The Role of Locomotory Ancestry on Secondarily Aquatic Transitions.

Land-to-sea evolutionary transitions are great transformations where terrestrial amniote clades returned to aquatic environments. These secondarily aquatic amniote clades include charismatic marine mammal and marine reptile groups, as well as countless semi-aquatic forms that modified their terrestrial locomotor anatomy to varying degrees to be suited for swimming via axial and/or appendicular propulsion. The terrestrial ancestors of secondarily aquatic groups would have started off swimming strikingly differently from one another given their evolutionary histories, as inferred by the way modern terrestrial amniotes swim. With such stark locomotor functional differences between reptiles and mammals, we ask if this impacted these transitions. Axial propulsion appears favored by aquatic descendants of terrestrially sprawling quadrupedal reptiles, with exceptions. Appendicular propulsion is more prevalent across the aquatic descendants of ancestrally parasagittal-postured mammals, particularly early transitioning forms. Ancestral terrestrial anatomical differences that precede secondarily aquatic invasions between mammals and reptiles, as well as the distribution of axial and appendicular swimming in secondarily aquatic clades, may indicate that ancestral terrestrial locomotor anatomy played a role, potentially in both constraint and facilitation, in certain aquatic locomotion styles. This perspective of the land-to-sea transition can lead to new avenues of functional, biomechanical, and developmental study of secondarily aquatic transitions.

New heterodont odontocetes from the Oligocene Pysht Formation in Washington State, U.S.A., and a reevaluation of Simocetidae (Cetacea, Odontoceti).

Odontocetes first appeared in the fossil record by the early Oligocene, and their early evolutionary history can provide clues as to how some of their unique adaptations, such as echolocation, evolved. Here, three new specimens from the early to late Oligocene Pysht Formation are described further increasing our understanding of the richness and diversity of early odontocetes, particularly for the North Pacific. Phylogenetic analysis shows that the new specimens are part of a more inclusive, redefined Simocetidae, which now includes Simocetus rayi, Olympicetus sp. 1, Olympicetus avitus, O. thalassodon sp. nov., and a large unnamed taxon (Simocetidae gen. et sp. A), all part of a North Pacific clade that represents one of the earliest diverging groups of odontocetes. Amongst these, Olympicetus thalassodon sp. nov. represents one of the best known simocetids, offering new information on the cranial and dental morphology of early odontocetes. Furthermore, the inclusion of CCNHM 1000, here considered to represent a neonate of Olympicetus sp., as part of the Simocetidae, suggests that members of this group may not have had the capability of ultrasonic hearing, at least during their early ontogenetic stages. Based on the new specimens, the dentition of simocetids is interpreted as being plesiomorphic, with a tooth count more akin to that of basilosaurids and early toothed mysticetes, while other features of the skull and hyoid suggest various forms of prey acquisition, including raptorial or combined feeding in Olympicetus spp., and suction feeding in Simocetus. Finally, body size estimates show that small to moderately large taxa are present in Simocetidae, with the largest taxon represented by Simocetidae gen. et sp. A with an estimated body length of 3 m, which places it as the largest known simocetid, and amongst the largest Oligocene odontocetes. The new specimens described here add to a growing list of Oligocene marine tetrapods from the North Pacific, further promoting faunistic comparisons across other contemporaneous and younger assemblages, that will allow for an improved understanding of the evolution of marine faunas in the region.

Bridging two oceans: small toothed cetaceans (Odontoceti) from the Late Miocene Chagres Formation, eastern Caribbean (Colon, Panama).

Fossil cetaceans are often found in Miocene marine outcrops across the globe. However, because this record is not homogeneous, the dissimilar increase in occurrences, along with the sampling bias has created regions with extensive records and others with great scarcity. Among these, the Caribbean has remained enigmatic due to the lack of well-preserved cetacean fossils. Here, we report new Caribbean fossil cetaceans from the Upper Miocene Chagres Formation exposed along Piña beach, Eastern Panama, including a scaphokogiine kogiid, an Acrophyseter-like physeteroid and the phocoenid Piscolithax. Along with previous records of the iniid Isthminia panamensis and the kogiine Nanokogia isthmia, the Chagres cetacean fauna shows some similarities with other Late Miocene cetacean communities such as the Californias in the North Pacific, although their closest affinities lie with the eastern South Pacific Pisco Formation, Peru. Such findings indicate that though deep and intermediate Caribbean-Pacific water interchange was reduced by the Middle Miocene due to the shallowing of the Central American Seaway, shallow waters marine connection that persisted until the Pliocene might have facilitated the dispersal of coastal species across both sides of the Isthmus.

Sperm whales (Physeteroidea) from the Pisco Formation, Peru, and their trophic role as fat sources for late Miocene sharks.

Shark-cetacean trophic interactions, preserved as bite marks in the fossil record, mostly correspond to isolated or fragmentary findings that bear limited information about major trophic patterns or roles. Here, we provide evidence of focalized foraging by sharks in the form of tooth bite marks over physeteroids fossil bones from the late Miocene of Peru. These findings indicate that sharks were targeting the forehead of coeval physeteroids to actively feed on their lipid-rich nasal complexes. Miocene physeteroids displayed a broad diversity, including giant predatorial forms, small benthic foragers and suction feeders. Like their extant relatives, these animals exhibited enlarged fatty forehead organs responsible for their sound production capabilities, thus evolving taxon-specific cranial architecture. Bite marks are found on the cranial bones where these structures were attached, indicating that sharks actively targeted this region; but also, in areas that would only be accessible following the consumption of the surrounding soft tissues. The shape of the bite marks and their distribution suggests a series of consecutive scavenging events by individuals of different shark species. Similar bite patterns can be recognized on other Miocene physeteroids fossils from across the globe, suggesting that sharks actively exploited physeteroid carcasses as fat sources.

The earliest record of Caribbean frogs: a fossil coquí from Puerto Rico.

The nearly 200 species of direct-developing frogs in the genus Eleutherodactylus (the Caribbean landfrogs, which include the coquís) comprise an important lineage for understanding the evolution and historical biogeography of the Caribbean. Time-calibrated molecular phylogenies provide indirect evidence for the processes that shaped the modern anuran fauna, but there is little direct evidence from the fossil record of Caribbean frogs about their distributions in the past. We report a distal humerus of a frog from the Oligocene (approx. 29 Ma) of Puerto Rico that represents the earliest known fossil frog from any Caribbean island. Based on its prominent rounded distal humeral head, distally projecting entepicondyle, and reduced ectepicondyle, we refer it to the genus Eleutherodactylus. This fossil provides additional support for an early arrival of some groups of terrestrial vertebrates to the Greater Antilles and corroborates previous estimates based on molecular phylogenies suggesting that this diverse Caribbean lineage was present in the islands by the mid-Cenozoic.

Early Oligocene chinchilloid caviomorphs from Puerto Rico and the initial rodent colonization of the West Indies.

By their past and present diversity, rodents are among the richest components of Caribbean land mammals. Many of these became extinct recently. Causes of their extirpation, their phylogenetic affinities, the timing of their arrival in the West Indies and their biogeographic history are all ongoing debated issues. Here, we report the discovery of dental remains from Lower Oligocene deposits (ca 29.5 Ma) of Puerto Rico. Their morphology attests to the presence of two distinct species of chinchilloid caviomorphs, closely related to dinomyids in a phylogenetic analysis, and thus of undisputable South American origin. These fossils represent the earliest Caribbean rodents known thus far. They could extend back to 30 Ma the lineages of some recently extinct Caribbean giant rodents (Elasmodontomys and Amblyrhiza), which are also retrieved here as chinchilloids. This new find has substantial biogeographic implications because it demonstrates an early dispersal of land mammals from South America to the West Indies, perhaps via the emergence of the Aves Ridge that occurred ca 35-33 Ma (GAARlandia hypothesis). Considering both this new palaeontological evidence and recent molecular divergence estimates, the natural colonization of the West Indies by rodents probably occurred through multiple and time-staggered dispersal events (chinchilloids, then echimyid octodontoids (spiny rats/hutias), caviids and lastly oryzomyin muroids (rice rats)).

Oldest record of monk seals from the North Pacific and biogeographic implications.

True seals (crown Phocidae) originated during the late Oligocene-early Miocene (approx. 27-20 Ma) in the North Atlantic/Mediterranean region, with later (middle Miocene, approx. 16-11 Ma) dispersal events to the South Atlantic and South Pacific. Contrasting with other pinnipeds, the fossil record of phocids from the North Pacific region is scarce and restricted to the Pleistocene. Here we present the oldest fossil record of crown phocids, monachines (monk seals), from the North Pacific region. The specimens were collected from the upper Monterey Formation in Southern California and are dated to 8.5-7.1 Ma, predating the previously oldest known record by at least 7 Ma. This record provides new insights into the early biogeographic history of phocids in the North Pacific and is consistent with a northward dispersal of monk seals (monachines), which has been recognized for other groups of marine mammals. Alternatively, this finding may correspond with a westward dispersal through the Central American Seaway of some ancestor of the Hawaiian monk seal. This record increases the taxonomic richness of the Monterey pinniped assemblage to five taxa, making it a fairly diverse fossil assemblage, but also constitutes the oldest record of sympatry among all three extant pinniped crown clades.

A new tuskless walrus from the Miocene of Orange County, California, with comments on the diversity and taxonomy of odobenids.

We describe Titanotaria orangensis (gen. et. sp. nov.), a new species of walrus (odobenid) from the upper Miocene Oso Member of the Capistrano Formation of Orange County, California. This species is important because: (1) It is one of the best-known and latest-surviving tuskless walruses; (2) It raises the number of reported odobenid taxa from the Oso Member to four species making it one of the richest walrus assemblages known (along with the basal Purisima of Northern California); (3) It is just the second record of a tuskless walrus from the same unit as a tusked taxon. Our phylogenetic analysis places T. orangensis as sister to a clade that includes Imagotaria downsi, Pontolis magnus, Dusignathus spp., Gomphotaria pugnax, and Odobeninae. We propose new branch-based phylogenetic definitions for Odobenidae, Odobeninae, and a new node-based name (Neodobenia) for the clade that includes Dusignathus spp., G. pugnax, and Odobeninae. A richness analysis at the 0.1 Ma level that incorporates stratigraphic uncertainty and ghost lineages demonstrates maximum peaks of richness (up to eight or nine coeval lineages) near the base of Odobenidae, Neodobenia, and Odobenini. A more conservative minimum curve demonstrates that standing richness may have been much lower than the maximum lineage richness estimates that are biased by stratigraphic uncertainty. Overall the odobenid fossil record is uneven, with large time slices of the record missing on either side of the Pacific Ocean at some times and biases from the preserved depositional environments at other times. We recognize a provisional timescale for the transition of East Pacific odobenid assemblages that include "basal odobenids" (stem neodobenians) from the Empire and older formations (>7 Ma), to a mixture of basal odobenids and neodobenians from the Capistrano and basal Purisima (7-5 Ma), and then just neodobenians from all younger units (<5 Ma). The large amount of undescribed material will add new taxa and range extensions for existing taxa, which will likely change some of the patterns we describe.

A dwarf walrus from the Miocene of Baja California Sur, Mexico.

Here, we describe the odobenid Nanodobenus arandai gen. et sp. nov., based on a nearly complete left mandible from the mid to late Miocene Tortugas Formation in Baja California Sur. Nanodobenus is distinguished among odobenids by displaying a unique combination of plesiomorphic and derived characters, such as narrow mandibular symphysis, well-developed genial tuberosity, bilobed canine and p2 roots, bulbous post-canine teeth with the paraconid, protoconid and hypoconid, and smooth lingual cingula. Moreover, it is characterized by its small adult body length, which is estimated at about 1.65 m. Throughout the Miocene-Pliocene odobenids are characterized by an increase in body size, especially after the extinction of desmatophocids in the late Miocene. The small size of Nanodobenus departs from this trend, demonstrating that there was greater size disparity among odobenids in the mid-late Miocene than previously thought. It is hypothesized that Nanodobenus occupied a niche that was later on occupied by similar-sized otariids, such as Thalassoleon mexicanus, which occurs sympatrically with large odobenids in the overlying Almejas Formation.

Eotaria citrica, sp. nov., a new stem otariid from the "Topanga" formation of Southern California.

A new taxon of stem otariid, Eotaria citrica sp. nov., is described from the upper Burdigalian to lower Langhian "Topanga" formation of Orange County, California. The new species is described from mandibular and dental remains that show a unique combination of plesiomorphic and derived characters. Specifically, it is characterized by having trenchant and prominent paraconid cusps in p3-m1, lingual cingula of p2-4 with faint crenulations, premolars and molars with vestigial metaconid, bilobed root of m2 and a genial tuberosity located under p3. Furthermore, additional material of the contemporaneous Eotaria crypta is described, providing new information on the morphology of this taxon. Both species of Eotaria represent the earliest stem otariids, reinforcing the hypothesis that the group originated in the north Eastern Pacific Region. At present, the "Topanga" Fm. pinniped fauna includes Eotaria citrica, Eotaria crypta, the desmatophocid Allodesmus sp., the odobenids Neotherium sp., Pelagiarctos sp. and includes the oldest records of crown pinnipeds in California. Overall this pinniped fauna is similar to the nearly contemporaneous Sharktooth Hill bonebed. However, unambiguous records of Eotaria are still missing from Sharktooth Hill. This absence may be due to taphonomic or paleoenvironmental factors. The new "Topanga" record presented here was integrated into an overview of the late Oligocene through early Pleistocene pinniped faunas of Southern California. The results show an overall increase in body size over time until the Pleistocene. Furthermore, desmatophocids were the largest pinnipeds during the middle Miocene, but were extinct by the beginning of the late Miocene. Odobenids diversified and became the dominant pinnipeds in late Miocene through Pleistocene assemblages, usually approaching or exceeding 3 m in body length, while otariids remained as the smallest taxa. This pattern contrasts with modern assemblages, in which the phocid Mirounga angustirostris is the largest pinniped taxon in the region, odobenids are extinct and medium and small size ranges are occupied by otariids or other phocids.

Isthminia panamensis, a new fossil inioid (Mammalia, Cetacea) from the Chagres Formation of Panama and the evolution of 'river dolphins' in the Americas.

In contrast to dominant mode of ecological transition in the evolution of marine mammals, different lineages of toothed whales (Odontoceti) have repeatedly invaded freshwater ecosystems during the Cenozoic era. The so-called 'river dolphins' are now recognized as independent lineages that converged on similar morphological specializations (e.g., longirostry). In South America, the two endemic 'river dolphin' lineages form a clade (Inioidea), with closely related fossil inioids from marine rock units in the South Pacific and North Atlantic oceans. Here we describe a new genus and species of fossil inioid, Isthminia panamensis, gen. et sp. nov. from the late Miocene of Panama. The type and only known specimen consists of a partial skull, mandibles, isolated teeth, a right scapula, and carpal elements recovered from the Piña Facies of the Chagres Formation, along the Caribbean coast of Panama. Sedimentological and associated fauna from the Piña Facies point to fully marine conditions with high planktonic productivity about 6.1-5.8 million years ago (Messinian), pre-dating the final closure of the Isthmus of Panama. Along with ecomorphological data, we propose that Isthminia was primarily a marine inhabitant, similar to modern oceanic delphinoids. Phylogenetic analysis of fossil and living inioids, including new codings for Ischyrorhynchus, an enigmatic taxon from the late Miocene of Argentina, places Isthminia as the sister taxon to Inia, in a broader clade that includes Ischyrorhynchus and Meherrinia, a North American fossil inioid. This phylogenetic hypothesis complicates the possible scenarios for the freshwater invasion of the Amazon River system by stem relatives of Inia, but it remains consistent with a broader marine ancestry for Inioidea. Based on the fossil record of this group, along with Isthminia, we propose that a marine ancestor of Inia invaded Amazonia during late Miocene eustatic sea-level highs.

Interordinal gene capture, the phylogenetic position of Steller's sea cow based on molecular and morphological data, and the macroevolutionary history of Sirenia.

The recently extinct (ca. 1768) Steller's sea cow (Hydrodamalis gigas) was a large, edentulous North Pacific sirenian. The phylogenetic affinities of this taxon to other members of this clade, living and extinct, are uncertain based on previous morphological and molecular studies. We employed hybridization capture methods and second generation sequencing technology to obtain >30kb of exon sequences from 26 nuclear genes for both H. gigas and Dugong dugon. We also obtained complete coding sequences for the tooth-related enamelin (ENAM) gene. Hybridization probes designed using dugong and manatee sequences were both highly effective in retrieving sequences from H. gigas (mean=98.8% coverage), as were more divergent probes for regions of ENAM (99.0% coverage) that were designed exclusively from a proboscidean (African elephant) and a hyracoid (Cape hyrax). New sequences were combined with available sequences for representatives of all other afrotherian orders. We also expanded a previously published morphological matrix for living and fossil Sirenia by adding both new taxa and nine new postcranial characters. Maximum likelihood and parsimony analyses of the molecular data provide robust support for an association of H. gigas and D. dugon to the exclusion of living trichechids (manatees). Parsimony analyses of the morphological data also support the inclusion of H. gigas in Dugongidae with D. dugon and fossil dugongids. Timetree analyses based on calibration density approaches with hard- and soft-bounded constraints suggest that H. gigas and D. dugon diverged in the Oligocene and that crown sirenians last shared a common ancestor in the Eocene. The coding sequence for the ENAM gene in H. gigas does not contain frameshift mutations or stop codons, but there is a transversion mutation (AG to CG) in the acceptor splice site of intron 2. This disruption in the edentulous Steller's sea cow is consistent with previous studies that have documented inactivating mutations in tooth-specific loci of a variety of edentulous and enamelless vertebrates including birds, turtles, aardvarks, pangolins, xenarthrans, and baleen whales. Further, branch-site dN/dS analyses provide evidence for positive selection in ENAM on the stem dugongid branch where extensive tooth reduction occurred, followed by neutral evolution on the Hydrodamalis branch. Finally, we present a synthetic evolutionary tree for living and fossil sirenians showing several key innovations in the history of this clade including character state changes that parallel those that occurred in the evolutionary history of cetaceans.

Evolutionary Patterns among Living and Fossil Kogiid Sperm Whales: Evidence from the Neogene of Central America.

Kogiids are known by two living species, the pygmy and dwarf sperm whale (Kogia breviceps and K. sima). Both are relatively rare, and as their names suggest, they are closely related to the sperm whale, all being characterized by the presence of a spermaceti organ. However, this organ is much reduced in kogiids and may have become functionally different. Here we describe a fossil kogiid from the late Miocene of Panama and we explore the evolutionary history of the group with special attention to this evolutionary reduction. The fossil consists of cranial material from the late Tortonian (~7.5 Ma) Piña facies of the Chagres Formation in Panama. Detailed comparison with other fossil and extant kogiids and the results of a phylogenetic analysis place the Panamanian kogiid, herein named Nanokogia isthmia gen. et sp. nov., as a taxon most closely related to Praekogia cedrosensis from the Messinian (~6 Ma) of Baja California and to Kogia spp. Furthermore our results show that reduction of the spermaceti organ has occurred iteratively in kogiids, once in Thalassocetus antwerpiensis in the early-middle Miocene, and more recently in Kogia spp. Additionally, we estimate the divergence between extant species of Kogia at around the late Pliocene, later than previously predicted by molecular estimates. Finally, comparison of Nanokogia with the coeval Scaphokogia cochlearis from Peru shows that these two species display a greater morphological disparity between them than that observed between the extant members of the group. We hypothesize that this reflects differences in feeding ecologies of the two species, with Nanokogia being more similar to extant Kogia. Nanokogia shows that kogiids have been part of the Neotropical marine mammal communities at least since the late Miocene, and gives us insight into the evolutionary history and origins of one of the rarest groups of living whales.

Repeated mass strandings of Miocene marine mammals from Atacama Region of Chile point to sudden death at sea.

Marine mammal mass strandings have occurred for millions of years, but their origins defy singular explanations. Beyond human causes, mass strandings have been attributed to herding behaviour, large-scale oceanographic fronts and harmful algal blooms (HABs). Because algal toxins cause organ failure in marine mammals, HABs are the most common mass stranding agent with broad geographical and widespread taxonomic impact. Toxin-mediated mortalities in marine food webs have the potential to occur over geological timescales, but direct evidence for their antiquity has been lacking. Here, we describe an unusually dense accumulation of fossil marine vertebrates from Cerro Ballena, a Late Miocene locality in Atacama Region of Chile, preserving over 40 skeletons of rorqual whales, sperm whales, seals, aquatic sloths, walrus-whales and predatory bony fish. Marine mammal skeletons are distributed in four discrete horizons at the site, representing a recurring accumulation mechanism. Taphonomic analysis points to strong spatial focusing with a rapid death mechanism at sea, before being buried on a barrier-protected supratidal flat. In modern settings, HABs are the only known natural cause for such repeated, multispecies accumulations. This proposed agent suggests that upwelling zones elsewhere in the world should preserve fossil marine vertebrate accumulations in similar modes and densities.

Iterative evolution of sympatric seacow (Dugongidae, Sirenia) assemblages during the past ~26 million years.

Extant sirenians show allopatric distributions throughout most of their range. However, their fossil record shows evidence of multispecies communities throughout most of the past ∼26 million years, in different oceanic basins. Morphological differences among co-occurring sirenian taxa suggest that resource partitioning played a role in structuring these communities. We examined body size and ecomorphological differences (e.g., rostral deflection and tusk morphology) among sirenian assemblages from the late Oligocene of Florida, early Miocene of India and early Pliocene of Mexico; each with three species of the family Dugongidae. Although overlapping in several ecomorphological traits, each assemblage showed at least one dominant trait in which coexisting species differed. Fossil sirenian occurrences occasionally are monotypic, but the assemblages analyzed herein show iterative evolution of multispecies communities, a phenomenon unparalleled in extant sirenian ecology. As primary consumers of seagrasses, these communities likely had a strong impact on past seagrass ecology and diversity, although the sparse fossil record of seagrasses limits direct comparisons. Nonetheless, our results provide robust support for previous suggestions that some sirenians in these extinct assemblages served as keystone species, controlling the dominance of climax seagrass species, permitting more taxonomically diverse seagrass beds (and sirenian communities) than many of those observed today.

A gharial from the Oligocene of Puerto Rico: transoceanic dispersal in the history of a non-marine reptile.

The Indian gharial (Gavialis gangeticus) is not found in saltwater, but the geographical distribution of fossil relatives suggests a derivation from ancestors that lived in, or were at least able to withstand, saline conditions. Here, we describe a new Oligocene gharial, Aktiogavialis puertoricensis, from deltaic-coastal deposits of northern Puerto Rico. It is related to a clade of Neogene gharials otherwise restricted to South America. Its geological and geographical settings, along with its phylogenetic relationships, are consistent with two scenarios: (i) that a single trans-Atlantic dispersal event during the Tertiary explains the South American Neogene gharial assemblage and (ii) that stem gharials were coastal animals and their current restriction to freshwater settings is a comparatively recent environmental shift for the group. This discovery highlights the importance of including fossil information in a phylogenetic context when assessing the ecological history of modern organisms.