchus dolphins split at varying times, not only during the recent (~2.5 Ma) ice ages, and that these species represent two or more lineages (Harlin-Cognato, 2010). Cephalorhynchus probably speciated around the Southern Ocean, with four distinctly circum-Antarctic/species. There is some fossil evidence for allopatric speciation: related species of the small Miocene dolphin Kentriodon from California and Maryland presumably evolved from an ancestor that ranged through the Central American Seaway before the uplift of Panama. The endangered vaquita, Phocoena sinus, from the Gulf of Mexico, probably originated when a few Burmeisters porpoises, Phocoena spinipinnis, dispersed across the equator probably during the Pleistocene. The vaquita, with its limited distribution and low genetic variability, illustrates founder effects: a new species, in an isolated region beyond normal range limits, may arise from a few original founders which are not genetically representative of the original population. Rapid sea level fluctuations changed continental shelf habitats during many glacial cycles since 2.5 Ma. During the last glacial maximum 17,000–19,000 years ago, sea level was 120 m lower than today, reducing shelf habitat for short intervals (Ludt and Rocha, 2015). Such change could affect normal ranges and habitats (Pyenson and Lindberg, 2011), perhaps causing habitat shift or extinctions. However, if species durations typically exceed 100,000 years, then most living cetacean species have survived many such fluctuations. Late Pliocene and early Pleistocene Cetacea include a few species from shallow-water habitats (e.g., the cetothere Herpetocetus, and dolphin Parapontoporia) that might have later disappeared because of Pleistocene climate changes and/or habitat loss (Boessenecker and Poust, 2015). Some cetacean groups have changed their range over time. Archaeocetes originated in the (sub)tropics, but later spread to temperate regions which have remained the region of peak (modern) cetacean diversity. The beluga and narwhal (Monodontidae) are now Arctic, but during warmer Pliocene times (4 Ma), monodontids occurred far south in subtropical waters (Vélez-Juarbe and Pyenson, 2012). New species might evolve by anagenesis, transforming from an ancestral to descendant species without lineage splitting, particularly in geographically wide-ranged species. Among living Cetacea, the sperm whale Physeter macrocephalus represents a genus with a single abundant and widely distributed species with no close relatives (sister species), and anagenesis might explain its history. Freshwater settings were important in the early transition of cetaceans from land to sea in the Tethys. Early archaeocetes were amphibious, with well-developed hindlimbs. Freshwater habits for some archaeocetes are indicated by oxygen isotopes from teeth. Fossil Neoceti show several much later reinvasions of freshwaters. For example, an unnamed possible platanistoid dolphin occurs in Late Oligocene lake sediments of central Australia. The presence of several specimens suggests long-term occupation of the habitat. Other fossil odontocetes from freshwater sediments include a large ziphiid from Kenya, and dolphins from China, California, and several locations in South America. All modern “river dolphins” had marine ancestors, some known from fossils, which invaded freshwaters in Asia and South America in several separate events. Modern mysticetes may range into rivers, but are not reported as fossil from freshwater settings.
VI. Life History Traits Cetaceans are K strategists in terms of life history (Estes, 1979): large animals that reproduce slowly, produce one offspring, show significant parental care of young, have long reproductive lives, and have relatively low mortality rates. This reproductive strategy has been linked evolutionarily to the nutritional requirements of the young and parents, and thus to food availability. Cetaceans show major evolutionary patterns linked to oceanic change, supporting the idea that food resources have helped to drive cetacean history. The exact roles of physical versus biological effects, viz., bottom-up or top-down drivers, in cetacean evolution are contentious.
VII. Taxonomic Longevity How long do species and genera persist? Few fossil species, if any, have ranges longer than one geological stage (stage: a time unit commonly 4–5 Ma). Among extinct Cetacea, the close-spaced succession of Eocene archaeocetes suggests species durations of 1–2 Ma. Living species range back into the Pleistocene, also implying durations of ~2 Ma. For living Balaenoptera species, molecular estimates for lineage splits range from 6–10 Ma to possibly 20 Ma, older than indicated by fossils. Consider other complications: a single lineage might contain a succession of species ending with a geologically young living species, there are negligible fossil records for living species, and the stratigraphic record for balaenopterids since 20 Ma is generally sparse (Marx and Fordyce, 2015). Extinct fossil species in crown Balaenoptera are of Pliocene to Late Miocene age. For odontocetes, a fossil-calibrated molecular phylogeny indicates that some living delphinid species lineages split only 1–2 Ma (McGowen et al., 2009). Little is known about quantified rates of evolution in Cetacea. A phylogeny for fossil and living Mysticeti shows a rapid Oligocene radiation, but no later peaks (Marx and Fordyce, 2015). Unlike the situation for some fossil land mammals, the cetacean record is too sparse to quantify change in structure over time. For living species, no speciation event has been dated reliably enough to clearly reveal evolutionary rate.
VIII. Diversity and Disparity Diversity is the number of species within a taxon (e.g., a genus or family), whereas disparity involves variation in structure within a taxon. Diversity is easily assessed, because advances in the philosophy and practice of systematics have produced an accepted classification of living cetaceans, but the study of disparity is still developing. The two living clades Odontoceti and Mysticeti differ markedly in diversity (Committee on Taxonomy, 2016). Mysticetes include 14 species in four families. The Balaenopteridae is most speciose, with eight species in two genera. Balaenoptera species vary in size, distribution, behavior, and especially aspects of the feeding apparatus (baleen size and spacing, size and shape of the upper jaw). Skeletal differences are rather minor, and disparity appears low. The gray whale, Eschrichtius robustus, is structurally quite different (disparate) from other mysticetes and is generally placed in its own family, but some phylogenies place it in the Balaenopteridae. Fossils show that gray whales lived in the Pliocene, ~4 Ma, with a predicted lineage origin of ~10 Ma. Odontocetes include at least 75 species in 10 families. With 37 species, Delphinidae is the most diverse family of cetaceans, and disparity seems higher than, e.g., within Balaenopteridae. Delphinids vary markedly in body size and proportion, skull form, proportions of the feeding apparatus and teeth, and distribution of air sinuses in the skull base. Among beaked whales (Ziphiidae; 22 species), Mesoplodon has 15 rather similar species in which only adult males are separated easily. Disparity here appears low and awaits
Cetacean Evolution explanation in terms of evolutionary ecology. Each of the four species of small long-beaked “river dolphins” represents a single family: Lipotidae, Iniidae, Pontoporiidae, and Platanistidae. These superficially similar dolphins differ markedly in skull form—hence the common separation into four families. The most intriguing is Platanista gangetica (Platanistidae), which is the last of the ancient and once diverse superfamily Platanistoidea. For crown Platanista, crown Platanistidae, and crown Platanistoidea, diversity is low (one or two living species of Platanista), with no fossil record, but stem platanistoids include diverse species ranging back to 29–28 Ma. Odontocetes are structurally disparate. Variation in the skull involves the shape, size, and composition of the feeding apparatus and teeth, facial region, including bony origin for nasofacial muscles implicated in echolocation, nasal passages, acoustic system, and air sinuses in the skull base. Disparity suggests specialization in many directions, but we struggle to understand the evolution of structural diversity. Future study of odontocete structural patterns could involve constructional morphology, three-dimensional geometric morphometrics, and finite element analysis.
IX. Extinction Extinction, the disappearance of lineages, is the fundamental natural complement to evolution. A species goes extinct when the number of individuals and geographic range drops to zero. The fossil record reveals that extinction is inevitable and usually terminal; few species go extinct by evolving into descendants. For most fossil cetacean species, the record comprises one or a few specimens that are rarely complete or in an obvious stratigraphic succession. Accordingly, we are uncertain whether the latest known individual is indeed the last of a species, or how to explain the cause of extinction. Among different styles of extinction, there is no evidence that cetaceans have been involved in a short, dramatic, mass extinctions comparable to that affecting nonavian dinosaurs. Taxonomic extinction involves the better documented disappearance of clades like the Squalodontidae and Aetiocetidae. Single-species extinction probably accounts for most of the record: piecemeal disappearance for uncertain reason. Many causes are possible (change in habitat, climate, or prey distribution, predation or pandemic) but we have little clue. Human impact may drive cetacean extinction (e.g., Lipotes) in the Anthropocene. Species susceptible to extinction are those in low-diversity clades (e.g., one or two species in a genus), with no close relatives, localized in physical settings that are unstable over geological time. For Cetacea, this means particularly the “river dolphins.” Conversely, widely distributed oceanic species would seem at less risk. Extinction begs the question: are there vacant modern niches that formerly were occupied by Cetacea? For example, long-jawed stem-Platanistidae lived in shallow marine settings until about 10 Ma, but Platanista now occurs only in freshwaters. Similarly, species of Squalodontidae and Eurhinodelphinidae were widely distributed before their demise in the later Miocene. Judging from the functional complexes seen in the latter fossils, there are no modern equivalents to these groups: some morphotypes and lifestyles have disappeared.
See Also the Following Articles Archaeocetes, Archaic n Basilosaurids and Kekenodontids
References Bajpai, S., and Thewissen, J.G.M. (2014). Protocetid cetaceans (Mammalia) from the Eocene of India. Palaeont. Elec. 17(34A), 1–19. Bianucci, G. (2013). Septidelphis morii, n. gen. et sp., from the Pliocene of Italy: new evidence of the explosive radiation of true dolphins (Odontoceti, Delphinidae). J. Vert. Paleo. 33, 722–740.
185
Boessenecker, R.W., and Poust, A.W. (2015). Freshwater occurrence of the extinct dolphin Parapontoporia (Cetacea: Lipotidae) from the upper Pliocene nonmarine Tulare Formation of California. Palaeontology 58, 489–496. Boyden, A., and Gemeroy, D. (1950). The relative position of the Cetacea among the orders of Mammalia as indicated by precipitin tests. Zoologica 35, 145–151. Buono, M.R., Fernández, M.S., Reguero, M.A., Marenssi, S.A., Santillana, S.N., and Mörs, T. (2016). Eocene basilosaurid whales from the La Meseta Formation, Marambio (Seymour) Island, Antarctica. Ameghiniana 53, 296–315. Churchill, M., Martinez-Caceres, M., de Muizon, C., Mnieckowski, J., and Geisler, J.H. (2016). The origin of high-frequency hearing in whales. Curr. Biol. doi:10.1016/j.cub.2016.06.004. Committee on Taxonomy (2016). List of marine mammal species and subspecies. Society for Marine Mammalogy, www.marinemammalscience.org. Crossman, C.A., Taylor, E.B., and Barrett‐Lennard, L.G. (2016). Hybridization in the Cetacea: widespread occurrence and associated morphological, behavioral, and ecological factors. Ecol. Evol. 6, 1293–1303. Estes, J.A. (1979). Exploitation of marine mammals: r-selection of K-strategists? J. Fish. Res. Bd. Can. 36, 1009–1017. Flower, W.H. (1883). On whales, past and present, and their probable origin. II. Nature 28, 226–230. Harlin-Cognato, A.D. (2010). The Dusky Dolphins’ place in the delphinid family tree. In “Dusky Dolphin: Master Acrobat off Different Shores”, (B. Wursig, and M. Wursig, Eds), pp. 1–20. Academic Press, Amsterdam. Lindberg, D.R., and Pyenson, N.D. (2007). Things that go bump in the night: evolutionary between cephalopods and cetaceans in the Tertiary. Lethaia 40, 335–343. Ludt, W.B., and Rocha, L.A. (2015). Shifting seas: the impacts of Pleistocene sea-level fluctuations on the evolution of tropical marine taxa. J. Biogeog. 42, 25–38. Marx, F.G., and Fordyce, R.E. (2015). Baleen boom and bust: a synthesis of mysticete phylogeny, diversity and disparity. R. Soc. Open Sci. 2. doi:10.1098/rsos.140434. McGowen, M.R., Spaulding, M., and Gatesy, J. (2009). Divergence date estimation and a comprehensive molecular tree of extant cetaceans. Mol. Phylogenet. Evol. 53, 891–906. Pastene, L.A., Goto, M., Kanda, N., Zerbini, A.N., Kerem, D.A.N., Watanabe, K.B.Y., Hasegawa, M., Nielsen, R., Larsen, F., and Palsboll, P.J. (2007). Radiation and speciation of pelagic organisms during periods of global warming: the case of the common minke whale, Balaenoptera acutorostrata. Mol. Ecol. 16, 1481–1495. Pyenson, N.D., and Lindberg, D.R. (2011). What happened to Gray Whales during the Pleistocene? The ecological impact of sea-level change on benthic feeding areas in the North Pacific Ocean. PLoS One 6. doi:10.1371/journal.pone.0021295. Quental, T.B., and Marshall, C.R. (2010). Diversity dynamics: molecular phylogenies need the fossil record. Tr. Ecol. Evol. 25, 434–441. Rice, D.W. (1998). Marine Mammals of the World. Systematics and Distribution. Society for Marine Mammalogy, Lawrence, KS. Rommel, S.A., Costidis, A.M., Fernandez, A., Jepsono, P.D., Pabst, D.A., McLellan, W.A., et al. (2006). Elements of beaked whale anatomy and diving physiology and some hypothetical causes of sonar-related stranding. J. Cet. Res. Manag. 7, 189–209. Thewissen, J.G.M., Cooper, L.N., Clementz, M.T., Bajpai, S., and Tiwari, B.N. (2007). Whales originated from aquatic artiodactyls in the Eocene epoch of India. Nature 450, 1190–1194. Tsai, C.-H., and Fordyce, R.E. (2014). Disparate heterochronic processes in baleen whale evolution. Evol. Biol. doi:10.1007/ s11692-11014-19269-11694. Uhen, M.D. (2010). The origin(s) of whales. Ann. Rev. Earth Planet. Sci. 38, 189–219. Vélez-Juarbe, J., and Pyenson, N.D. (2012). Bohaskaia monodontoides, a new monodontid (Cetacea, Odontoceti, Delphinoidea) from the Pliocene of the western North Atlantic Ocean. J. Vert. Paleo. 32, 476–484.
C