Cladogenesis and replacement in the fossil record of Microsyopidae (?Primates) from the southern Bighorn Basin, Wyoming

Abstract

The early Eocene of the southern Bighorn Basin, Wyoming, is notable for its nearly continuous record of mammalian fossils. Microsyopinae (?Primates) is one of several lineages that shows evidence of evolutionary change associated with an interval referred to as Biohorizon A. Arctodontomys wilsoni is replaced by a larger species, Arctodontomys nuptus, during the biohorizon interval in what is likely an immigration/emigration or immigration/local extinction event. The latter is then superseded by Microsyops angustidens after the end of the Biohorizon A interval. Although this pattern has been understood for some time, denser sampling has led to the identification of a specimen intermediate in morphology between A. nuptus and M. angustidens, located stratigraphically as the latter is appearing. Because specimens of A. nuptus have been recovered approximately 60 m above the appearance of M. angustidens, it is clear that A. nuptus did not suffer pseudoextinction. Instead, evidence suggests that M. angustidens branched off from a population of A. nuptus, but the latter species persisted. This represents possible evidence of cladogenesis, which has rarely been directly documented in the fossil record. The improved understanding of both evolutionary transitions with better sampling highlights the problem of interpreting gaps in the fossil record as punctuations.

1. Introduction

The Bighorn Basin of northwestern Wyoming has been the location of palaeontological expeditions for more than 100 years [1]. Nearly continuous collecting over more than 50 years from the southern Bighorn Basin has yielded tens of thousands of mammalian fossils [2,3], most of which can be tied into a finely resolved stratigraphic section [4]. Because of the density of sampling, and its clear relationship to a temporal framework [5], the Bighorn Basin has played a critical role in arguments over the relative importance of gradualism and punctuated evolution [6]. The southern Bighorn Basin, in particular, has yielded some of the clearest examples of the gradual evolution of one species (or even genus) into another, including the Teilhardina and Tetonius–Pseudotetonius lineages of omomyid primates [7,8], species of the adapoid genus Cantius [9], and the evolution of the paromomyid primate Phenacolemur fortior from Phenacolemur praecox [10]. In each of these examples, the earlier taxon appears to have undergone pseudoextinction without branching as it evolved into the later taxon, supporting an interpretation of anagenesis. As some of the best-documented cases of anagenesis among vertebrates, these examples have provided an interesting challenge to the problem of incorporating a temporal component into the definition of species [11–14]. The southern Bighorn Basin record is also notable for its documentation of periods of coordinated mammalian turnover, with a substantial change in mammalian fauna accompanying the Palaeocene–Eocene Thermal Maximum in some of the earliest deposits [15] and subsequent periods of turnover that have been called biohorizons [5,16]. There is compelling evidence [3] for two such events: Biohorizon A, potentially associated with the onset of regional cooling, and Biohorizon B, which may represent the beginning of a period of warming [3,17]. Identification of these events allows for the study of the effects of climate on mammalian evolution. For these reasons, the southern Bighorn Basin record is important not only within the context of mammalian palaeontology, but because of its relevance to fundamental questions in evolutionary biology.

Microsyopine microsyopids are well known from southern Bighorn Basin deposits, with over 1500 specimens being referable to that group. Microsyopidae is one of 11 families of extinct early Tertiary mammals that are often clustered together as plesiadapiforms [18,19]. The broader relationships of plesiadapiforms in general, and microsyopids specifically, are a source of debate. Although microsyopids are generally held to be euarchontans (i.e. members of the clade that includes Primates, Scandentia [treeshrews] and Dermoptera [colugos]; [20]), some analyses suggest that they are stem primates [21–23], whereas others suggest that some microsyopid species may be more closely related to dermopterans [24–26]. We consider them likely stem primates following Bloch and colleagues [21], but the observations and conclusions presented here do not depend on a particular answer to the question of their broader relationships.

Microsyopidae is one of the longest-lived groups of plesiadapiforms, persisting for over 20 million years in North America, stretching from the late Palaeocene to the late Eocene [27,28]. The subfamily Microsyopinae generally includes the larger species in the family, grouped in the genera Arctodontomys, Microsyops, Megadelphus and Craseops [27]. Previous work [27,29] documented a transition in the microsyopine lineage from Arctodontomys wilsoni to Arctodontomys nuptus around Biohorizon A, with subsequent replacement of A. nuptus by Microsyops angustidens before the onset of Biohorizon B. However, the sample upon which this inference was based was limited, lacking in particular specimens from Biohorizon A itself, and with a gap between the latest occurrence of A. nuptus and the earliest clear occurrence of M. angustidens [27]. Consequently, consideration of the evolutionary mechanisms involved in these transitions was necessarily speculative. The current work reconsiders this set of evolutionary transitions using a sample of approximately 400 specimens (N = 120 with measurable lower fourth premolars [P₄]; electronic supplementary material, information; figure 1) from the deposits below and near Biohorizon B that critically provides data in the gaps in the previously documented sample.

The most diagnostic tooth among microsyopine microsyopids is the P₄. In species of Arctodontomys, this is a relatively simple tooth, with a large protoconid and simple talonid basin with one or two cuspids (figure 1b,c; [29]). There may be a tiny paraconid associated with a paracristid, but there is never a distinctly developed metaconid cuspid, although in some cases a crestid descends from the apex of the protoconid distolingually. All of the microsyopine specimens from below 260 m of the southern Bighorn Basin section lack a metaconid, and so can be identified as pertaining to Arctodontomys. A. nuptus can be differentiated from A. wilsoni in the larger size of its P₄ (ANOVA comparing P₄ area among the three species [F{2,116} = 162.05, p < 0.0001, Tukeys HSD p < 0.0001]), and in this tooth's generally more bulbous appearance, with a protoconid that is broader based and less acutely pointed (figures 1b and 2). Microsyops is distinguished from Arctodontomys by the development of a distinct metaconid cuspid [29]. In M. angustidens (figures 1a and 2d), the P₄ is similar in size to that tooth in A. nuptus (Tukeys HSD p = 0.782) but is notably more molariform; it invariably has a clearly demarcated metaconid, and in many cases a well-developed paraconid. This forms the first stage of a general trend in microsyopine evolution towards a progressively more molariform P₄ in the evolution of Microsyops [27]. Our analysis of dental topographic metrics shows that distinctions in P₄ shape among the three species under consideration here are statistically significant. The M₂s of A. wilsoni and A. nuptus were also found to differ in shape (molars of A. wilsoni have taller, more acute cusps), whereas the molars of A. nuptus are not different in shape from those of M. angustidens [30].

Figure 1.

Natural logarithm of P₄ area versus stratigraphic level (m) from the base of the Willwood Formation. Arctodontomys wilsoni is replaced by the larger A. nuptus near the top of Biohorizon A. Above Biohorizon A, A. nuptus evolves into M. angustidens, as documented by the presence of an A. nuptus–M. angustidens intermediate (star in figure 1), but then reoccurs after an approximately 60 m gap. (a) Left P₄ of Microsyops angustidens (DPC 1392; 378 m); (b) left P₄ of Arctodontomys nuptus (USNM 533678; 190 m); and (c) left P₄ of A. wilsoni (UW 7112; 70 m). Abbreviations: me = metaconid; pa = paraconid; pt = protoconid; ta = talonid basin.

Figure 2.

(a) Arctodontomys wilsoni (DMNH EVP 91287; 160 m); (b) Arctodontomys nuptus (USNM 521438; 250 m); (c) intermediate between A. nuptus and Microsyops angustidens (USNM 540280; 262 m); (d) M. angustidens (USNM 540246; 260 m); and (e) A. nuptus (YPM 30493 reversed; 354 m). The blue arrow in (c) indicates the bulge in the crestid descending from the protoconid distolingually where the metaconid develops in Microsyops, as indicated by the orange arrow in (d). Scale = 1 mm.

In the southern Bighorn Basin sample, the last occurrence of A. wilsoni and the first occurrence of A. nuptus are both documented at the same site (WW-92, ‘Jay's Pocket’), a localized concentration of fossils occupying approximately 10 m² located near the top of Biohorizon A at 212 m above the base of the Willwood Formation. As with similar sites in the southern Bighorn Basin [31], this highly concentrated deposit with copious, very fragile remains of small mammals, likely formed geologically instantaneously. The presence of both species at the site, therefore, indicates that they were essentially coeval, and the absence of intermediates is most consistent with the interpretation that A. nuptus replaced A. wilsoni through immigration rather than through a local evolutionary process. The fact that there are no records of A. wilsoni from higher in the section suggests that the replacement event was complete, and that A. wilsoni became at least locally extinct. This event occurred during the same interval in which many other species in the fauna (1/4 of standing species richness) were also experiencing similar transitions (Biohorizon A), suggesting a common forcing mechanism that has been speculated to relate to regional cooling [2,3,17,32].

By contrast, the turnover from A. nuptus to M. angustidens has a different character. Clearly identifiable specimens of A. nuptus are known from 212 m (locality WW-92) to 250 m ([4]; e.g. USNM 521438 from locality UW-730561; figure 2b). There are no known occurrences of microsyopine microsyopids that include P₄ from 251 to 259 m, a very poorly sampled part of the section. Locality USGS D-1297 straddles the 260–262 m interval [4]. That locality has produced a specimen of A. nuptus (USGS 3812), one of the two lowest documented occurrences of M. angustidens in the southern Bighorn Basin (USNM 540246, figure 2d; also known from DPC 1546 from USGS D-1419 at 260 m) and a specimen that can be identified as an intermediate between A. nuptus and M. angustidens (USNM 540280; figure 2c). USNM 540280 is morphologically similar to Arctodontomys in lacking a clearly demarcated metaconid on P₄. However, it has a very strong crestid extending distolingually from the apex of the protoconid, with a clear swelling along its length, in the typical position of a metaconid. The P₄ also has a well-demarcated paraconid, contributing to a generally more molariform morphology than is typical for an Arctodontomys premolar. This specimen is both stratigraphically and morphologically intermediate between A. nuptus and M. angustidens, and suggests that the former evolved into the latter in the time period sampled at USGS D-1297, which corresponds to approximately 10–12 000 years (10 000 years inferred from an estimate of 3 million years for the total Willwood section, and the temporal value scale of Bown & Kraus [5]; 12 000 years calculated using average sediment accumulation rates between the Palaeocene–Eocene boundary [0 m, 56.33 Ma] and the base of the Chron C24n.3n [455 m, 53.57 Ma]). A. nuptus is then undocumented in the record until 322 m, but reoccurs with four specimens known from 322 to 354 m (figure 2e), in a part of the record from which M. angustidens is also known. These high A. nuptus specimens are the only microsyopines known from above 262 m that lack a metaconid. They can be identified as A. nuptus not only based on that absence, but because they share the broad, bulbous protoconid that is observed in specimens of the species from lower in the section. A. nuptus disappears from the record again (this time permanently) below the base of Biohorizon B, which begins at 370 m.

The combination of an intermediate morphology documented by USNM 540280, followed by the recurrence of A. nuptus at the 322 m level, would suggest the evolution of A. nuptus into M. angustidens, but without the complete pseudoextinction of A. nuptus. This can be interpreted as a potential instance of cladogenesis, with M. angustidens branching off from A. nuptus, but that species persisting. This differs from previously identified evolutionary transitions from the Bighorn Basin (e.g. Tetonius–Pseudotetonius lineage of omomyoid primates; Phenacolemur fortior to Phenacolemur praecox; [7,8,10]), which are more plausibly interpreted as simple anagenesis, since the ancestral species are not known to persist or reappear. Specifically, the inference that this is cladogenesis rests on the persistence of specimens from two diagnostically different species after the inferred evolution of one from the other, documented by the presence of an intermediate.

How does this pattern bear on debates over gradualism and punctuated equilibrium? Perhaps this example highlights the difficulty (or futility) in distinguishing between these modes of evolution, since the interpretations here rest on having an exceptionally densely sampled fossil record, with extremely fortuitous, rare discoveries. If the intermediate between A. nuptus and M. angustidens had not been found, that transition could have been interpreted as simply a punctuated event, probably due to immigration. However, the existence of the intermediate makes a gradual local transition seem likely. The transition from A. wilsoni to A. nuptus could also be interpreted as a punctuated evolutionary event. However, the presence of both species in a single, geographically and geologically very restricted site (‘Jay's Pocket’, WW-92), and the absence of intermediates, is more consistent with an interpretation of replacement by immigration/emigration or immigration and local extinction than sympatric gradual evolution.

In sum, the pattern of evolution in microsyopine microsyopids from the southern Bighorn Basin provides a rare example of possible cladogenesis, and also highlights the necessity of excellent geological data and high-density sampling in understanding apparent punctuation events in the fossil record.

Data accessibility

The data for this paper are available in electronic supplementary material, information.

Authors' contributions

M.T.S. conceived of the study, designed the study, made the measurements and drafted the manuscript. All authors contributed to data interpretation, collected field data and critically revised the manuscript. All authors gave final approval for publication and agree to be held accountable for the work performed therein.

Competing interests

We declare we have no competing interests.