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Authors:

Thomas Guillerme

The University of Sheffield

Google Scholar searches additional OTUs rarefaction curve. The x-axis repre

…

Taxonomic matching algorithm used in this study. For each matrix, each

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Version dated: March 29,2016

Assessment of available anatomical characters for linking

living mammals to fossil taxa in phylogenetic analyses

Electronic Supplementary Material 1

Thomas Guillerme1,∗and Natalie Cooper1,2

1School of Natural Sciences, Trinity College Dublin, Dublin 2, Ireland.

2Department of Life Sciences, Natural History Museum, Cromwell Road, London, SW7 5BD, UK.

*Corresponding author. t.guillerme@imperial.ac.uk

1- Data collection

Public repositories

We downloaded available matrices containing fossil and/or living mammal taxa from

the three databases using the following list of keywords:

Mammalia; Monotremata; Marsupialia; Placentalia; Macroscelidea;

Afrosoricida; Tubulidentata; Hyracoidea; Proboscidea; Sirenia; Pilosa;

Cingulata; Scandentia; Dermoptera; Primates; Lagomorpha; Rodentia;

Erinaceomorpha; Soricomorpha; Cetacea; Artiodactyla; Cetartiodactyla;

Chiroptera; Perissodactyla; Pholidota; Carnivora; Didelphimorphia;

Paucituberculata; Microbiotheria; Dasyuromorphia; Peramelemorphia;

Notoryctemorphia; Diprotodontia.

Details about the speciﬁc search options used for each public repository are

listed below. Note that some matrices were downloaded from more than one database

but this is not a problem because we are interested in the total number of unique living

operational taxonomic units (OTUs), therefore even if some were present in more than

one matrix they still only counted as a single OTU.

MorphoBank.— We accessed the MorphoBank repository (morphobank.org) on 10th June

2015 and used the keywords listed above in the search menu. We downloaded the data

associated with each project matching with the keyword.

Graeme Lloyd.— We accessed Graeme Lloyd’s website repository (graemetlloyd.com/)

on 10th June 2015 and downloaded all the matrices that were available with a direct

download link in the mammal data section of the website

(graemetlloyd.com/matrmamm.html).

Ross Mounce.— We accessed Ross Mounce’s GitHub repository

(github.com/rossmounce/cladistic-data) on 11th June 2015 and downloaded all 601

matrices. We then ran a shell script to select only the matrices that had any text element

that matched with one of the search terms (github.com/TGuillerme/Missing_living_

mammals/blob/master/Functions/select.files.sh). To make the matrix selection

more thorough, we ignored the case and Latin sufﬁx (i.e. ia,ata,ea, and a) of the

keywords.

Google Scholar (accessed 11th June 2015)

To ensure we did not miss any extra matrices that were not available on one of these

repositories, we ran a Google Scholar search on the 11th June using the following

keywords:

order ("morphology" OR "morphological" OR "cladistic") AND characters

matrix paleontology phylogeny

where order was replaced by each of the taxonomic subdivision keywords listed

above in turn. For each taxonomic subdivision keyword we selected the 20 ﬁrst papers

published since 2010 resulting in 660 papers. We selected only the 20 ﬁrst results for

each search term to avoid downloading large numbers of irrelevant articles, and

because the rate of discovery of new matrices was very low and unlikely to be

substantially improved by downloading more papers. For example, in the 660 papers

we downloaded, only 50 contained extra living OTUs and only contributed 425 OTUs

to our total of 4950 OTUs (Figure 1). We selected only articles published since 2010

because almost every recently published matrices contained some of the morphological

characters and OTUs from previous studies, thus almost all older studies are

represented in the matrices we collected. For example, the six living primates used in

[1] (Aotus trivirgatus, Galago demidoff, Lemur catta, Microcebus murinus, Nycticebus coucang

and Saimiri sciureus) and their associated characters are reused along with more living

species and characters in [2,3,4,5,5,6,7,8,9,10,11,12,13].

The list of all 286 downloaded matrices is available on

github.com/TGuillerme/Missing_living_mammals/tree/master/Data/Matrices. The

matrices contained a total of 11010 operational taxonomic units (OTUs) of which 5228

were unique. In this study, we refer to OTUs rather than species because the entries in

the downloaded matrices were not standardised and ranged from speciﬁc individual

specimen names (i.e. the name of a collection item) to the family-level. Where possible,

we considered OTUs at their lowest valid taxonomic level (i.e. species) but some OTUs

were only valid at a higher taxonomic level (e.g. genus or family). Therefore for some

orders, we sampled more genera than species.

Standardising the matrices

0 100 200 300 400 500 600

150 200 250 300 350 400

Google Scholar matches

Number of additional OTUs

Figure 1: Google Scholar searches additional OTUs rarefaction curve. The x-axis repre-

sents the number of Google Scholar matches (papers, books or abstracts) and the y-axis

represents the cumulative number of additional living OTUs for each Google Scholar

match.

We transformed all the non-NEXUS matrices (TNT, Word, Excel, JPEG) to NEXUS

format manually. We then cleaned the NEXUS matrices by removing any extra

information (trees, continuous characters, morphological character descriptions,

molecular data) to end up with NEXUS matrices containing only the discrete

morphological data. We then manually ﬁxed the incorrectly-formatted binomial names

(e.g. H. sapiens became Homo sapiens) using the abbreviation list in the relevant

publications. All the standardised matrices are available on github.com/TGuillerme/

Missing_living_mammals/tree/master/Data/Matrices_binomial/Matrices.

Selecting the living OTUs

We designated as “living” all OTUs that were either present in the phylogeny of [14] or

the taxonomy of [15], and designated as “fossil” all OTUs that were present in the

Paleobiology database (paleobiodb.org/). For OTUs that did not appear in these three

sources, we ﬁrst decomposed the name (i.e. Homo sapiens became Homo and sapiens)

and tried to match the ﬁrst element with a higher taxonomic level (family, genus etc.).

Any OTUs that still had no matches in the sources above were designated as

non-applicable (NA; Figure 2). Non-applicable OTUs were either specimen IDs with

no related taxon names (e.g. FMNHPR2081), abbreviations that were not described in

the associated paper (e.g. Ho.sap.), non-mammals stricto-sensu (e.g. Sinoconodon), non

standard taxonomic levels (e.g. Spalcotheriids) invalid taxonomic designations (e.g.

sp nov 1or Outgroup) or typos (e.g. Hobo sapions).

Matrix

(NEXUS)

single OTU Bininda-Emonds

tree 2007

living

OTU

Wilson &

Reeders 2005 living

OTU

Paleobiology

Database fossil

OTU

ignored

OTU

matches

with? yes

yes

Figure 2: Taxonomic matching algorithm used in this study. For each matrix, each

operational taxonomic unit (OTU) is matched with the supertree from Fritz et al. 2009.

If the OTU matches, then it is classiﬁed as living. Otherwise it is matched with the

Wilson & Reeder 2005 mammalian taxonomy. If the OTU matches, then it is classiﬁed as

living. Otherwise it is matched with the Paleobiology database list of mammals. If the

OTU matches, then it is classiﬁed as fossil. Otherwise it is ignored.

2- Data collection reproducibility

Every step of the analysis (apart from downloading and standardisation of the matrices)

is entirely repeatable via GitHub (github.com/TGuillerme/Missing_living_mammals).

References

[1] Ross C, Williams B, Kay RF. Phylogenetic analysis of anthropoid relationships. J

Hum Evol. 1998;35(3):221–306.

[2] Seiffert ER, Simons EL, Attia Y. Fossil evidence for an ancient divergence of lorises

and galagos. Nature. 2003;422(6930):421–424.

[3] Marivaux L, Antoine PO, Baqri SRH, Benammi M, Chaimanee Y, Crochet JY, et al.

Anthropoid primates from the Oligocene of Pakistan (Bugti Hills): data on early

anthropoid evolution and biogeography. Proc Nat Acad Sci.

2005;102(24):8436–8441.

[4] Seiffert ER, Simons EL, Clyde WC, Rossie JB, Attia Y, Bown TM, et al. Basal

anthropoids from Egypt and the antiquity of Africa’s higher primate radiation.

Science. 2005;310(5746):300–304.

[5] Bloch JI, Silcox MT, Boyer DM, Sargis EJ. New Paleocene skeletons and the

relationship of plesiadapiforms to crown-clade primates. Proc Nat Acad Sci.

2007;104(4):1159–1164.

[6] Kay RF, Fleagle J, Mitchell T, Colbert M, Bown T, Powers DW. The anatomy of

Dolichocebus gaimanensis, a stem platyrrhine monkey from Argentina. J Hum

Evol. 2008;54(3):323–382.

[7] Silcox MT. The biogeographic origins of Primates and Euprimates: east, west,

north, or south of Eden? In: Mammalian Evolutionary Morphology. Springer;

2008. p. 199–231.

[8] Seiffert ER, Perry JM, Simons EL, Boyer DM. Convergent evolution of

anthropoid-like adaptations in Eocene adapiform primates. Nature.

2009;461(7267):1118–1121.

[9] Tabuce R, Marivaux L, Lebrun R, Adaci M, Bensalah M, Fabre PH, et al.

Anthropoid versus strepsirhine status of the African Eocene primates

Algeripithecus and Azibius: craniodental evidence. P Roy Soc B-Biol Scis. 2009;p.

rspb20091339.

[10] Boyer DM, Seiffert ER, Simons EL. Astragalar morphology of Afradapis, a large

adapiform primate from the earliest late Eocene of Egypt. Am J Phys Anthropol.

2010;143(3):383–402.

[11] Seiffert ER, Simons EL, Boyer DM, Perry JM, Ryan TM, Sallam HM. A fossil

primate of uncertain afﬁnities from the earliest late Eocene of Egypt. Proc Nat

Acad Sci. 2010;107(21):9712–9717.

[12] Marivaux L, Ramdarshan A, Essid EM, Marzougui W, Ammar HK, Lebrun R, et al.

Djebelemur, a tiny pre-tooth-combed primate from the Eocene of Tunisia: a

glimpse into the origin of crown strepsirhines. PloS ONE. 2013;8(12):e80778.

[13] Ni X, Gebo DL, Dagosto M, Meng J, Tafforeau P, Flynn JJ, et al. The oldest known

primate skeleton and early haplorhine evolution. Nature. 2013;498(7452):60–64.

[14] Bininda-Emonds OR, Cardillo M, Jones KE, MacPhee RD, Beck RM, Grenyer R,

et al. The delayed rise of present-day mammals. Nature. 2007;446(7135):507–512.

Available from: http://dx.doi.org/10.1038/nature05634.

[15] Wilson DE, Reeder DM. Mammal species of the world: a taxonomic and

geographic reference. vol. 1. JHU Press; 2005.

ResearchGate has not been able to resolve any citations for this publication.

Djebelemur, a Tiny Pre-Tooth-Combed Primate from the Eocene of Tunisia: A Glimpse into the Origin of Crown Strepsirhines

Article

Full-text available

Dec 2013
PLOS ONE

Background: Molecular clock estimates of crown strepsirhine origins generally advocate an ancient antiquity for Malagasy lemuriforms and Afro-Asian lorisiforms, near the onset of the Tertiary but most often extending back to the Late Cretaceous. Despite their inferred early origin, the subsequent evolutionary histories of both groups (except for the Malagasy aye-aye lineage) exhibit a vacuum of lineage diversification during most part of the Eocene, followed by a relative acceleration in diversification from the late Middle Eocene. This early evolutionary stasis was tentatively explained by the possibility of unrecorded lineage extinctions during the early Tertiary. However, this prevailing molecular view regarding the ancient origin and early diversification of crown strepsirhines must be viewed with skepticism due to the new but still scarce paleontological evidence gathered in recent years. Methodological/principal findings: Here, we describe new fossils attributable to Djebelemur martinezi, a≈50 Ma primate from Tunisia (Djebel Chambi). This taxon was originally interpreted as a cercamoniine adapiform based on limited information from its lower dentition. The new fossils provide anatomical evidence demonstrating that Djebelemur was not an adapiform but clearly a distant relative of lemurs, lorises and galagos. Cranial, dental and postcranial remains indicate that this diminutive primate was likely nocturnal, predatory (primarily insectivorous), and engaged in a form of generalized arboreal quadrupedalism with frequent horizontal leaping. Djebelemur did not have an anterior lower dentition as specialized as that characterizing most crown strepsirhines (i.e., tooth-comb), but it clearly exhibited a transformed antemolar pattern representing an early stage of a crown strepsirhine-like adaptation ("pre-tooth-comb"). Conclusions/significance: These new fossil data suggest that the differentiation of the tooth-comb must postdate the djebelemurid divergence, a view which hence constrains the timing of crown strepsirhine origins to the Middle Eocene, and then precludes the existence of unrecorded lineage extinctions of tooth-combed primates during the earliest Tertiary.

The oldest primate skeleton and early haplorhine evolution

Article

Full-text available

Jun 2013
NATURE

Reconstructing the earliest phases of primate evolution has been impeded by gaps in the fossil record, so that disagreements persist regarding the palaeobiology and phylogenetic relationships of the earliest primates. Here we report the discovery of a nearly complete and partly articulated skeleton of a primitive haplorhine primate from the early Eocene of China, about 55 million years ago, the oldest fossil primate of this quality ever recovered. Coupled with detailed morphological examination using propagation phase contrast X-ray synchrotron microtomography, our phylogenetic analysis based on total available evidence indicates that this fossil is the most basal known member of the tarsiiform clade. In addition to providing further support for an early dichotomy between the strepsirrhine and haplorhine clades, this new primate further constrains the age of divergence between tarsiiforms and anthropoids. It also strengthens the hypothesis that the earliest primates were probably diurnal, arboreal and primarily insectivorous mammals the size of modern pygmy mouse lemurs.

The Biogeographic Origins of Primates and Euprimates: East, West, North, or South of Eden?

Chapter

Full-text available

Jan 2008

Mary T Silcox

The place of origin of Primates is a subject that has received surprisingly little treatment in the literature. Part of the difficulty in considering this question is terminological. Until recently, the order Primates had usually been considered to include both euprimates sensu Hoffstetter, 1977, which are clearly related to modern members of the order, and the more archaic “plesiadapiforms” (e.g., Simpson, 1945; Hoffstetter, 1977; Szalay and Delson, 1979; MacPhee et al., 1983; Szalay et al., 1987; note that “plesiadapiforms” is placed in quotation marks to signify that it is likely a non-monophyletic group; Gunnell, 1989; Silcox, 2001). Since the very influential publication of two papers back-to-back in Nature in 1990 (Beard, 1990; Kay et al., 1990), which suggested paromomyid “plesiadapiforms” were more closely related to dermopterans than to euprimates, it has become common practice for authors to exclude “plesiadapiforms” from the order Primates (e.g., Beard, 1998a; Hartwig, 2002; Tavaré et al., 2002; Soligo and Martin, 2006). In this case the taxon name Primates was equivalent in meaning to Euprimates (see also Martin, 1968, 1986; Cartmill, 1972, 1974; Wible and Covert, 1987). This paper seeks to consider, therefore, two distinct but interrelated questions: the place of origin of Primates, and that of Euprimates. The first of these two questions is probably of greater relevance to those interested in the general patterns of mammalian evolution, in that it marks the point at which primates became a lineage distinct from other mammalian orders. The latter question may be of greater relevance to primate specialists, in that it is at this evolutionary transition that characteristic primate features such as convergent orbits and postcranial traits for leaping appear to have arisen (Silcox et al., 2007), although the process by which these features were acquired is not currently documented in the fossil record.

Astragalar morphology of Afradapis, a large adapiform primate from the earliest Late Eocene of Egypt

Article

Full-text available

Nov 2010
AM J PHYS ANTHROPOL

The ∼37 million-year-old Birket Qarun Locality 2 (BQ-2), in the Birket Qarun Formation of Egypt's Fayum Depression, yields evidence for a diverse primate fauna, including the earliest known lorisiforms, parapithecoid anthropoids, and Afradapis longicristatus, a large folivorous adapiform. Phylogenetic analysis has placed Afradapis as a stem strepsirrhine within a clade of caenopithecine adapiforms, contradicting the recently popularized alternative hypothesis aligning adapiforms with haplorhines or anthropoids. We describe an astragalus from BQ-2 (DPC 21445C), attributable to Afradapis on the basis of size and relative abundance. The astragalus is remarkably similar to those of extant lorises, having a low body, no posterior shelf, a broad head and neck. It is like extant strepsirrhines more generally, in having a fibular facet that slopes gently away from the lateral tibial facet, and in having a groove for the tendon of flexor fibularis that is lateral to the tibial facet. Comparisons to a sample of euarchontan astragali show the new fossil to be most similar to those of adapines and lorisids. The astragali of other adapiforms are most similar to those of lemurs, but distinctly different from those of all anthropoids. Our measurements show that in extant strepsirrhines and adapiforms the fibular facet slopes away from the lateral tibial facet at a gradual angle (112-126°), in contrast to the anthropoid fibular facet, which forms a sharper angle (87-101°). Phylogenetic analyses incorporating new information from the astragalus continue to support strepsirrhine affinities for adapiforms under varying models of character evolution.

A fossil primate of uncertain affinities from the earliest late Eocene of Egypt

Article

Full-text available

May 2010
P NATL ACAD SCI USA

Paleontological work carried out over the last 3 decades has established that three major primate groups were present in the Eocene of Africa-anthropoids, adapiforms, and advanced strepsirrhines. Here we describe isolated teeth of a previously undocumented primate from the earliest late Eocene ( approximately 37 Ma) of northern Egypt, Nosmips aenigmaticus, whose phylogenetic placement within Primates is unclear. Nosmips is smaller than the sympatric adapiform Afradapis but is considerably larger than other primate taxa known from the same paleocommunity. The species bears an odd mosaic of dental features, combining enlarged, elongate, and molariform premolars with simple upper molars that lack hypocones. Phylogenetic analysis across a series of different assumption sets variously places Nosmips as a stem anthropoid, a nonadapiform stem strepsirrhine, or even among adapiforms. This phylogenetic instability suggests to us that Nosmips likely represents a highly specialized member of a previously undocumented, and presumably quite ancient, endemic African primate lineage, the subordinal affinities of which have been obscured by its striking dental autapomorphies. Discriminant functions based on measurements of lower molar size and topography reliably classify extant prosimian primates into their correct dietary groups and identify Nosmips and Afradapis as omnivores and folivores, respectively. Although Nosmips currently defies classification, this strange and unexpected fossil primate nevertheless provides additional evidence for high primate diversity in northern Africa approximately 37 million years ago and further underscores the fact that our understanding of early primate evolution on that continent remains highly incomplete.

Convergent evolution of anthropoid-like adaptations in Eocene adapiform primates

Article

Full-text available

Oct 2009
NATURE

Adapiform or 'adapoid' primates first appear in the fossil record in the earliest Eocene epoch ( approximately 55 million years (Myr) ago), and were common components of Palaeogene primate communities in Europe, Asia and North America. Adapiforms are commonly referred to as the 'lemur-like' primates of the Eocene epoch, and recent phylogenetic analyses have placed adapiforms as stem members of Strepsirrhini, a primate suborder whose crown clade includes lemurs, lorises and galagos. An alternative view is that adapiforms are stem anthropoids. This debate has recently been rekindled by the description of a largely complete skeleton of the adapiform Darwinius, from the middle Eocene of Europe, which has been widely publicised as an important 'link' in the early evolution of Anthropoidea. Here we describe the complete dentition and jaw of a large-bodied adapiform (Afradapis gen. nov.) from the earliest late Eocene of Egypt ( approximately 37 Myr ago) that exhibits a striking series of derived dental and gnathic features that also occur in younger anthropoid primates-notably the earliest catarrhine ancestors of Old World monkeys and apes. Phylogenetic analysis of 360 morphological features scored across 117 living and extinct primates (including all candidate stem anthropoids) does not place adapiforms as haplorhines (that is, members of a Tarsius-Anthropoidea clade) or as stem anthropoids, but rather as sister taxa of crown Strepsirrhini; Afradapis and Darwinius are placed in a geographically widespread clade of caenopithecine adapiforms that left no known descendants. The specialized morphological features that these adapiforms share with anthropoids are therefore most parsimoniously interpreted as evolutionary convergences. As the largest non-anthropoid primate ever documented in Afro-Arabia, Afradapis nevertheless provides surprising new evidence for prosimian diversity in the Eocene of Africa, and raises the possibility that ecological competition between adapiforms and higher primates might have played an important role during the early evolution of stem and crown Anthropoidea in Afro-Arabia.

Anthropoid versus strepsirhine status of the African Eocene primates Algeripithecus and Azibius: craniodental evidence

Article

Full-text available

Sep 2009
Proc Biol Sci

Recent fossil discoveries have demonstrated that Africa and Asia were epicentres for the origin and/or early diversification of the major living primate lineages, including both anthropoids (monkeys, apes and humans) and crown strepsirhine primates (lemurs, lorises and galagos). Competing hypotheses favouring either an African or Asian origin for anthropoids rank among the most hotly contested issues in paleoprimatology. The Afrocentric model for anthropoid origins rests heavily on the .45Myr old fossil Algeripithecus minutus from Algeria, which is widely acknowledged to be one of the oldest known anthropoids. However, the phylogenetic position of Algeripithecus with respect to other primates has been tenuous because of the highly fragmentary fossils that have documented this primate until now. Recently recovered and more nearly complete fossils of Algeripithecus and contemporaneous relatives reveal that they are not anthropoids. New data support the idea that Algeripithecus and its sister genus Azibius are the earliest offshoots of an Afro– Arabian strepsirhine clade that embraces extant toothcombed primates and their fossil relatives. Azibius exhibits anatomical evidence for nocturnality. Algeripithecus has a long, thin and forwardly inclined lower canine alveolus, a feature that is entirely compatible with the long and procumbent lower canine included in the toothcomb of crown strepsirhines. These results strengthen an ancient African origin for crown strepsirhines and, in turn, strongly challenge the role of Africa as the ancestral homeland for anthropoids

The delayed rise of present-day mammals

Article

Full-text available

Dec 2008
NATURE

Did the end-Cretaceous mass extinction event, by eliminating non-avian dinosaurs and most of the existing fauna, trigger the evolutionary radiation of present-day mammals? Here we construct, date and analyse a species-level phylogeny of nearly all extant Mammalia to bring a new perspective to this question. Our analyses of how extant lineages accumulated through time show that net per-lineage diversification rates barely changed across the Cretaceous/Tertiary boundary. Instead, these rates spiked significantly with the origins of the currently recognized placental superorders and orders approximately 93 million years ago, before falling and remaining low until accelerating again throughout the Eocene and Oligocene epochs. Our results show that the phylogenetic `fuses' leading to the explosion of extant placental orders are not only very much longer than suspected previously, but also challenge the hypothesis that the end-Cretaceous mass extinction event had a major, direct influence on the diversification of today's mammals.

Mammal Species of the World: A Taxonomic and Geographic Reference

Article