Zalambdalestidae, , Archibald and Averianov, 2003

Wible, JR, Rougier, GW, Novacek, MJ & Asher, RJ, 2009, The Eutherian Mammal Maelestes Gobiensis From The Late Cretaceous Of Mongolia And The Phylogeny Of Cretaceous Eutheria, Bulletin of the American Museum of Natural History 2009 (327), pp. 1-123 : 73-76

Zalambdalestidae

According to Kielan-Jaworowska et al. (2004), the Asian Cretaceous clade Zalambdalestidae includes Zalambdalestes from the Mongolian Djadokhta Formation; Barunlestes from the Mongolian Barun Goyot Formation; Alymlestes from the Darbasa Formation of Kazakhstan; Kulbeckia from the Bissekty Formation of Uzbekistan and Yalovach Formation of Tadjikistan; and tentatively the poorly known Beleutinus Bazhanov, 1972 , from the Bostobe Formation of Kazakhstan. Zhangolestes Zan et al., 2006 , from the Quantou Formation of northeast China was referred to Zalambdalestidae by Zan et al. (2006). Zalambdalestids are known to have an enlarged, procumbent anteriormost lower incisor with enamel discontinuous posteriorly and procumbent posterior lower incisors, with the exception of Alymlestes and Beleutinus for which the incisors are unknown.

Wible et al. (2007; figs. 29: P, 30) support- ed a monophyletic Zalambdalestidae (that included the above taxa minus Beleutinus , which was not considered) with 10 synapomorphies (appendix 4: node P): ultimate upper incisor in the maxilla (character 14); anteriormost lower incisor size greatly enlarged (character 15; fig. 35); anteriormost lower incisor procumbent (character 17; fig. 35); anteriormost lower incisor enamel discontinuous posteriorly (character 20); posterior lower incisor(s) procumbent (character 21; fig. 35); m2 hypoconulid lingually placed with slight approximation to the entoconid (character 120; fig. 34); posteriormost mental foramen below the penultimate premolar (character 130; fig. 35); translacrimal canal of Wible et al. (2004) present (character 182); premaxillary-maxillary suture on the palate wedge-shaped, pointing anteriorly (character 184); and a medial course of internal carotid artery (character 270; fig. 36). Kulbeckia is the basalmost zalambdalestid, followed by Zhangolestes , and a trichotomy of Zalambdalestes , Barunlestes , and Alymlestes .

Archibald et al. (2001) (fig. 31B herein) have interpreted Zalambdalestidae , represented by Kulbeckia , Zalambdalestes , and Barunlestes , as a paraphyletic stem lineage to Glires (rodents and lagomorphs). Howev- er, as noted already, all phylogenetic analyses published since 2002 that include zalambdalestids have supported them as members of the placental stem lineage (fig. 29; Ji et al., 2002; Meng et al., 2003a; Luo et al., 2003; Asher et al., 2005; Zack et al., 2005; Luo and Wible, 2005; Wible et al., 2007).

Maelestes has few resemblances to zalambdalestids. Both have procumbent lower incisors, but in the case of Maelestes the anteriomost is neither enlarged (fig. 35) nor has an open, elongate root (fig. 9B). Maelestes shares two unusual features with Zalambdalestes and Barunlestes : a postcristid (between the entoconid and hypoconulid) that is taller than the hypoconulid and nearly transverse (fig. 34), and a midline rod-shaped eminence on the basisphenoid (fig. 36). However, such a postcristid is lacking in Kulbeckia and Zhangolestes and the morphology of the basisphenoid is unknown for zalambdalestids other than Zalambdalestes and Barunlestes , or for most other Cretaceous eutherians for that matter.

CONCLUSIONS

Maelestes is the seventh genus of Late Cretaceous eutherian known from associated upper and lower jaws and most of the skull. Five of the other genera ( Zalambdalestes , Barunlestes , Kennalestes , Asioryctes , and Ukhaatherium ) are also from the Campanian of Mongolia, with the sixth ( Uchkudukodon ) from the Turonian of Uzbekistan (fig. 35). Further, Maelestes is one of five Late Cretaceous eutherian genera (with Ukhaa- therium, Asioryctes , Zalambdalestes , and Barunlestes ) known by postcranial elements other than the atlas and/or axis.

To observe the impact of Maelestes on our analysis, we ran a TNT iteration without it, which resulted in six most parsimonious trees at 2245 steps. The strict consensus of these captured the same principal Late Cretceous clades as the original analysis (fig. 29) with one exception; Cimolestes and Batodon were not grouped together. Furthermore, all resolution between the principal Late Cretaceous clades disappeared, leaving a multichotomy with Montanalestes Cifelli, 1999 , Cimolestes , Batodon , Zhelestidae , Paranyctoides + Eozhelestes , Asioryctitheria , and the clade including Deccanolestes , Zalambalestidae, Leptictidae , and Placentalia. In turn, we eliminated individually the remaining six well-known Late Cretaceous craniodental genera from our TNT analysis. The most extreme modification to the original tree (fig. 29) was produced by eliminating Kennalestes , which produced a strict consensus similar to that produced by the elimination of Maelestes but retaining Cimolestidae . At the other extreme, eliminating Ukhaatherium retrieved the same three most parsimonious trees and strict consensus as did the original tree (of course, minus Ukhaatherium ). Finally, we simultaneously eliminated all seven well-known craniodental Late Cretaceous genera, which resulted in a strict consensus with virtually no resolution among the remaining Late Cretaceous taxa and the exclusion of the Early Cretaceous genera Eomaia , Prokennalestes , Murtoilestes Averianov and Skutschas, 2001 , and Montanalestes from Eutheria , the last to Metatheria and the others outside Theria.

Our analysis including Maelestes supports relationships between Batodon and Cimolestes , as suggested in the absence of phylogenetic analysis by Lillegraven (1969) and Kielan-Jaworowska et al. (2004). Affinities between Batodon and Cimolestes were not supported in the only two prior phylogenetic analyses that included both forms (i.e., Nessov et al., 1998; Archibald et al., 2001; fig. 31B). Moreover, recent classifications ( McKenna and Bell, 1997; Rose, 2006a) have these two forms in widely divergent clades: Batodon in soricomorph lipotyphlans and Cimolestes in Ferae . Our inclusion of Mae- lestes in Cimolestidae sensu Kielan-Jaworowska et al. (2004) expands the previous upper Campanian-Maastrichtian North American Mesozoic range of this clade to the lower Campanian of Mongolia and suggests a possible Asian origin for Cimolestidae . Because few nondental characters are known for Batodon (in particular) and Cimolestes , the features allying these forms with Maelestes are largely from the antemolar lower dentition (fig. 32). The relationship of Batodon and Maelestes is supported principally by upper and lower molar features (figs. 33, 34). The type of the early Paleocene Cimolestes simpsoni preserves the anterior two-thirds of the skull, which has been commented on by Reynolds (1936) and Van Valen (1966) but not fully treated. Given that knowledge of the skull in Late Cretaceous eutherians has expanded significantly since 1966 (e.g., Kielan-Jaworowska, 1981, 1984a, 1984c; Wible et al., 2004, 2005), this specimen deserves additional consideration.

Among the seven Late Cretaceous eutherian genera known from fairly complete skulls, Maelestes is unique. Although not carbon copies, the skulls of the Mongolian asioryctitheres Kennalestes , Asioryctes , and Ukhaatherium are generally similar to one another (fig. 35; Novacek et al., 1997; Kielan-Jaworowska et al., 2004) as are the skulls of the zalambdalestids Zalambdalestes and Barunlestes to each other (fig. 35; Kielan- Jaworowska et al., 2004; Wible et al., 2004). The Uzbekistani asioryctithere Uchkudukodon has the poorest preserved skull of the lot, but it generally resembles those of the Mongolian asioryctitheres (fig. 35; McKenna et al., 2000; Kielan-Jaworowska et al., 2004). On the other hand, Maelestes is the only one to have five upper and lower premolars in the adult (a juvenile Kennalestes has five uppers), a palatal vacuity, a prootic canal, and a postglenoid foramen behind the postglenoid process (fig. 36); it is also the only one not to have an entoglenoid process of the squamosal, which in the other forms is continuous (fig. 36) with the postglenoid process and provides abutment for the anterior crus of the ectotympanic (the latter condition cannot be verified in Uchkudukodon ).

Postcranially, the elements preserved in Maelestes that are also preserved in the much more complete Ukhaatherium are generally similar. According to Horovitz (2003: 866):

Among placental mammals, the skeletal morphology of Ukhaatherium nessovi resembles that of generalized insectivores, for example tenrecs, although Ukhaatherium is more primitive than any placental mammals known in several respects. Ukhaatherium and Asioryctes display several characters that were unknown to occur in eutherians before their discovery, but were known to be present in its outgroups, such as metatherians and Vincelestes . Some of these characters are the presence of epipubic bones (absent in Placentalia but present in zalambdalestids), astragalofibular and medial astragalotibial facets placed at an angle larger than 90 ° with respect to the lateral astragalotibial facet (unlike Placentalia where the angle is straight), lack of a groove on the astraglar trochlea, and a tuber calcis that is depressed in its anteriormost area (whereas it is compressed in Placentalia).

Another feature that can be added to the list as a result of Maelestes is a supraspinous fossa that is not coplanar with the infraspinous fossa. Horovitz’s (2003) suspicion that the position of the infraspinous fossa deep to the supraspinous fossa in Ukhaatherium was natural, rather than the result of postmortem damage, is supported by the preservation of the same arrangement in Maelestes (figs. 24, 25). In turn, a similar positional relationship is preserved in Vincelestes and the dryolestoid Henkelotherium Krebs, 1991 ( Rougier, 1993) . We believe that a similar arrangement is present in the Early Cretaceous eutherian Eomaia , despite the crushed nature of the type specimen (see Ji et al., 2002).

More than half of the roughly 40 genera of Cretaceous eutherians have been named in the last 25 years. An outcome of our increased understanding of morphological diversity among Cretaceous eutherians is a reduction in the number of features diagnostic of Eutheria and Metatheria as well as between crown placentals and their stem lineage. One example is the prootic canal in Eutheria and Metatheria. The absence in placentals, and presence in monotremes and basal marsupials, of the primary lateral head vein and its major distributary, the prootic sinus (which passes through the petrosal on the skull base via the prootic canal) was long believed to be a vascular distinction among modern mammals ( Wible and Hopson, 1993, 1995). This distinction held for fossil members of these clades (canal present in metatherians but absent in eutherians) until 2001, when a prootic canal was reported in an isolated petrosal referred to the Early Cretaceous eutherian Prokennalestes ( Wible et al., 2001) . More recently, a prootic canal was reported in isolated petrosals referred to Late Cretaceous zhelestids ( Ekdale et al., 2004) and in Maelestes (figs. 11, 16; Wible et al., 2007). A prootic canal no longer distinguishes eutherians and metatherians, but is present in two of the most diverse Late Cretaceous eutherian clades (i.e., Zhelestidae and Cimolestidae + Asioryctitheria ). Moreover, the recent report of a small prootic canal in the extant Hispanolan solenodon ( Wible, 2008) is the first for Placentalia. Our tree topology makes the occurrence of the prootic canal in Solenodon a convergent acquisition, and the absence of this structure is still recovered as synapomorphic of Placentalia. Given the level of detail needed to record small structures of the ear region, it is actually likely that these subtle features have been overlooked and a reexamination of basal placentals with a heightened level of awareness may identify a broader distribution of the prootic canal among placentals and eutherians.

Regarding crown placentals and their stem lineage, four early Cenozoic taxa usually considered placentals ( Protungulatum , Oxyprimus , Purgatorius , and Leptictis ) ( McKenna and Bell, 1997; Archibald et al., 2001; Kielan- Jaworowska et al., 2004; Rose, 2006a) fall outside Placentalia in our tree (fig. 29). This alteration in turn has a profound effect on the morphological features occurring at the base of Placentalia (appendix 4). Many features previously considered by some of us (Wible et al., 2004, 2005) to be placental synapomorphies fall at nodes outside the crown group in our tree, including loss of epipubic bones, a complete auditory bulla, pterygoid bones that do not meet on the midline, and contact between the frontal and maxillary bones on the rostrum. This result is firmly supported by our analysis; however, some caveats are pertinent. The taxon sample of the putative placental groups to which these fossils could be related is limited in our analysis and a full treatment would require a sampling effort outside the scope of this project and better suited for long term, broad scale phylogenetic endeavors, such as the mammal part of the National Science Foundation’s Tree of Life program.

The three most diverse clades of Late Cretaceous eutherians ( Zhelestidae , Zalambdalestidae , and Cimolestidae + Asioryctitheria ) are dentally distinct, but within each there are repeating convergent trends in dental evolution. The most unexpected is the reduction in premolar number from five per jaw quadrant. Twenty-five years ago only two Late Cretaceous eutherians were known to have five premolars. Today five premolars are the rule among Early Cretaceous eutherians and occur in Parazhelestes , Zhelestes , and Aspanlestes among Zhelestidae (Archibald et al., 2001) ; in Zhangolestes among Zalambdalestidae ( Zan et al., 2006) ; and in Maelestes (and juvenile Kennalestes ) among Cimolestidae + Asioryctitheria (Kielan-Jaworowska, 1981; Wible et al., 2007). At least some members of each clade reduce to four (or even three in Zalambdalestidae ). In contrast, modern placentals have a maximum of four premolars (e.g., dog) down to none (e.g., mouse).

Kielan-Jaworowska et al. (2004: 463) painted a somewhat bleak picture of the state of our knowledge of Cretaceous eutherians:

With few exceptions, though, the relationships of these taxa [Cretaceous eutherians] to one another—and, perhaps more importantly, to mammalian groups that rose to prominence in the Cenozoic—remain poorly understood. For these reasons, systematic arrangement is arbitrary and unsatisfactory in many cases, and the general adequacy of the Mesozoic record to either calibrate or test models of mammalian evolution based on molecular data (e.g., Foote et al., 1999) is highly suspect. Overall phylogenies should be taken for what they are: hypotheses rather than definitive statements of relationships.

Phylogenies should always be taken as hypotheses. Although our overall picture is perhaps not strongly supported, it is relatively well resolved. The principal clades of Late Cretaceous eutherians identified in our phylogenetic analysis (figs. 29, 30) have been supported over the last few years in phylogenetic analyses by several teams of authors (e.g., Archibald et al., 2001; Luo and Wible, 2005; Archibald and Averianov, 2006). Of course, repetition of a result is not proof of its veracity, but it does further corroborate the hypothesis. Morever, several papers (e.g., Foote et al., 1999; Archibald and Deutschmann, 2001) have tested positively the adequacy of the Cretaceous eutherian fossil record for assessing evolutionary models; Kielan-Jaworowska et al.’s claim that these data are highly suspect is not justified. We acknowledge that controversy exists regarding the relationships of Cretaceous eutherians and Tertiary placentals. Nevertheless, the evidence from the current analysis, which represents the most thorough to date regarding taxa and characters, along with the analyses by Meng et al. (2003a) and Asher et al. (2005), strongly refutes the identification of any skeletally well-known Cretaceous clades within crown Placentalia. The oldest placental in our tree is Mimotona from the early-middle Paleocene of China (Li and Ting, 1986; Wang et al., 1998), which with Heomys from the same formation represent the oldest members of Glires (Li and Ting, 1986; Asher et al., 2005). Given the nested position of Glires in our tree (fig. 29), the diversification of Placentalia likely straddled the K-T boundary into the Mesozoic, but we contend not by much. Latest Cretaceous placentals likely existed, but we have yet to uncover them.