PalZ (2017) 91:601–627 DOI 10.1007/s12542-017-0362-8 RESEARCH PAPER Astragali of Pakicetidae and other early-to-middle Eocene archaeocetes (Mammalia, Cetacea) of Pakistan: locomotion and habitat in the initial stages of whale evolution 1 2 3 4 Philip D. Gingerich • Kurt Heissig • Ryan M. Bebej • Wighart von Koenigswald Received: 6 December 2016 / Accepted: 26 May 2017 / Published online: 28 June 2017 Ó Pala¨ontologische Gesellschaft 2017 Abstract Richard Dehm and colleagues of the Bayerische archaeocete taxa based on teeth. Multivariate morphomet- Staatssammlung fu¨r Pala¨ontologie und Geologie in Munich ric comparison (Auto3Dgm) shows that pakicetid astragali made an important collection of early-to-middle Eocene overlap almost completely in shape with those of early mammals at Ganda Kas in Pakistan during the winter of artiodactyls. Middle Eocene protocetid astragali are 1955/56. The genera and species Ichthyolestes pinfoldi and divergent from both. Retention of an astragalus indistin- Gandakasia potens were named from this collection. Both guishable from that of artiodactyls shows that pakicetids are now recognized as early and primitive archaeocete are closely related to artiodactyls phylogenetically, but cetaceans. In addition, Dehm’s group collected 16 com- does not make Ichthyolestes and Pakicetus terrestrial or plete or partial astragali of archaeocetes that were cursorial. Other skeletal elements and bone microstructure misidentified as artiodactyls. These bring the total number indicate that pakicetids were semiaquatic like later proto- of archaeocete astragali known from Ganda Kas to 28. cetids. Tropical riverine and marginal marine facies of the They separate clearly into four species distinguished by Kuldana Formation are likely habitats for initial stages of size: from smallest to largest Ichthyolestes pinfoldi Dehm the transition from terrestrial artiodactyls to semiaquatic and Oettingen-Spielberg, Pakicetus attocki (West), Gan- and fully aquatic archaeocetes. dakasia potens Dehm and Oettingen-Spielberg, and Am- bulocetus natans Thewissen et al. Ganda Kas artiodactyls Keywords Eocene Á Artiodactyla Á Cetacea Á Astragalus Á are smaller and rare in comparison. Ichthyolestes and Pa- Semiaquatic locomotion Á Transition from land to sea kicetus are pakicetid archaeocetes, Gandakasia is presently indeterminate to family, and Ambulocetus is an ambulo- Kurzfassung Richard Dehm machte mit Kollegen der cetid. Tooth size and astragalus size are highly correlated, Bayerischen Staatsammlung fu¨r Pala¨ontologie und corroborating reference of astragali to the first three Geologie Mu¨nchen im Winter 1955/56 bedeutende Aufsammlungen von Wirbeltierfossilien aus dem Handling editor: Thomas Mo¨rs. Unter- bis Mittel-Eoza¨n von Ganda Kas in Pakistan. Die Gattungen und Arten Ichthyolestes pinfordi und & Philip D. Gingerich Gandakasia potens beruhen u. a. auf diesem Material. [email protected] Beide werden jetzt als fru¨he und primitive Archaeoceten angesehen. Die Dehm-Gruppe sammelte daru¨ber hinaus 16 1 Museum of Paleontology, University of Michigan, 1109 Geddes Avenue, Ann Arbor, MI 48109-1079, USA vollsta¨ndige Astragali von Archaeoceten, die seinerzeit den Paarhufern zugeordnet wurden. Somit bela¨uft sich jetzt die 2 Bayerische Staatssammlung fu¨r Pala¨ontologie und Geologie, Richard-Wagner-Straße 10, 80333 Munich, Germany Zahl der Astragali von Archaeoceten von Ganda Kas auf 28. Diese lassen sich aufgrund ihrer Gro¨ße den 3 Department of Biology, Calvin College, 1726 Knollcrest Circle SE, Grand Rapids, MI 49546-4403, USA nachfolgenden vier Arten (in aufsteigender Gro¨ße) zuordnen: Ichthyolestes pinfoldi Dehm und 4 Steinmann-Institut fu¨r Geologie, Mineralogie und Pala¨ontologie, Rheinische Friedrich-Wilhelms-Universita¨t Oettingen-Spielberg, Pakicetus attocki (West), Gandakasia Bonn, Nussallee 8, 53115 Bonn, Germany potens Dehm und Oettingen-Spielberg sowie Ambulocetus 123 602 P. D. Gingerich et al. natans Thewissen et al. Die Artiodactyla aus Ganda Kas astragalus with a deep proximal pulley or trochlea and a sind im Vergleich dazu kleiner und seltener. Die shallower distal trochlea (see below). These diagnostic Archaeoceten Ichthyolestes und Pakicetus sind features are also present in the astragalus of early Pakicetidae, Gandakasia kann zurzeit noch keiner Familie archaeocetes. The deep proximal and distal trochleae and zugeordnet werden; Ambulocetus repra¨sentiert die the parallel medial and lateral tori of the former permit Ambulocetidae. Da die Gro¨ße der Za¨hne und die der dorsoventral flexion of the astragalus and foot relative to Astragali sehr gut korrelieren, besta¨tigt sich die Zuordnung the tibia and lower leg, but preclude mediolateral rotation der Astragali zu den ersten drei Taxa, die aufgrund der and pivoting that would be detrimental in the cursorial Za¨hne unterschieden wurden. Ein multivariater locomotion of artiodactyls (Schaeffer 1947). morphometrischer Vergleich (Auto3Dgm) zeigt, dass sich Whales were long thought to have evolved from general- die Astragali der Pakicetidae in der Gestalt fast vollsta¨ndig ized Paleocene-epoch mesonychian condylarths (Van Valen mit denen der fru¨hen Artiodactyla decken. Die Astragali 1966, 1968). However, discovery of skeletons of the early der mitteleoza¨nen Protocetidae unterscheiden sich aber von whales Artiocetus and Rodhocetus with associated artiodactyl beiden. Die Beibehaltung eines Astragalus, der von dem astragali showed that whales evolved from Eocene Artio- der Artiodactyla nicht unterscheidbar ist, zeigt dass die dactyla and not from Mesonychia (Gingerich et al. 2001b). Pakicetiden mit den Artiodactylen in einem engen This corroborated molecular evidence that Cetacea are phy- phylogenetischen Bezug stehen. Daraus folgt aber nicht, logenetically nested within Artiodactyla in a clade sometimes dass Ichthyolestes und Pakicetus terrestrisch lebten und called Cetartiodactyla (Montgelard et al. 1997). vorwiegend La¨ufer waren. Andere Skelettelemente und die We regard the traditional mammalian orders Cetacea Mikrostruktur der Knochen zeigen, dass diese Pakicetiden and Artiodactyla as distinct taxa of equal rank to ebenso semiaquatisch waren, wie die ju¨ngeren acknowledge that one major group of mammals united by Protocetidae. Die Fazies tropischer Flussmu¨ndungen und similarity (Cetacea) can, and did, evolve from another such die randlichen marinen Bereiche, die in der group (Artiodactyla). Systematists emphasizing holophyly Kuldana-Formation belegt sind, bilden den Lebensraum fu¨r in classification over monophyly in evolution are free to einen beginnenden U¨ bergang von terrestrischen group Cetacea with Non-Cetacean-Artiodactyla in an order Artiodactylen u¨ber semiaquatische Formen zu den voll Artiodactya, or Cetacea with Non-Cetacean-Cetartio- aquatischen Archaeoceten. dactyla in an order Cetartiodactyla. In this case our use of ‘Artiodactyla’ (and informal ‘artiodactyl’) can be regarded Schlu¨sselwo¨rter Eoza¨n Á Artiodactyla Á Cetacea Á as a shorthand equivalent of ‘Non-Cetacean-Artiodactyla’ Astragalus Á semiaquatische Fortbewegung Á U¨ bergang or ‘Non-Cetacean-Cetartiodactyla.’ vom Land zum Meer Study of locomotion in the initial stages of whale evo- lution is timely for comparing two contrasting narratives: (1) the early-to-middle Eocene archaeocetes Ichthyolestes Introduction and Pakicetus (Pakicetidae) were cursorial and terrestrial like their artiodactyl ancestors—implying that aquatic Whales are marine mammals that evolved from land-mam- adaptation originated after the origin of Cetacea (Thewis- mal ancestors in one of the major evolutionary transitions sen et al. 2001b; Fish 2016); or (2) early-to-middle Eocene documented in the fossil record. This transition affected the Ichthyolestes and Pakicetus were already semiaquatic, and form and function of many anatomical and physiological cetaceans originated from an unknown early Eocene ter- systems. The locomotor complex is one of the transitioning restrial or semiaquatic artiodactyl similar to Elomeryx systems most accessible for study in the fossil record. Here, (Gingerich et al. 2001b; Gingerich 2003a, 2005)orIndo- we focus on the form and function of a key skeletal element, hyus (Thewissen et al. 2007; Cooper et al. 2011)—imply- the astragalus, during the initial stages of whale evolution. ing that aquatic adaptation took place before or during the The astragalus is the bone in each mammalian ankle, left and origin of Cetacea. right, that forms an articular surface permitting flexion and extension of the foot relative to the lower leg. Astragali are present in archaic whales (Archaeoceti) that retained feet, History of study but astragali are no longer present in living toothed whales (Odontoceti) and baleen whales (Mysticeti) that lack exter- This study started, in some sense, when Arthur Wynne nal hind limbs and feet. (1877) first reported fragmentary Eocene mammals from The astragalus in mammals is often distinctly shaped sites near Fatehjang in the Kala Chitta Range of Punjab. and diagnostic of taxonomic orders. For example, Artio- This region is now part of Pakistan, and the bones came dactyla (cows, sheep, deer, etc.) have a ‘double-pulley’ from strata variously referred to as the Kuldana series 123 Astragali of Pakicetidae and other Eocene archaeocetes of Pakistan 603 (Wynne 1874; Middlemiss 1896), upper nummulitic group the group was able to make a substantial collection of (Wynne 1877), ‘nummulitics’ (Lydekker 1880), lower middle Eocene specimens. The mammalian dental remains Chharat series (Pinfold