The Fossil Record

Before proceeding any further, it is necessary to draw a crucial distinction between the time of initial divergence of a given group, such as the primates, and the age of the last common ancestor of all known, diagnosable members of that group (Figure 1). In a phylogenetic tree, the initial time of origin of any given taxon is indicated by the point of divergence between that taxon and its most closely related sister taxon (node 1 in Figure 1). Initially, the taxon of interest might diverge from its closest relatives as a lineage lacking the characteristic morphological features of its later descendants and then exist for some time before developing recognizable diagnostic characters. A considerable temporal gap may, therefore, occur between the initial divergence of a taxon and the emergence of diagnostic morphological characteristics as recognized by paleontologists (i.e., between nodes 1 and 2 in Figure 1). With respect to the evolution of placental mammals, this point has been succinctly expressed by Madsen et al. (2001): "Easteal (1999) suggested that primitive placentals from the Cretaceous may have diversified phylogenetically before they diverged morphologically and acquired the diagnostic features of ordinal level crown-group clades." The upper limit for the temporal gap between the initial divergence of a taxon and the emergence of diagnostic morphological characteristics is set by the estimated age of the last common ancestor of modern lineages within the taxon (node 3 in Figure 1), or by the age of the oldest known clearly recognizable fossil representative of the taxon, whichever is older.

Figure 1. In a molecular phylogeny, the time of origin of taxon A (with living representatives A1, A2, and A3) is indicated by node 1, the point of inferred divergence from the most closely related sister taxon with living representatives (B). The time of initial divergence of living representatives of taxon A from their last common ancestor may be considerably younger, as indicated by node 3. Molecular estimates can also be used to infer the date of node 3, in this case the time of divergence between A1 and (A2 + A3). Derived morphological features shared by the living representatives of taxon A may have developed at any time between nodes 1 and 3. The earliest morphologically recognizable member of taxon A exhibiting derived diagnostic features shared with the living representatives is indicated by node 2. The first known fossil representative allocated to taxon A (AF), on the basis of derived features shared with living representatives, yields a minimum date for the origin of the taxon. It should be noted that AF may be nested within the adaptive radiation leading to living representatives (as is widely presumed to be the case for Eocene adapiforms and omomyiforms), but it is also possible that AF diverged at some time prior to the common ancestor of living representatives (i.e., prior to node 3).

It should be noted that inferred phylogenetic relationships, in conjunction with the fossil record, may be used to extend minimum estimates of divergence times in some cases (Norell, 1992; Smith, 1994). Under the assumption that sister groups had the same time of origin, the later-appearing sister group is assumed to have existed at least by the time of first appearance of the earlier-appearing sister group. The range extension for the later-appearing sister group is referred to as a ghost lineage (Norell, 1992). In the case of the primates, the uncertainties that prevail regarding both the composition of and the relationships within Archonta—the supraordinal grouping to which primates are often allocated—make it difficult to apply the concept of the ghost lineage. It can be noted, however, that none of the modern orders of Archonta extends back much beyond the time of the earliest known primate fossils. The oldest known fossils belonging to Scandentia are from Eocene deposits (Tong, 1988), while the oldest fossils tentatively attributed to Volitantia (Dermoptera + Chiroptera) are late Paleocene (Stucky and McKenna, 1993), which would extend the expected range of the primates back by no more than a few million years. Among extinct groups of archontans, the Plesiadapiformes and the Mixodectidae (as possible members of Dermoptera) are potentially relevant (Hooker, 2001). If confirmed to represent the sister group of primates, either of these would extend the expected range of primates back to the early Paleocene.

Undoubted primates (equated here with Euprimates) first appeared in the fossil record at the beginning of the Eocene period in Western Europe, Asia, and North America. A reported primate from the late Paleocene of Morocco (Sige et al., 1990), Altiatlasius, has recently been reassigned to the Plesiadapiformes (Hooker et al., 1999) and is, therefore, not considered here. The absence from the known fossil record of any pre-Eocene primates of modern aspect is usually interpreted as evidence that the order originated not long before that period, around 60 MYA and no earlier than 65 MYA.

However, the ages of the first known fossil representatives of certain other mammalian groups are in themselves incompatible with the interpretation that the placental lineage leading to primates diverged only 60-65 MYA. The best illustration of this is provided by studies of artiodactyl relationships. It has long been accepted that cetaceans and artiodactyls are sister-groups, but recent molecular evidence has uniformly indicated that cetaceans are actually nested within the artiodactyls and that their closest relatives are hippopotamuses. This conclusion, initially suggested by immunological data (Sarich,

1993), is now supported by nuclear gene sequences (Gatesy, 1997; Gatesy et al., 1996, 1999; Graur and Higgins, 1994; Madsen et al., 2001; Murphy et al., 2001a, b), by insertions of interspersed elements (retroposons) in the nuclear genome (Nikaido et al., 1999), and by complete mitochondrial genomes (Ursing and Arnason, 1998). In fact, evidence from two early terrestrial relatives of cetaceans: Ichthyolestes and Pakicetus (Thewissen et al., 2001), has confirmed that they share the unique tarsal morphology of artiodactyls and are, therefore, more closely related to them than to mesony-chians, which were long thought to be the direct sister group of cetaceans. Although a cladistic analysis of the morphological data did not confirm a specific link between cetaceans and hippopotamuses, there is undoubtedly a closer link between cetaceans and artiodactyls than hitherto believed by paleontologists. The molecular evidence now uniformly indicates that the following sequence of divergences occurred during the evolution of the hoofed mammals (ungulates): (1) between odd-toed perissodactyls and even-toed artiodactyls; (2) within artiodactyls between camels + pigs and ruminants + hippos + cetaceans; (3) between ruminants and hippos + cetaceans; (4) between hippos and cetaceans. Given that the first known fossil representative of the cetaceans is dated to about 53.5 MYA (Bajpai and Gingerich, 1998), it follows that the initial divergence in this well-supported sequence of 4 splits in ungulate evolution must have occurred at a relatively early date and that the separation between ungulates and the lineage leading to primates must have taken place even earlier. A date of only 60-65 MYA for the divergence of the primate lineage from other lineages of placental mammals hence seems inherently improbable. It seems likely, instead, that the early evolution of primates has simply remained undocumented in the known fossil record.

Early placental mammals seem to be generally poorly documented in the known fossil record. This is strikingly illustrated by the case of bats (order Chiroptera). Modern bats constitute a widespread and diverse group containing around a thousand species, including at least 165 megachiropterans (Old World fruit bats) and at least 815 microchiropterans (Corbet and Hill, 1991). As with primates of modern aspect, the earliest known clearly identifiable bat fossils date back to the beginning of the Eocene (about 55 MYA) in North America, Europe, Africa, and Australia, although one report extends this back into the latest Paleocene, to 56 MYA. The first relatively complete bat skeletons are known from early Eocene deposits in North America (Icaronycteris) and from Early/Middle Eocene deposits in Europe

(Archaeonycteris, Hassianycteris, and Palaeochiropteryx). By this time, all of the major defining morphological features of bats can be identified, notably including the development of a wing membrane (patagium) between digits II and V of the hand and extreme backward rotation of hindlimbs for suspension, involving extensive remodeling of the pelvis and ankle joint. Furthermore, all four Eocene bat genera documented by relatively complete skeletons show weak to moderate enlargement of the cochlea, indicating the development of some degree of echolocation capacity. For this and other reasons, a recent review of morphological evidence (Simmons and Geisler, 1998) concludes that these 4 genera are more closely related to microchi-ropterans than to megachiropterans and branched off successively from the lineage leading to the common ancestor of microchiropterans, such that they are an integral part of the adaptive radiation that led to modern bats. Yet there are no known fossils documenting the transition from a generalized early placental ancestor to the highly specialized, immediately recognizable condition of the earliest known bat skeletons. Furthermore, there is an obvious and extreme bias in the geographical occurrence of well-preserved bat fossils. Whereas at least 4 skeletons of Icaronycteris have been reported from a single site in North America (Green River, Wyoming, approx. 53 MYA), all the others (some 100 skeletons of Archaeonycteris, Hassianycteris, and Palaeochiropteryx) have been discovered at the European site of Messel, southern Germany (approx. 49 MYA). With some of the exquisitely preserved bat skeletons from Messel, remains of the stomach contents are also present. Analysis of these has revealed moth wing scales indicating dietary habits comparable to those of modern microchiropteran bats.

The fossil record for Old World fruit-bats (megachiropterans) is even less informative. The earliest known remnant is a single tooth identified as that of a megachiropteran found in upper Eocene deposits of Thailand (Ducrocq et al., 1993). Given that microchiropterans are reliably documented from the earliest Eocene, this could indicate a ghost lineage of some 15 MY prior to the earliest known megachiropteran.

Furthermore, a recent cladistic analysis of archontan relationships using both cranial and postcranial characters has provided evidence for a Cretaceous origin of bats (Hooker, 2001). In the cladogram issued from that study, bats branch off at a lower node than both the extinct genus Deccanolestes—a possible primitive Archontan—and the extinct family Nyctitheriidae. Therefore, the early Paleocene age of the oldest known nyctithere and the latest

Cretaceous age of Deccanolestes imply that the divergence of bats from other known mammals occurred at least as long ago as the latest Cretaceous (Hooker, 2001).

Overall, it is obvious that there are very large gaps in the fossil record for bats. In particular, the transition to the shared morphology of all known bats is not documented at all.

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