mammalian phylogeny: comparison of morphological and ... · mammalian phylogeny: comparison of...

Mammalian Phylogeny: Comparison of Morphological and Molecular Results’~2

Jeheskel Shoshani Department of Biological Sciences, Wayne State University

In an attempt to resolve the “bushy” part at the root of the eutherian tree, 182 nondental morphological characters from 100 species (79 extant and 21 extinct; 98 mammalian and 2 nonmammalian) were analyzed using two maximum-parsimony tree-building algorithms. Parallel analyses of 2,258 pairwise immunodiffusion comparisons with chicken antisera on 10 1 mammalian species and of amino acid sequence data of alpha and beta hemoglobins and other published protein sequences were also carried out. The morphological and molecular phylogenies agree in depicting the infraclass Eutheria as consisting of five major clades (thus resolving part of the “bush”). Rates of evolution were also found to be similar in the two types of phylogenies.

Introduction

Most students of mammalian evolution agree on a tripartite division of the class Mammalia into the subclasses Prototheria and Theria with the further subdivision of Theria into infraclasses Metatheria and Eutheria as discussed by Simpson (1945); beyond that point, agreement stops (Novacek 1982). Evidence presented here corrob- orates this tripartite division.

Differences in opinion center on the branching patterns close to the root of Euth- eria; “the phylogenetic history of eutherians is commonly depicted as a bushlike radiation sprouting from mysterious roots at the end of the Mesozoic” (Novacek 1982, P. 3).

A major objective of this study has been to resolve this “bushy” pattern at the root of Eutheria. Research began 10 years ago using the immunodiffusion (IMDFN) technique (Goodman and Moore 197 1) to study relationships among the living Paen- ungulata (Proboscidea, Sirenia, and Hyracoidea) of Simpson (1945). The nature of the IMDFN technique (only living species can be studied) and the need to study extinct forms resulted in the examination of morphological characters, specifically, nondental osteological characters. More recently, this writer analyzed amino acid sequences of alpha and beta hemoglobins (Shoshani et al. 1985a). These studies enabled the author to view problems of mammalian systematics in a broad perspective, an opportunity afforded by employing both molecular and morphological methods of investigation. This paper summarizes these findings and compares them to those of other investigators.

1. Key words: Mammalia, Eutheria, Paenungulata, phylogeny, morphology, molecules.

2. This paper was presented to the Fourth International Theriological Congress, Edmonton, Alberta, Canada, August 13-20, 1985.

Address for correspondence and reprints: Dr. Jeheskel Shoshani, Department of Biological Sciences, Wayne State University, Detroit, Michigan 48202.

Mol. Biol. Evol. 3(3):222-242. 1986. 0 1986 by The University of Chicago. All rights reserved. 0737-4038/86/0303-3307$02.00

222

Morphological versus Molecular Results 223

Material and Methods Material IMDFN

Some of the blood samples employed in this study had been collected and stored frozen at Morris Goodman’s laboratory (Wayne State University), while other samples were collected by the author in the United States, Asia (mostly the Far East), and Africa. Purified albumins were either obtained commercially or prepared following the procedures of Travis and Pannell (1973). White leghorn chickens (Gallus domes- ticus, order Galliformes, class Aves), used as hosts for antibody production, were purchased at a local market. The equipment required to conduct the IMDFN exper- iments was available in Goodman’s laboratory (see Goodman and Moore 197 1 for details). Table 1 provides an outline of the methods employed.

Amino Acid Sequences

The amino acid sequences compared in this paper come from three studies (Kleinschmidt et al. 1985; Shoshani et al. 1985a; Miyamoto and Goodman 1986).

Osteological Investigations

The osteological material examined in this study consisted of disarticulated bones and mounted skeletons found in 22 museum collections or field locales in the United States, Eurasia, and Africa. Most of the data were collected at the following museums: (1) American Museum of National History, New York; (2) British Museum (Natural History), London; (3) Field Museum of Natural History, Chicago; (4) Geological Mu- seum, Cairo; (5) Michigan State University Museum of Zoology, East Lansing, Mich- igan; (6) National Museum of Natural History, Smithsonian Institution, Washington, D.C.; (7) University of Michigan Museums of Zoology and Paleontology, Ann Arbor, Michigan; and (8) Wayne State University Museum of Natural History, Detroit. Table 1 provides a summary of the total number of eutherian taxa studied.

Methods IMDFN

In brief, this method involves the following procedure: day 1, injection of a donor’s blood sample (i.e., antigens) into a host, (here a chicken); day 30, booster injection; day 60, withdrawal of blood sample containing antibodies from the host for testing.

Table 1 Outline of Methods of Investigation Employed

Technique/Method No. of Eutherian Orders Studied

Methods of Analysis

IMDFN . . . . . . . . 19” UWPGM Osteological . . . . . . 24b MPC Amino acid sequences . . . . . . 13 (16)* MP

UWPGM = unweighted Pair Group Method (after Sokal and Michener 1958). * Erinaceomorpha and Soricomorpha, as given in fig. 2, are names used by McKenna (1975);

in fig. 3 these were grouped under Lipotyphla (Simpson 1945). b Approximate, depending on inclusion or exclusion of certain taxa within or out of other

taxa. c Two algorithms were used (one after Goodman et al. 1982 and one after Swofford 1984). * Numbers outside and inside parentheses refer to number of orders studied by Shoshani et

al. (198%) and by Miyamoto and Goodman (1986), respectively.

224 Shoshani

Chickens were used because they are equally distant from all mammalian orders. Immunization and IMDFN techniques have been thoroughly described by Goodman and Moore (197 I), Dene et al. (1978), and Shoshani et al. (198%).

Morphology: Character Evaluation

All the characters examined in this study are nondental. Dentition was avoided for two main reasons: ( 1) Dental features of certain mammals are lacking (e.g., some are edentates) or are unique among mammals (e.g., aardvark, Orycteropus a$%)-and therefore do not reveal much about their phylogenetic position-and (2) dental characters of mammals have been studied extensively and there is a need for independent evidence.

The main concern in the examination of osteological characters has been that characters examined in different species are homologous. Characters were carefully studied and compared among individuals of the same species and among different species. Character-state polarity was determined as proposed’ by Hecht and Edwards (1977) and Novacek (1985). In the vast majority of cases, at least three specimens- juvenile, subadult, and adult-per species were examined. Specimens of fetuses, males, females, and wild as well as captive individuals were included whenever available. When a character proved to be variable, at least seven more specimens were examined. Four rare species were represented only by one or two specimens. The examination of a few or several specimens per species was particularly important when studying cranial foramina in Mammalia; in this class the crania of young animals (or fetuses) were compared to those of adults because it was not always possible to delineate the particular bones forming a specific foramen in the fused bones of adult specimens. A 10X magnifying glass was usually sufficient for examinations of small skulls, but a microscope was used when needed.

Size and adult weight of members of a species were also a consideration when selecting taxa for examination. Thus, representatives of the smallest mammals (shrews) as well as of the largest mammals (proboscideans and perissodactyls) were included in the analyses to test the hypothesis that size and weight, as well as phylogenetic affinities, may influence characters such as patterns of bone articulation and number of ribs.

A total of 182 nondental osteological characters was examined on 100 species (representing 28 orders, 26 of which are mammals; Reptilia and mammal-like reptiles are employed as outgroups).

Morphology: Coding the Characters

Since the osteological data were to be analyzed by a program initially written for amino acid sequence data (Goodman et al. 1982) and by Swofford’s (1984) program, which is mostly used for morphological characters, there was a need to employ letter codes that would suit the formats of both programs and yet not bias the results. For binary coding, letters Y and N were used, whereas for unordered, multistate characters up to four letters were used: Y, N, D, and H. These letters represent a single evolutionary change from any one state to any other (Goodman et al. 1982).

In a few cases when the polarity of a character could be determined from the literature, a system of two or more columns was used to show that polarity. For example, character states a = NN, b = NY, and c = YY would imply a possible transformation series of a - b - c. Alternatively, it could also imply a - b - c or a - b - c, depending on the position of the outgroup taxa in relation to the ingroup


taxa possessing a specific character state. In Swofford’s (1984) program, ordered and unordered characters are specified.

Maximum Parsimony: General

The maximum parsimony (MP) principle has been considered the most effective tool for constructing phylogenetic trees (Fitch 197 1; Goodman et al. 1982; Cracraft 1985). The amino acid sequence data discussed in this paper were analyzed by the MP program of Goodman et al. ( 1982). The osteological data collected were analyzed by two different MP programs (Goodman et al. 1982; Swofford 1984) in order (1) to reply to criticism directed against the Goodman et al. (1982) program because it was initially written for analyzing amino acid sequences (Moore 1976) and (2) to compare the similarities and differences between them. Outlines of these computer programs follow.

MP after Goodman et al.

Goodman’s MP method (GMPM; Goodman et al. 1982) is employed principally to analyze sequence data and yields trees with the fewest number of steps from the ancestral to the descendant nodes. This method minimizes parallel and back mutations and thus maximizes the similarities among them arising from common ancestry. The GMPM includes (1) production of a matrix of minimum mutation distances from data (following the procedure of Fitch and Margoliash [ 1967]), (2) construction of unbiased starting trees from this distance matrix (one by the unweighted-pair-group method of Sokal and Michener [ 19581 and another by the distance Wagner tree of Farris [ 1972]), and (3) branch swapping in search of a parsimonious phylogenetic solution, using a dendrogram given in step (2) as a starting point.

Phylogenetic Analysis Using Parsimony (PA UP) after Swoflord

The PAUP program (Swofford 1984) is employed to infer phylogenetic trees following the principle of MP; thus homoplasy (convergent evolution, parallel evolution, and back mutations) is minimized. PAUP can be used to estimate Wagner trees; however, unlike the Wagner program (see Farris 1970 on Wagner trees), PAUP can treat unordered as well as ordered characters, that is, multistate characters may or may not exhibit directionality of evolution.

A data file can include mixed ordered and unordered characters because characters are assumed to be independent, and analyses are not affected by this mixing. An unordered multistate character has no a priori transformation series and thus is pre- ferred in most cases, but if the transformation series is known, the command “ordered” should be used (see also explanation under GMPM). Other options available in PAUP include rooting of a tree (by an outgroup) and listing of synapomorphies. An important option available is that branch swapping can be performed both locally and globally. The global mulpars (multiple equally parsimonious solutions) is by far the most powerful branch-swapping combination. In this option, the branch swapping is performed on the shortest tree, and if there are mulpars, they are kept in memory and retested in search of more-parsimonious topologies. The global mulpars option, ac- cording to Swofford (1984), “reduces the problem of entrapment in local optima.” Swapping and rearrangement of one of the equally parsimonious trees may lead, on further rearrangement, to a still shorter tree. In this study, the osteological data were analyzed with the options “mulpars” and “unordered all.” The PAUP has also been


of the spur-making species to the homologous species (the species against which the antibodies were made) than do those species that did not make spurs. From these and other comparisons, antigenic distance tables are produced, one of which is shown in table 2. In this table the taxon that is most closely related to the homologous species is listed first and that least closely related is listed last. Data from 11 antisera (six against whole sera and five against purified albumins) were employed to produce 11 antigenic distance tables. These tables were then used to generate the divergence tree depicted in figure 2.

Figure 2 is a summary of combined IMDFN results based on 11 chicken antisera produced against albumins and whole sera. A total of 2,258 IMDFN comparisons was conducted among 10 1 mammalian species representing 2 1 orders. Results show that within Eutheria the following branching arrangements are more well-founded than are other possibilities: (1) close relationships among the Paenungulata ([PAEN] = Proboscidea, Tubulidentata, Hyracoidea, and Sirenia), (2) close affinity between Carnivora and Pholidota, (3) very close relationships between Cetacea and Artiodactyla, (4) distant relationship between PAEN and Ungulata (Artiodactyla and Perissodactyla), (5) association between Primates and Scandentia (not as strong associations as in [ l]-[3] above because antibodies were made only against Primates and only against albumin).

The order of relationships of PAEN ([l] above and fig. 2) is different from that which is based on chicken antisera to whole sera (data not presented); that is, Pro-

Table 2 Antigenic Distance Table for Chicken Antiserum against Whole Serum of Elephas maximus (Asian elephant)

Taxon Antigenic Distance

Loxodonta africana ...... Sirenia ................ Tubulidentata .......... Hyracoidea ............ Rodentia .............. Edentata .............. Dermoptera ............ Primates .............. Perissodactyla .......... Scandentia ............. Tenrecidae ............. Soricidae .............. Macroscelidea .......... Artiodactyla ............ Cetacea ............... Erinaceidae ............ Chiroptera ............. Carnivora ............. Lagomorpha ........... Marsupialia ............ Monotremata ..........

-0.5706 1 a 3.01558 3.2 1640 3.59808 3.8652 1 3.88347 3.90058 4.060 11 4.069 17 4.20284 4.20308 4.20930 4.28084 4.36983 4.49929 4.53963 4.67760 4.70778 4.8238 1 4.83348 5.07098

’ The negative value indicates that Loxodonta made spurs against all the heterologous species compared.

228 Shoshani

FIG. 2.-A divergence tree of combined results from chicken antisera produced against mammalian whole sera and albumins obtained from IMDFN-plate comparisons. Solid lines (-) ascend to taxa employed as homologous (donor) species to whole sera; broken lines (-a - * -) ascend to taxa employed as homologous species to albumins; dashed lines (-- - - -) ascend to taxa employed as heterologous (nondonor) species. UN- C = Ungulata-Cetacea; P-C = Pholidota-Camivora; PAEN = Paenungulata. Relationships within PAEN change with the type of antisera used (see text and note a to table 1 for details).

boscidea and Sirenia joined first, and the resultant branch was then joined by Tubu- lidentata and Hyracoidea, respectively (cf. results presented in fig. 1 and table 2). These differences stem from the total number of species compared with each antiserum and the overall network of comparisons. Whole-sera results, which incorporate several proteins, are better founded than purified-albumin results, which are based on a single protein. The author believes that these IMDFN-based differences among the living paenungulate taxa are not as important as the fact that the four orders appear to share a monophyletic origin (cf. results of de Jong et al. 198 1; Rainey et al. 1984). The original data, list of species, or other information from the IMDFN, amino acid sequences, and morphological studies may be obtained from the author on request.

Amino Acid Sequences

Shoshani et al. (1985a) analyzed alpha and beta hemoglobin chains of 83 vertebrate species (2 1 of which were nonmammals), and Kleinschmidt et al. (1985) ex- panded the study by adding a sirenian species (Trichechus inunguis) and some rodents. The latter’s eutherian tree is similar to that in Shoshani et al. (1985a) and has the Sirenia grouped with Proboscidea and Hyracoidea. Miyamoto and Goodman (personal communication) combined all known sequences of seven protein molecules in one file and analyzed them by the GMPM. Their eutherian tree shows Edentata as an


outgroup to all other placental taxa, followed successively by these seven clades: (1) Tubulidentata-Sirenia-Proboscidea-Hyracoidea, (2) Artiodactyla-Perissodac- tyla-Cetacea, (3) Primates-Lagomorpha-Rodentia, (4) Chiroptera, (5) Scandentia, (6) Insectivora, and (7) Carnivora-Pholidota. Comparable sequences for Dermoptera and Macroscelidea were unavailable. Compare this branching pattern to those in figures 2 and 3.

Morphological Characters

Figure 3 summarizes the morphological results; it is one of the most parsimonious cladograms. Letters A-E at the top of this figure represent the five major clades of Eutheria. Letters a-z at the nodes in the cladogram refer to associated synapomorphic characters for these branching points; see table 3 for a listing. Splitting times of taxa were obtained either for the oldest record of a specific taxon examined or for the maximum possible divergence time. Information was taken from either museum rec- ords or the literature (e.g., Romer 1966; Novacek 1982; Savage and Russell 1983).

Hypothesis Testing

The testing of alternative phylogenetic hypotheses against the same data set was conducted as illustrated by several examples in table 4. The results tabulated in part A (hypotheses of other workers) are depicted in figure 4. As shown, it costs 3 1 additional evolutionary changes (EC) to reconcile the relationships after Simpson (1945) with the author’s morphological data. Similarly, it costs 19 and 2 1 additional EC to reconcile

300

WW

FIG. 3.-One of the most parsimonious cladograms for ordinal relationships within Mammalia (Reptilia and Cynodontia serve as outgroups) based on nondental morphological characters. Letters A-E at the top represent major clades for easy reference; letters a-z at the branching points refer to synapomorphic characters (see table 3). See table 4 and text for other equally parsimonious solutions.

Table 3 Synapomorphic, Nondental Characters as Evidence in Support of the Hvoothesis Shown in Fig. 3

a-c: 9, 19, and 10 Synapomorphies, respectively.

d: Eutheria: 1. 2.

3. 4. 5. 6. 7. 8.

!Z 9.

10.

Septomaxilla bone: absent a Optic foramen: separate (not confluent with orbital fissure and/or other cranial foramina) Mandibular symphysis: fused Femur-fibula contact: absent Embryonic trophoblast: present b Chorioallantoic placenta: present Intrauterine gestation: prolonged Ureters: pass lateral to derivatives of Miillerian ducts Cerebral hemispheres: enlarged Corpus callosum: present

e: Trichotomy (see text under Equally Parsimonious Solutions [EPS])

f: Clades B, C, D, and E: 1. Stapes: horseshoe-shaped, large basal

perforation and arched crurac 2. Clavicle: absent

g: Clade B (see text under EPS for alternatives within this clade): 1.

2.

3.

A foramen ventral to postorbital process: absent Mandibular foramen: ventral to alveoli line of cheek teeth (w; see z9) Scapula: infraspinous fossa larger than supraspinous fossa (B; see r5, w3, and zll)

4. Humeral entepicondylar foramen: absent (m; see r7 and z 12)

5. Ulna-lunar contact: present h: Paenungulata, in part, of Simpson ( 1945):

1.

2.

3. 4. 5.

6.

7.

8. 9.

Premaxillary canal: present (m; see n 1 and ~1)~ Maxilla: contributes to rim of orbit (i.e., wedged between lacrimal and jugal) (m; see ul) Alisphenoid canal: present (m; see x2) Postglenoid process: present (m; see t 1) Secondary external acoustic meatus: incomplete e Jugal foramen: present (B; see r2 and sl) Humeral lateral condyle: distal end articulates equally with radius and ulna Thoracic vertebrae: 19 plus f Astragalar head: with short neck, semicircular

i: Tethytheria of McKenna (1975, and personal communication):

1. Carpal bones: serially arrangedg 2. Foramen magnum: formed by

basioccipital and exoccipitals (B; see r3)

3. Angular process of dentary: vestigial (D; see r4)

4. Scapular acromion process: short or absent (m; see 92)

5.

6.

7. -. J-

1. 2.

3.

4.

Pisiform: flat anteroposteriorly, broad contact with cuneiform Jugal bone: participates in mandibular fossa (M; see ~7)~ Coronoid canal: present f

Postglenoid process: absent (0; see h4) Coronoid process of dentary: axis is perpendicular to or forms an acute angle with molar alveoli Coronoid process of dentary: does not project dorsal to margin of zygomatic arch (m; see 04 and y5) Astragalus-cuboid contact: absent (m; see u5)

k: (Note: It costs only two additional evolutionary changes to join Proboscidea to Desmostylia in support of the hypothesis of Domning et al. [ 19861): 1.

2.

3.

4.

5.

6.

Naso-facial region: retracted (=elevated external naris) Premaxilla-frontal: wide contact at or posterior to middle of orbit Position of orbit: forward (anterior to molars) 1

( , Squamous portion of zygoma: extends

much laterally Secondary external acoustic meatus: complete e Hypoglossal foramen: confluent with jugular foramen

7. Mastoid foramen: present (m; see m2) 8. Coronoid process of mandible: anterior

end extends forward into labial molar- premolar region

9. Patella: roundish, approximately ball shaped (B; see OS)

I: I. Naso-lacrimal foramen: absent 2. Jugal foramen: absent (0; see h6) 3. Jugal: does not participate in

mandibular fossa (0; see i6) 4. Ethmoid foramen: absent 5. Spheno-frontal foramen (=sinus canal):

present (D; see ~2) 6. Digit III: not the longest (B; see ~8)

m: Glades C, D, and E (see text under EPS

z for alternative arrangements): I Mesethmoid bone: present’ 2. Mastoid foramen: present (m; see k7) 3. Thoracic vertebrae: 14 or less 4. Femoral third trochanter: present 5. Astragalus: globular head, neck

distinct, keels developed’ n: Clade C:’

1. Premaxillary canal: present (W; see h I and VI)

2. Naso-lacrimal foramen: two foramina present (W; see ~2)

3. Transverse canal: present 4. Petro-tympanic fissure: present 5. Postparietal-postsquamosal foramina:

two to four or more 6. Astragalar foramen: present’

o: (see text under EPS for alternative arrangement): I. Lacrimal bone: facial flange large 2. SupragIenoid foramen: present 3. Mandibular foramen: dorsal to alveoli

line of cheek teeth 4. Coronoid process of dentary: does not

project dorsal to margin of rygomatic arch (D; see j3 and y5)

5. Patella: roundish; approximately ball shaped (m; see k9)

P: I Femoral patellar keels: medial is

knobby 2. Tibia-fibula: fused proximally and/or

distally (m; see x4) 3. Metacarpals and metatarsals: keels

present on distal articulating surfaces 4. Digits on manus and pedes: less than

five, even number on either or both appendages (m; see y7)

5. Astragalar groove: deep (W; see x5)

cl: I. Supraorbital foramen: present (w; see

v4) 2. Scapular acromion process: short or

absent (w; see i4) 3. Humeral intertubercular groove: deep,

almost semicircular 4. Thoracic vertebrae: I5- 18 (0; see m3)’ 5. Digits on manus and pedes: less than

five, odd number on either or both appendages

6. Astragalar foramen: absent (0; see n6) 7. Astragalus: nonglobular head

(0; see m5) r: Ungulata:

1. Mesethmoid bone: absent (0; see m 1)” 2. Jugal foramen: present (m; see h6

and sl) 3. Foramen magnum: formed by

basioccipital and exoccipitals (m; see i2)

4. Angular process of dentary: vestigial (W; see i3)

5. Scapula: infraspinous fossa larger than supraspinous fossa (m; see 83, w3, and zll)

6. Humeral, lateral, and medial condyles: distal ends articulate almost exclusively with the radius

7. Humeral entepicondylar foramen: absent (w; see g4 and z 12)

8. Ulna and radius: fused s: Glades D and E (see text under EPS for

alternative arrangements): I. Jugal foramen: present (m; see h6

and r2) 2. Spheno-frontal foramen (=sinus canal):

present (m; see 15) 3. Mandibular symphysis: not fused

(0; see d3) 4. Clavicle: present (0; see f2) 5. Humeral supratrochlear foramen:

present 6. Femoral third trochanter: at proximal

end of bone

Table 3 (continued)

7. Tibia and fibula: extensively fused especially along distal and medial shafts

8. Digit III: not the longest (m; see 16) t: Clade D:

Postglenoid process: present (W; see h4) Scaphoid and lunar: fused Baculum: present

Maxilla: contributes to rim of orbit (i.e., wedged between lacrimal and jugal) (m; see h2) Mandibular symphysis: fused (0; see s3 and d3) Humeral supratrochlear foramen: absent (0; see s5) Fibula-calcaneum contact: absent Astragalus-cuboid contact: absent (m; see j4)

v: (Note: It costs only three evolutionary changes to reconcile the Archonta hypothesis of Gregory ( 19 10) with the author’s morphological data (table 4B, 2):

Premaxillary canal: present (m; see nl and hl) Naso-lacrimal foramen: two foramina present (m; see n2) Naso-lacrimal foramen: on rim, neither within nor outside orbit boundaries Supraorbital foramen: present (m; see ql)

5. 6.

7.

8.

9. 10.

WI

1.

2.

3.

4.

5.

6.

7.

8.

Postpalatine torus: present Optic foramen: confluent with opposite side (m; see y2) Jugal: participates in mandibular fossa (m; see i6)f Stylo-mastoid foramen: in line with alveoli of cheek teeth Basisphenoid foramen: present a Hypoglossal foramen: two to three foramina (m; see 28)

Spheno-frontal foramen (=sinus canal): absent (0; see s2) Foramen rotundum: confluent with orbital fissure (m; see ~1)~ Scapula: infraspinous fossa larger than supraspinous fossa (m; see i-583, and zll) Forelimbs and hind limbs: notably long’ Scapular coracoid process: long and/or large Ulna and radius: fused (ulna greatly reduced) (see r8) “Ossified cartilages”: articulate with sternum Femoral third trochanter: absent (0; see m4)

x: Clade E: 1. Foramen rotundum: confluent with

orbital fissure (m; see w2)

Alisphenoid canal: present (m; see h3) Mandibular condyle: oriented anteroposteriorly or almost roundish Tibia-fibula: fused proximally and/or distally (m; see p2) Astragalar groove: deep (m; see p5)

y: Anagalida of McKenna (personnal communication); see also Novacek 1982):

5.

6.

7.

Squamosal (dorsal flange): contributes to rim of orbit Optic foramen: confluent with opposite side (m; see v6) Basioccipital foramen: presentj External auditory meatus: projects almost vertically from horizontal plane of cranium Coronoid process of dentary: does not project dorsal to zygomatic arch (m; see 04 and j3) Scapula: acromion process-long and thin; neck-long and narrow; spine- short (- */3- 3/4 of scapular length) Digits on manus and pedes: less than five, even number on either or both appendages (m; see p4)

z: Glires of Gregory ( 19 10): 1. Infraorbital foramen: anterior opening

in line with rostra1 end of premolars 2. Premaxilla-frontal contact: present 3. Spheno-palatine vacuity: present

4.

5. 6. 7.

Spheno-frontal foramen (=sinus canal): absent (0; see s2) Masticatory foramen: present Buccinator foramen: present Foramen ovale: confluent with foramen lacer-urn medium and/or petro-tympanic fissure

8.

9.

10.

Hypoglossal foramen: two to three foramina (U; see ~10) Mandibular foramen: ventral to alveoli line of cheek teeth (N; see 82) Medial angular process foramen: present k

11.

12.

13.

Scapula: infraspinous fossa larger than supraspinous fossa (m; see w3, r5, and 83) Humeral entepicondylar foramen: absent (m; see r7 and g4) Digit III: the longest (0; see ~8)~

NOTE.-Because the focus of this study is on the ordinal relationships within the infraclass Eutheria, synapomorphies are listed for Eutheria as a clade and only for categories above the ordinal level. Letters a-z refer to branching points on the cladogram in fig. 3. Unless indicated otherwise, listing of characters for each branching point (d-z) is not in order of importance but from anterior

ti to posterior end, beginning with the cranium. A total of 102 characters (counting parallelisms and reversals only once) is listed in this table, a difference of 80 from the 182 mentioned in the text.

w These 80 characters appear on branch points (a-c) and other points (e.g., intraordinal) not shown in fig. 3. Names of skull foramina and skeletal features are after Cope ( 1880), Gregory (19 lo), deBeer (1937), Romer (1966) Wahlert (1974) and references therein. n = Parallelism; 0 = reversal.

a After deBeer (1937, p. 442) for dl, ml, and rl; and after deBeer (1937, e.g., plate 109, [“th = hypophysical fenestra”]) for v9. b After Novacek (1982, p. 14) and references therein. These characters (6-l 1) are the only soft-anatomy characters; all the rest are nondental osteological characters. ’ After Doran (1876) and Novacek (1982, p. 14). d Paired. On ventral side of premaxillae between incisive foramen and interpremaxillary foramen, close to midline or on margin (new). ’ After Osbom (1942, p. 916). f Character distribution and method of analysis resulted in this character being a shared-derived by these taxa, even though it may be a shared-primitive when examined as an independent character

for Mammalia. Note that character m5 may be included under branch d. * Characters 1-5 are arranged in order of importance; characters 6-7 may be symplesiomorphic (shared-primitive). h Because of missing data, Condylarthra is a union of three extinct genera (Phenacodus, Arctocyon, and Mesonyx). i After Novacek (1982, p. 14). j Paired. On ventral side of basioccipital close to midline, found mostly in crania of juvenile and subadult specimens (new). k Paired. On medial side of dentary at anterior end of mandibular fossa and directed anteriorly (new).

234 Shoshani

Table 4 Selected Hypotheses and Their Scores (Tree Lengths) of Interordinal and Higher-Category Relationships within Eutheria

Phylogenetic Relationship(s) Tree Lengths

(EC)

A. Testing hypotheses of other workers (2-4): 1. Abbreviated version of fig. 3 (see fig. 4A) . . . . . . . . . . . . . . . . . 2. Simpson 1945 (see fig. 4B) . . . . . . . . . . . . . . . . . . . . . . . 3. McKenna 1975 and personal communication (see fig. 4C) . . . 4. Miyamoto and Goodman 1986 (see fig. 4D) . . . . . . . . . . . . . .

B. As in figs. 3 and 4A but with the following changes: 1. Pholidota joined to Carnivora . . . . . . . . . 2. Primates joined to the branch of Chiroptera-Dermoptera-Scandentia . . . . . . 3. Tubulidentata joined to extant Paenungulata (between Embrithopoda and

Hyracoidea) . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .,..... 4. Tubulidentata joined to Edemata . . . . . . . . . . . . . . . . . . . 5. Hyracoidea joined to Perissodactyla . . . . . . . . . . . . 6. Cetacea joined to Artiodactyla . . . . . . . . . . . . . . . . .

C. Interclade swapping (letters A-E in fig. 3): 1. SuccessivejoiningofcladesC,D,E,B,andA . . . . . . . . . . . . . . . . 2. Clade sets E and D, C and B join separately and the resultant branches

join together . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 3. Clade sets E and C, B and D join separately and the resultant branches

join together . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 4. SuccessivejoiningofcladesA,D,C,B,andE . . . . . . . . . . . . . . .

963 994 982 984

970 966

981 972 970 974

963

964

967 969

relationships after McKenna ( 1975) and Miyamoto and Goodman ( 1986), respectively. Other tests (table 4B) were conducted to accommodate current thoughts on mammalian phylogeny (see Discussion).

A more significant test, in terms of major clades within Eutheria, would examine interclade relationships. Stated otherwise, How many EC would be added to the original length of the tree if we rearrange the five major eutherian clades (A-E in fig. 3) such that members of each clade remained as a unit while “shuffling”? Table 4C shows that when we swap clades A-E in various combinations, it costs between zero and four additional EC, except when the order of joining of clades is reversed, in which case it costs six EC. The phylogenetic positions of members within clades are better supported than interclade relationships.

Evolutionary Rates

Evolutionary rates were calculated as EC/ 100 Myr. The EC values shown in table 5A clearly demonstrate alternating fast and slow rates of morphological evolution from the common ancestor of Cynodontia along the line of descent to Pan and Homo. Table 5B provides evolutionary rates from the common eutherian ancestors for selected eutherian orders over time ( - 85 Myr before the present [ Mybp]) to ancestors of each order (50-65 Mybp). These rates are followed by the rates from each order’s ancestor (50-65 Mybp) to the present. Comparisons of these two sets of rates show that a distinct acceleration at the base of Eutheria (except for Edentata) is followed by a steep deceleration during the next 65 Myr.


A B C D E

/ Condensed [Eutheria only]

/ After McKenna [1975 and Perr. Commd.

/ After Simpson [19451.

/ After Miyamoto and Goodman [ 19881

FIG. 4.-Alternative hypotheses for major branching patterns within Eutheria and their scores as obtained by branch swapping. Part A is a condensed version of fig. 3; terminal taxa A-E represent major clades in fig. 3. Elsewhere, letters in brackets imply some, but not all, members of that clade. Hypotheses tested in parts B-D are those of other authors (cf. table 4A).

Discussion IMDFN

Most of the IMDFN findings presented here or elsewhere (e.g., Dene et al. 1978; Goodman and Cronin 1982) have been corroborated by other studies using different data and methods of analysis (de Jong et al. 198 1; Goodman et al. 1982; Novacek 1982; Kleinschmidt et al. 1985). Thus, IMDFN, although a crude method with which to study phylogeny, is a valuable tool in providing working hypotheses.

‘(Living Fossils ”

“Living fossils” are species that reflect little morphological evolution since their divergence from their closest relatives and are usually the sole survivors of their lineages. Because living fossils retain many primitive characters, morphologists find it difficult

236 Shoshani

Table 5 Rates of Evolution from Eutheria Ancestor to Ancestor of Selected Eutherian Taxa to the Present

Evolutionary Period Age Rate”

(Mybp) (EC/100 Myr)

A. From Cynodontia ancestor to Pan and Homo: Cynodontia ancestor to Mammalia ancestor ................... Mammalia ancestor to Eutheria ancestor ...................... Eutheria ancestor to Anthropoidea ancestor ................... Anthropoidea ancestor to Homo-Pan ancestor ................ Homo-Pan ancestor to Pan ............................... Homo-Pan ancestor to Homo .............................

B. From Eutheria ancestor to ancestor of selected taxa to the present: b Eutheria ancestor to Edentata ancestor ....................... Edentata ancestor to the present ............................. Eutheria ancestor to Proboscidea ancestor ..................... Proboscidea ancestor to the present .......................... Eutheria ancestor to Perissodactyla ancestor ................... Perissodactyla ancestor to the present ........................ Eutheria ancestor to Primates ancestor ....................... Primates ancestor to the present ............................. Eutheria ancestor to Lipotyphla ancestor ...................... Lipotyphla ancestor to the present ........................... Eutheria ancestor to Rodentia ancestor ....................... Rodentia ancestor to the present ............................

250-200 36 200-85 17

85-40 60 40-5 37

5-o 0 5-o 100

85-60 16 60-O 35 85-55 90 55-o 27 85-55 113 55-o 20 85-60 84 60-O 23 85-65 90 65-O 25 85-55 120 55-o 60

a Calculated from augmented link lengths obtained by the computer program of Goodman et al. (1982). For simplicity, these link lengths were not incorporated in fig. 3 (see examples in Goodman et al. 1982 and Shoshani et al. 1985~). The reader can, however, calculate relative rates (not exact values as given in this table) by counting the number of synapomorphies along a given line in fig. 3 and dividing that number by the time required for these changes to take place (middle column). For example, for Rodentia, the number of synapomorphies along the line from branch point e to point z is 40 (from table 3), and the rate is 133.3 (85 - 55 = 30 and 40/0.30 = 133.3). Similarly, for Perissodactyla the rate is 126.6. (Details have been omitted here; they can be obtained from the author.)

b Average rate from Eutheria to a taxon is 70.5; average rate from a taxon to the present is 3 1.6.

to ascertain their phylogenetic position; thus, new opportunities for insight can come from molecular biologists. Some excellent examples of vertebrate living fossils are the tuatara (Sphenodon punctatus, Rhynchocephalia, Reptilia), aardvark (Orycteropus afer, Tubulidentata, Mammalia), and tarsier (Tarsius spp., Primates, Mammalia). The latter two examples are of direct interest.

Early workers placed Orycteropus within the order Edentata, including Pholidota, but most recent workers consider Tubulidentata to be a condylarth derivative (see Simpson 1945 and Patterson 1978 for summaries). Thewissen (1985), however, chal- lenges this latter hypothesis on morphological grounds. Molecular studies such as those of de Jong et al. (198 1) and Shoshani et al. (198 1) place Tubulidentata close to Proboscidea, Sirenia, and Hyracoidea (and also show Pholidota close to Carnivora). Dene et al. (1983) concluded that the aardvark lineage is “one of the most ancient among Eutheria.” Data based on nondental osteological characters presented here show Tubulidentata as a sister group to the condylarth derivatives Ungulata (Artio- dactyla and Perissodactyla) and Notoungulata. The phylogenetic position of Tubuli- dentata is far from being resolved.


Debate over the relationships of Tars&s within Primates also continues. It has been placed in a separate suborder, close to either higher primates (Haplorhini) or lower primates (Prosimii) (see Simpson 1945 for details). Molecular studies (e.g., Goodman and Cronin 1982, and references therein) concluded that Tarsius is more closely related to higher primates than to prosimians. Analyses of osteological data by this author also place Turks close to higher primates (relations within Primates are not shown).

The Hyracoidea Controversy

The phylogenetic position of Hyracoidea has been the subject of continuing controversy for over 200 years; hypotheses suggested include relationships to Rodentia (Storr in 1780 and Cuvier in 1798), to Notoungulata (Ameghino in 1897 and Stromer in 1926), to Proboscidea and Sirenia (e.g., Gill in 1870, Gregory [ 19101, Simpson [ 19451, Romer [ 19661, de Jong et al. [ 19811, Shoshani et al. [,1981], Rainey et al. [ 19841, and Kleinschmidt et al. [ 1985]), and to Perissodactyla (e.g., Gaudry in 1862, Owen in 1868, Frechkop in 1936, Whitworth in 1954, McKenna [ 19751, and Fischer [ 19851) (earlier references that are not included in Literature Cited can be found in Simpson [ 19451, McKenna [ 19751, or Novacek [ 19821).

All molecular studies (de Jong et al. 198 1; Shoshani et al. 198 1; Rainey et al. 1984; Kleinschmidt et al. 1985; R. E. Benveniste, personal communication) agree that Hyracoidea is related to Proboscidea and Sirenia (extant Paenungulata of Simpson [ 1945]), whereas morphological studies (the remaining references above) differ in their conclusions. Evidence presented in both molecular and morphological aspects of this study and independently in the morphological work of Novacek and Wyss (1985) support the Paenungulata hypothesis of Simpson (1945).

Equally Parsimonious Solutions

A total of 18 equally parsimonious solutions (EPS) was generated by the computer programs; three of these solutions are indicated by the trichotomy at branch e in figure 3. Thus, (1) Edentata can join the rest of Eutheria, leaving Pholidota as an outgroup to the rest of Eutheria, (2) Edentata can join Pholidota, or (3) Pholidota can unite with the rest of Eutheria, leaving Edentata as the most ancient branch of Eutheria (see McKenna 1975 for hypothesis [ 31; see testings of other hypotheses in table 4). Of the remaining 15 possibilities, 10 EPS were intraordinal (seven within Primates, two within Perissodactyla, and one within Rodentia), and the rest were interordinal. These five interordinal EPS were: (l-2) changes within clade B in figure 3 ([l] Dinocerata and Embrithopoda joined or [2] Embrithopoda and Hyracoidea exchanged places) (these EPS were not incorporated in figure 3 because evidence from the literature [e.g., Simp- son 1945; de Jong et al. 198 1; Shoshani et al. 198 l] supports the relationships shown in figure 3); (3) within clade C in fig. 3: Tubulidentata and Pantodonta exchanged places (not shown in fig. 3 following the hypothesis suggested by McKenna [ 1975, and personal communication]); (4) subclade Chiroptera-Dermoptera-Scandentia joined clade E in figure 3 (this possibility is not shown since works of Gregory [ 19 lo], McKenna [ 19751, and Dene et al. [ 19781 indicate close affinity of Primates to the Chiroptera-Dermoptera- Scandentia branch per the Archonta hypothesis of Gregory [ 19 lo]; see also table 4B); (5) clades D and C joined (this alternative is not supported by any studies; in contrast, relationships shown in fig. 3, or the joining of clades C and B, are supported by, e.g., McKenna [ 19751 and Novacek [ 19821: see table 4C2).

238 Shoshani

Comparisons of Morphological versus Molecular Results

Relationships and rates within Eutheria. -Tables 6 and 7 summarize comparisons of relationships and rates of evolution within Eutheria. Relationships between Cetacea and Ungulata were discussed by Shoshani et al. (1985a). A glance at table 6 shows a considerable correspondence between amino acid sequence, IMDFN, and osteological relationships. The disagreements include the sister group of Pholidota (Edentata osteologically but Carnivora molecularly) and the sister group of Tubulidentata (Ungulata and Notoungulata osteologically but Paenungulata molecularly).

The similarities of evolutionary rates resulting from the two studies are clearly evident (table 7). In both, we note a burst of acceleration of rates at the base of Eutheria toward the ancestors of eutherian orders. This acceleration is followed by an uneven deceleration within the orders themselves during the Tertiary period. An explanation for this pattern (Goodman 198 1) is that the rapid rate of evolution during the end of the Cretaceous period was produced in response to selective .pressures for adaptation to the newly available niches vacated by the most recent extinctions. Once adaptive radiation took place, selection for preservation and improvement of traits followed and resulted in decelerated evolutionary rates.

Summary of Observations: Molecular versus Morphological Data

The underlying principles of PAUP (after Swofford 1984) and GMPM (after Goodman et al. 1982) are very similar; both programs aim to minimize homoplasy in phylogenetic reconstruction. Differences stem from some of the technical details of achieving that goal, and each of these MP methods has its advantages and disad- vantages. Table 8 includes a summary of general observations comparing morphological and molecular methods.

After applying both methods (PAUP and GMPM) to the morphological data, the author feels strongly that criticism of the GMPM arises, to some extent, because critics are unfamiliar with details of the program. The GMPM program may not have

Table 6 Comparisons of Relationships within Eutheria

Taxon: Evolutionary Relations Amino Acids

(IMDFN)* Osteological

Edemata: at the root of tree . . . . . . . . . . . . . . Yes (N) Paenungulata: Proboscidea, Sirenia, and Yes (Y)

Hyracoidea group together . . . . . . . . . . Tubulidentata: close to . . . . . . . . . . . . . . . . . . Paenungulata and Ungulata-separated . . . . Cetacea-close to condylarth derivatives . . . . Archonta-Camivora: close to each other . . . Rodentia: close of Lagomorpha . . . . . . .

Paenungulata (Y) Yes (Y)” Yes, with Ungulata (Y) Yes, overall (Y) Yes, overall (N)

Yes, with Pholidotab Includes Desmostyliac

Ungulatad Yes Yes, with Paenungulata Yes, overall Yes, and to

Macroscelidea

NOTE.-Amino acid sequence results after Miyamoto and Goodman (1986). ’ (N) = Not corroborated by the IMDFN study; (Y) = corroborated by the IMDFN study. b Pholidota with Camivora in molecular studies. ’ See Domning et al. (1986) for differences in relationships. d Perissodactyla and Artiodactyla. ’ Not in alpha and beta hemoglobin study of Shoshani et al. (198%~).


Table 7 Comparison of Evolutionary Rates Within Eutheria

RATE

TIME SPAN

Overall: uneven rates . . . . . . . . . . . . . . . . . . . . . . . Ordinal level:

Amino Acid

Uneven

Osteological

Uneven

Eutheria ancestor to ancestors of eutherian orders . . . . . . Acceleration Acceleration” Ancestor of eutherian orders to the present . . . . . . Deceleration Deceleration

* Except for Edemata, in which the rates are reversed (see table 5B).

all the options that other programs have, but its important asset is that when many alternatives are tested, the possibility of missing a tree that is shorter than the most parsimonious tree is reduced further and further with each try. Shorter trees usually depict changes within an order or a family, and the overall branching pattern of a class, such as Mammalia, remains unchanged.

Conclusions

Results presented here show that the “bushy” part at the root of Eutheria, initially comprised of 24 branches (orders and taxa), may be condensed into five major branches (clades A-E in fig. 3). Thus, a major objective of this study-that is, to shed light on the “bushy” part of Eutheria- has been accomplished. Some of the relationships within clades A-E in figure 3 are also corroborated by the results from IMDFN (fig. 2) and from amino acid sequences (Miyamoto and Goodman 1986); pertinent hypotheses

Table 8 Summary of General Observations: Morphological vs. Molecular Data

Subject Morphological Molecular

Distance from genetic code . . . . . . . . . . . . . . . . . Taxa that can be studied . . . . . . . . . . . . . . . . . Numbers of individual specimens examined per

species . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Number of characters that can be examined . . Investigator’s input can be or is . . . . . . . . . . . . . . . Ability to determine polarity of a specific character . Resolving power of phylogenetic trees , . . “Global” branch swappingd . . . . . . .

Removed Extant and extinct Few, several, or more

Fewer Subjective YesC Betterc By the computer program

Close Extant only One, rarely

twoa More b Objective b No’

C . . . “By hand”d

NOTE.-Observations are not limited to PAUP (Swofford 1984) and GMPM (Goodman et al. 1982). ’ Because of the lengthy process involved. In small samples variations cannot be detected. b Automation enables gathering of large amounts of sequence data in a relatively short time without human input, whereas

collecting morphological data can involve subjective descriptions of a process on a bone, such as “small,” “medium,” “large,” or “absent.”

c As many as 20 character states are possible for one amino acid position, a situation that makes it impossible to determine the transformation series of a character. Polarity can be determined (in most cases) on morphological characters, and thus they yield more phylogenetic information and have better resolving power, especially when the ontogeny and phylogeny of a lineage is well documented in the literature.

d Pertains to PAUP and GMPM. The GMPM (Goodman et al. 1982) performs local, not global, branch swapping. Therefore, alternative hypotheses (edited versions generated by the local branch swapping) are submitted by the investigator to the computer to get the scores.

240 Shoshani

are tested as shown in table 4. Independent corroboration of certain relationships depicted in figure 3 was presented by Novacek and Wyss (1985). Other workers (e.g., Gregory 19 10; Simpson 1945; McKenna 1975, and personal communication) also support some of the relationships presented here. I conclude that there are more similarities than dissimilarities between morphological and molecular data sets and that, as demonstrated in table 6 (relationships within Eutheria) and table 7 (rates of evolution), each approach complements the other (table 8).

Acknowledgments

Foremost, I thank my Ph.D. committee for their help and patience, especially M. Goodman for his mentorship and guidance. The many individuals and institutions who helped me obtain blood and tissue samples have been acknowledged in the papers by Shoshani et al. ( 198 1, 198%) or are being acknowledged in my Ph.D. dissertation. The help received from the staffs and curators of the museums where the osteological data were collected (see listing of museums under Material) has been invaluable. Other museums not mentioned here are acknowledged in my dissertation. I thank R. J. G. Savage and D. P. Domning for providing answers concerning some characters of Barytherium and Prorastomus, respectively. Special thanks also to D. B. Buchanan, D. P. Domning, M. C. McKenna, E. Manning, M. J. Novacek, G. Overbeck, J. G. W. Thewissen, W. L. Thompson, and J. Wahlert for stimulating discussions, promoting a better understanding of certain osteological characters, and/or making comments to improve the manuscript (Domning, in particular, made meticulous and valuable comments). D. A. Walz helped to purify albumins, J. Czelusniak has been helpful with the computer analyses of the immunological and osteological data, and M. M. Miyamoto introduced me to the PAUP program and helped me get started. Heartfelt thanks also to those individuals who helped me understand the mechanics of and resolve many problems while working on PAUP: D. L. Swofford (who wrote this computer program), A. G. Kluge, W. L. Fink, and J. S. Farris.

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WALTER M. FITCH, reviewing editor

Received December 23, 1985; revision received January 29, 1986.

mammalian phylogeny: comparison of morphological and ... · mammalian phylogeny: comparison of...

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