Evolution of the brain of Plio/Pleistocene wolves Evolution of the brain of Plio/Pleistocene wolves George Lyras Alexandra van der Geer Michael Dermitzakis Summary Caninae be divided three the the foxes and the SouthAmerican The living subfamily can roughly into groups: dogs, canids, which started to diverge somewherein the Miocene.Here theevolution ofthe dogs is dealtwith, starting with the which in North America the Middle and the Old World. genus Eucyon, originated during Miocene, spread over During the Pleistocene, the dogs were abundant in Eurasia, with as most well-knownrepresentative the Etruscan Canis and the Late Pleistocene the Canis The evolution of the is wolf, etruscus, later, during gray wolf, lupus. dogs thebasis oftheevolutionoftheir cerebrum. The of and folds the make followedon specific patterns grooves on cortex the inner side of the neurocranium. of this inner this is revealed. The an impression on By making a cast side, pattern authors madesuch casts (endocasts) of all living dogs and red foxes, plus a number of fossil species and compared them It that foxes ofthe have short and a of mutually. appears Vulpes-lineage a prorean gyrus, penthagon-like pattern the have broad and grooves on sensory-motor region. Dogs (Canis, Cuon, Lycaon ) a long, bilaterally compressed and of the the to be rather prorean gyrus, an orthogonal pattern grooves on sensory-motor region. Eucyon appears differ close to the Vulpes-pattern, whereas Canis lepophagus is very similarto living Canis. Vulpes stenognathus doesn’t significantly from the living Vulpes. Samenvatting onderfamilie kan verdeeld drie de de de De huidige Cartinae grofweg worden in groepen: honden, vossen en Zuid-Amerikaanse diezich elkaar scheiden in het Mioceen. Hier wordt deevolutie hondachtigen, van ergens ver weg het Midden Noord Amerika het zich van de honden besproken, die in Mioceen in begon met geslacht Eucyon, en de wereld. In het Pleistoceen de in als daarna verspreidde over oude waren hondachtigen talrijk Eurazië, met Etruskische wolf het Pleistoceen de bekendste vertegenwoordiger de Canis etruscus, en in Laat grijze wolf, Canis evolutie de honden wordt de hand de evolutie hun hersenen. lupus. De van gevolgd aan van van grote De specifieke de de binnenkant de hersenschedel. Door patronen van groevenen windingen op cortex geveneen afdruk aan van die dat hebben een afgietsel van hersenschedel te maken, wordt patroon zichtbaar. De auteurs zulke afgietsels gemaakt van alle nu voorkomende wilde honden en vossen, plus van een aantal fossiele soorten en onderling het korte vergeleken. De vossen van geslacht Vulpes blijken een prorean winding te hebben, en een de de sensorische De honden penthagon-vormig patroon van groeven op motorcortex. (Canis, Cuon, Lycaon) hebben daarentegen een lange en samengeknepen proreanwinding, en een orthogonaal patroon (als twee gebogen de sensorische is dicht het de Canis haakjes) op motorcortex. Eucyon nog bij Vulpes-patroon, maar laat-pliocene al af de lepophagus is echt Canis-achtig. De miocene Vulpes stenognathus wijkt niet significant van huidige soorten van het geslacht Vulpes. Introduction whereas the same cannotbe said for the evolution of their brain cortex. Muscles leave scars on the Members of the canid subfamily Caninae are bones, from which their and foundall the andradiated into shape development over world, many can be inferred. The same is true for the brain, genera and species (fig. 1). Today, all living which leaves traces on the interior side of the canids are classified in this subfamily. The other neurocranium. This fact makes the study of the two subfamilies are the Hesperocyoninae and the brain of fossil species possible, and thus the study Borophaginae (Tedford, 1978), both extinct. It is of the evolutionof this also this subfamily that entered the Old World, in organ. the others. contrast to two They appeared quite Radinsky (1973) reviewed the evolution of the successfull. One of our most common domestic canid brain as known sofarby that time, based on animals, the to this And the dog, belongs group. endocasts. Endocasts are casts, usually of latex or enemies of other domestic two most common our made of the interior of whatever gypsum, struc- animals and chickens), also to this (cattle belong ture. They can be artificial, man made, or natural, same wolves and foxes. group: caused by fossilization of infillings. The impres- sions of the inner surface of the structure are It is therefore surprising that the evolution of copied (in negative) on theendocast. In the case of features such as dentition and skull characters the neurocranium, the endocasts reveal the has been extensively studied for the Canininae, 30 CRANIUM, 18, 2 - 2001 Apart from Radinsky's work little has been CAWINAE published on brain morphology of fossil Caninae. Vulpini Canini I II Descriptions of endocasts of the cerebrum of fossil species are knownonly for the raccoon dog sinensis” in Tedford HESPEROCYONINAE BOROPHAGINAE ”Nyctereutes (Nyctereutes sp. Leptocyon Vulpes Otocyon Urocyon ”Pseudalopex” Pseudalopex Dusicyon Lycalopex Chrysocyon Cerdocyon Nyctereutes Atelocynus Speothos Canis Cuon Lycaon & Qiu, 1991, and N. procyonoides in Soria & Aguirre, 1976) from the Pleistocene of Choukoutien (Pei, 1934), for a «Canis» sp. and from the Pliocene Nyctereutes sp. Late (Czyzewska, 1981), for a Canis dirus (Moodie, 1922), and of an arctic fox from the Late Pleisto- cene (Vanura, 1943). From the scarce studies available, one thing There be immediately arises. appears to an amazing uniformity of the pattern of folds and the them the brain all grooves separating on large living Caninae. This uniformity can be extended into most of the extinct species, and is probably due to the fact that the adaptive radiation of the Fig 1 Cladogram of the family Canidae showing the Caninae started in a some- of the within the not too remote phylogenetic relationships genera past, where the Middle Late Miocene. subfamily Caninae. Redrawn from Tedford, Taylor during to Small, differences & Wang (1995) crucial are, however, distinguishable, and on the basis of these differences, the evolu- van de familieCanidaewaaruit de ver- Cladogram tion of the Canine brain can be followed along the wantschap blijkt tussen de verschillende geslachten phylogenetic path. We focus on the wolf lineage van de onderfamilie Caninae. De onderfamilies Hes- of North America, Eurasia and Africa, and omit perocyoninae en Borophaginae zijn uitgestorven, the South American canids (several zorro's, evenals het geslacht Leptocyon. Onder de vossen maned wolf, bush dog). The South American (Vulpini) vallen de rode vos, de grootoorvos en de canids started to radiate during the Late Pliocene grijze vos. De honden (Canini) vallen uiteen in twee with and Protocyon, and are endemic hoofdgroepen. Aan de rechterkant: Canis, de dhole Pseudalopex to the subcontinent, andare not foundelsewhere. (Indische rode hond) en de hyenahond. Aan de lin- rechts: Zuid Endemic known to radiate kerkant, van links naar de vijf Ameri- species are far beyond kaanse zorro’s en manenwolf, de wasbeerhond, de the extent seen on the mainland (De Vos & Van kortoorvos en de boshond. Gebaseerd Tedford, op der Geer, in press), so South American canids & Taylor Wang (1995). quite probable do not follow the same evolutio- mainland relatives. nary pattern as For similar reasons we omit Cynotherium sardous, the pleisto- caused the folds and of impressions by grooves cene Sardinian dhole, which is endemic to Sardi- the brain cortex during the animal's life. In this nia-Corsica. is the cortical way, it possible to study landscape of a specimen of which no brain is available. Espe- for fossil cially specimens this is the only way to Materials and methods study the external morphology of the brain. The neurocraniumis used as a mouldto make a cast of The endocasts that are used in this study are the lost brain. In fact, the external morphology made according to the technique described by and the of thebrain size are more acccurately seen Radinsky (1968). He developed a non-destructive on endocast than on fresh brains. This is because of endocasts with technique producing the use of the brain changes its shape once it is freed from its latex. A thin (1-2 mm) layer of latex is applied hard bone shell 1948). Natural endo- (Edinger, inside thebraincase in successive layers. Since the casts arise when the neurocranium is filled with latex elastic be is very it can pulled out through hard matrix fossilisation, after which the during the and it is out of the foramen magnum, once bone itself dissolves. A made stone core remains, in its braincase, it pops out original shape. of the sediment that used to fill the braincase. Endocasts were taken of all Caninae Natural endocasts living are very rare. species, except for the South American species, and from some fossil Caninae (for scientific 31 Evolution of thebrain of Plio/Pleistocene wolves of related the in names, see table 1). The endocasts living to genusEucyon (Sotnikova, press; species were mainly taken from the collections of Rook, 1993). the National Natural History Museum, Leiden, A in the of faunalturn-over, or faunal event sense The Netherlands; the endocasts of fossil species Repenning (1967) characterizes the boundary taken from the collections of the were mainly between the end of the middle Villafranchian American Museum of Natural History, New (MN17; Senèze Faunal Unit, 1.8 Ma) and the York. Theendocasts used by Radinsky (1973) are beginning of the late Villafranchian (MN18; stored in the Field Museum of Natural History, Olivola Faunal Unit, 1.7 Ma) in Europe, or the Chicago. Plio-Pleistocene boundary, appointed to 1.77Ma describe of the that et al., The is sometimes To the pattern grooves sepa- (Berggren 1995). event the well folds on the cere- called thewolf-event 1983; Torre, 1992 rate many developed (Azzaroli, and marked of bral cortex, we use the (translated) names given et al), is by the disappearance the folds and of the domestic Gazella for grooves dog Nyctereutes megamastoides, borbonica, brain by Filimonov (1928, represented by Adri- Eucladoceros tegulensis, Pseudodama cf.