MAMMALS AS A KEY TO EVOLUTIONARY THEORY
ELISABETHS. VRBA
YaleUniversity,
Department
of Geologyand Geophysics,
P.O.Box 6666, NewHaven,CT 06511
at the70thAnnualMeetingof
Presented
Address,
Keynote
The American Society of Mammalogists, Frostburg,MD, June 1990
Mammalogy provides exceptionally fertile groundsfor advancingevolutionarytheory, because its data base spans from diverse researches on living forms to a rich fossil record. I
illustratethis by integratinginterdisciplinaryevidenceand hypothesesin the habitat theory,
including:1) the context of paleoclimaticchanges, and how species' distributionsresponded
to them;2) geographicalbiases in turnoverrates of species;3) the turnover-pulsehypothesis;
4) breadthof resourceuse as a cause of phylogeneticturnoverrates. Preliminarytests using
the late Neogene recordsof the Americasand Africa suggest that majoraspects of the Great
American Interchange have parallels in the African record, as predicted by the habitat
theory.Comparableforces may have operatedin both cases. The habitat theory of the Great
American Interchangediffers from the traditional emphasis on the effects of interspecific
competition.
Key words: mammals, evolution,climate, America, Africa
"The advance of science is not due to the
fact that more and more perceptual experiencesaccumulate. ... Bold ideas, unjustified anticipations, and speculative
thought, are our only means for interpreting nature" (Popper, 1968:280).
It is not in vain that the Cenozoic is called
the age of mammals:The massive Cenozoic
diversificationof mammals offersabundant
information on fossil history and on a diverse modem biology. I will be "mammalocentric" and suggest that today we are in
a particularlyfavorableposition to originate
bold new evolutionary hypotheses and to
test them. In this light, the opening quotation may seem paradoxical,because it was
Popper who arguedthat, because biological
evolution is a unique historical process,
evolutionary hypotheses are untestable. In
my view he was wrong on this point, and
correct in his later recantation (Popper,
1978). Others have arguedfor testable evolutionary hypotheses, with good examples
(e.g., Williams, 1973, 1982).
J. Mamm., 73(1):1-28, 1992
Nearly three centuries ago Isaac Newton
delivered his famous dictum "hypotheses
non fingo" (I frame no hypotheses). For a
long ensuing period the invention of hypotheses was regardedas a suspect activity-incompatible with scientificcautionand
rigor. Whewell (1847) early on argued differently, that "the process of scientific discovery is cautious and rigorous,not by abstainingfrom hypotheses, but by rigorously
comparing hypotheses with the facts, and
by resolutely rejecting all which the comparisondoes not confirm."Today it is widely accepted (following Popper, 1968) that
science progresses by hypothetico-deductive reasoning,and Medawar's(1967) words
are still current:"hypothesisno longertows
'gratuitous,''mere' or 'wild' behind it, and
the pejorative usage ('evolution is a mere
hypothesis' ...) is one of the outwardsigns
of little learning"(p. 139). "This imaginative element in science is one of its chief
glories" (p. 142).
What is the secret, the logical path to hypotheses of process, and of rules and laws
1
2
JOURNAL OF MAMMALOGY
governing processes? "There is no logical
path," said Albert Einstein in his address
on Max Planck's 60th birthday(in Popper,
1968:32), "they can only be reachedby intuition, based on something like an intellectual love of the objects of experience."
Everyone agrees that intuition and inspiration are important,and that in some way
these arisefrom the "objects"of experience,
namely the rangeof facts and ideas that one
encounters. Some famous hypothesizers
found fertile ground for their intuitions at
the intersection of experiences from different fields of knowledge. Consider that
Darwin's (1859) bold new ideas reconciled
elements from the works of a social demographer(ThomasMalthus),a statistician
(Adolphe Quetelet), and an economist
(Adam Smith).
Few people articulatehypotheseswith the
scope of Darwin'smajoridea. Nevertheless,
if true that the juxtapositions of ideas and
data from largely independent studies can
inspire new hypotheses, then mammalogy
is surely a marvellous substratefor discoveries within the evolutionary paradigm.In
total range and strength, mammalian researchis unrivalledin biology. Contributing
to this are the intensive studies of ourselves
and our domestic animals. Data on mammals span exceptionallyrich ecological and
phenotypic ranges, extending to complex
behavior. Whereas, in these respects, researcheson mammals are rivalled by those
on birds and insects (and whereasno mammal breeds as quickly as Drosophila), ornithologists and entomologists can see only
a tiny fraction of the morphologicalpanorama through long time that the mammalian fossil record affords.
I illustratethis, in a preliminaryand modest way, by cross-disciplinary hypotheses
that emphasize how species relate to their
habitats, and how they respond to habitat
alterationinitiated by physical change. Together these hypotheses form a compatible
theory, referredto as the "habitat theory"
(E. S. Vrba, in litt.). It offersan alternative
to the competition paradigm,namely to the
Vol. 73, No. I
traditional emphasis on interspecies competition as a cause of extinctions and on
empty niches as akin to magnetsthat attract
species' origins (reviews in Benton, 1983;
Martin and Klein, 1984; Vrba, 1985).
Many historicextinctionson islandsseem
to have been causedby purelybiotic factors:
competitive exclusion of native species occurred in the absence of notable physical
changes, after human introductions of invading species (Brown, 1989; Diamond,
1984). I doubt the importanceduringlife's
history of such purely biotic initiation of
true (not merelylocal) extinctions,and I am
even more skepticalof the initiatingrole of
empty niches in phylogeneticradiation (E.
S. Vrba, in litt.). Instead of expanding on
reasons for such doubts, I here focus on the
alternative representedby the habitat theory.
Subpartsof the habitat theory have had
a long history within the theories of others,
who include Lyell (1842) on initiation of
species' origins and extinctions by geological changes,Mayr(1963) on the importance
of allopatry in speciation, Croizat et al.
(1974) on vicariance biogeography, Eldredge and Gould (1972) on punctuated
equilibria, Coope (1979) on constant habitats of species in driftinggeographicdistributions, Paterson(1982) on the relationship
between species' habitats and their fertilization systems,and Haffer(1982) on refuge
theory.Certainorientations(especiallysome
extreme ones) within each of these theories
are not requiredby the habitat theory. The
partsthat are used are put togetherin a new
way. Some of the component hypotheses
and evidencearevariouslydiscussedin Vrba
(1980, 1985, 1987a, 1988; Greenacreand
Vrba, 1984). While I here discuss the habitat theory with particular reference to
mammals, I suggestthat its basic principles
may apply to other organismal groups as
well.
It is fairto pick the best examplesclaimed
by a paradigmif one wants to challenge it
by an alternativeview. Fossil case histories
in which one major organismalgroup de-
February1992
VRBA-MAMMALS AND EVOLUTIONARYTHEORY
clined as another radiated are common.
Some of these are widely accepted as evidence for the importanceof competitionand
empty niches (reviewed in Benton, 1983),
such as the replacement of dinosaurs by
mammals, and of marsupialsby placentals
duringthe GreatAmericanInterchange.Because the latter is often cited as the best
example for the competition paradigm, I
use it to explore the habitat theory. But first
I recallsome old ideas on habitatspecificity,
and introduce recent paleoenvironmental
results,which togetherprovide a context for
evolution.
HABITATS
A habitat is a place that contains the resources necessaryfor life of an organism or
species. A given species' habitat may include places that are unoccupied by that
species.This follows Davis (1960:538):"The
blood stream of man is suitable for malaria
parasitesand constitutes a habitat for them
beforeinfectiontakesplace."In analogywith
Hutchinson's (1957) distinction, the fundamental habitat of a species includes all
the places,plus necessaryresources,in which
a species can live, and the realized habitat
at a given time includes all those in which
it does live. The concept is time specific:
with climatic changes a species' habitat
patchesin particularareasmay shift, shrink,
disappear,appear,and expandthroughtime.
-An axiAll speciesare habitat-specific.
om for the habitat theory is that all species
have limited habitat specificities. Although
species may be flexible in the range of habitat components--the
resources--under
which they can live, no species can live in
all life-supporting environments on earth.
My present focus is on the habitat specificities of terrestrialmammals.
The limits, with respect to variables such
as temperature,rainfall,substrate,food, and
vegetation cover, of a species' habitat specificity can in principle be estimated and
quantified. For instance, N. Caithness (in
litt.) used multivariate discriminant-function methods and bioclimatic-profile
3
matching (Nix, 1986) to estimate such limits for each of 73 species of Africanantelope,
in terms of 12 temperature- and rainfallrelated variables. He found high climatic
predictability from area to area within the
same species' distribution.
In a different approach, we used correspondence analysis on antelope census data
from areas representing different ecosystems across subsaharanAfrica (Greenacre
and Vrba, 1984). This method does not presume any causal structure underlying the
data. Instead, any nonrandom structureis
revealed afterwards.In our study, we comparedthe distributionoftaxa and areasalong
the principal axes with supplementaryenvironmental variables for each game area,
including mean annual rainfall and temperature,soil nutrientstatus,and vegetation
cover coded from low to high proportions
of wood cover comparedto grasscover. We
found (Fig. 1) thatthe vegetationcover codes
plot in almostperfectascendingorderagainst
axis 1: among the variables we considered,
grossvegetationalphysiognomy
(notdefined
by plant species, but by wood-to-grassproportions) was pinpointed as primaryin the
habitat specificities of the antelopes.
Cladistic relationshipsin Fig. 1 are based
on mitochondrial DNA (J. Gatesy, pers.
comm.) and skull characters (e.g., Vrba,
1979). They suggestthat within broadlimits
vegetationalhabitat specificitiescan be heritable and characteristic for entire clades
through millions of years. For instance, all
eight species in the reduncineclade (Kobus,
Redunca) are in the open woodland part,
and all seven in the alcelaphine clade (Alcelaphus,etc.) are in the open grasslandpart
of the vegetation spectrum. Each clade is
known since at least 5 million years ago
(Vrba, 1987a). In fact, the distributions of
habitat characters among taxa form hierarchicallynested sets and subsets. Using the
same reasoningconventionallyemployed in
cladistics, I suggestthat habitat specificities
can be heritablefrom species to species, and
for entire clades, just as can phenotypic
characters. (I am aware of arguments that
4
JOURNALOF MAMMALOGY
AXIS 1
),=0.67
Vol.73, No. 1
often is discussedin terms of generalistsand
specialists with respect to some resource
4CEPHALOPHUS
--16
category. For instance, euryphagyand stenophagy refer, respectively, to broad and
narrowtolerance of food resources,that is,
L1 to the greater or lesser variety of foods or
food species that the organisms eat. A particularlyimportant contrastis that between
eurybiomicand stenobiomic species (Vrba,
1987a). The term biome has been applied
mostly to distinctive communities on land,
SERENGETI -although also to marine ones. Biomes of
land mammals are characterizedby gross
I GAZELLA- 12 2
NGORONGORO
vegetational physiognomy, precisely the
habitat variable that emerged as important
to antelopes (Fig. 1). Thus a stenobiomic
species is restricted to a particularbiome,
implying in the terrestrial case a narrow
range of vegetation physiognomy, while a
1
ANTIDORCAS
eurybiomicspeciescan use resourcesin more
than one biome.
The concepts of generalist and specialist
make sense only when specified in relation
FIG. 1.--Census analysis of extant antelopes to particularresources,becauseeach species
in 16 African areas by correspondenceanalysis (and each organism within it) commonly
(Greenacreand Vrba, 1984) resulted in axis 1 has a mosaic of specializations and gener(center).Among several variables for the areas, alizations, although one category usually
vegetationcover (left)correspondedmost closely predominates.Of primaryimportancein the
with axis 1, showingthe preeminentinfluenceof
habitat theory is not so much the contrast
this habitat variableon antelope ecology. Com- between specialists and generalists,but the
parison with independently-generated cladodistribution of resource patches across the
grams (right) suggests that vegetation habitat- historical environmental range of phylogespecificities have been heritable characteristics nies. For
example, most ecologists (e.g.,
(synapomorphies)for some entirecladesthrough
Smithers,
1985) would describe the aardmillions of years.
vark, Orycteropusafer, as stenophagous(it
feeds exclusively on ants and termites), as
a substrate specialist (it digs burrows only
characterdisplacementthroughinterspecif- in sandy or clay soil), and as stenophotic (it
ic competition should result in long-term is nocturnal).Yet the aardvarkis eurybiomchange in habitat specificities [e.g., review ic: its specialized "resourcepatches" range
in Begon et al., 1990]. Nevertheless, I sug- from semidesert to dense, moist woodland
gest that the alternative hypothesis of net across Africa. Nevertheless, in most herbivores euryphagyis associated with euryconstancy is viable and testable.)
Breadth of habitat specificity.-While re- biomy, and stenophagy with stenobiomy
lated species and clades may share habitat (Vrba, 1987a).
characters, they often differ heritably in
PALEOCLIMATIC
CONTEXT
breadth of habitat specificity (Eldredge,
1979; Rensch, 1959; Simpson, 1953; StebThe Milankovitch climatic cycles. - Globbins, 1950; Vrba, 1980, 1984). This subject al temperature changes over the past 65 mil-SYNCERUS
I
AEPYCEROS --
1
MANYARA
KRUGER
QUICAMA
WANKIE
HLUHLUWE
CUELEI
OUREBIA
REDOUNCA
1-3
4
KAFUE
NAIROBI .
ALCELAPHUS -
I
CONNOCHAETES-3
DAMALISCUS -3
KALAHARI
ETOSHA
LAKE TURKANA
VEGETATIONCOVER
LOW
z
MEDIUM
-f,
GAME
A
AREAS
AS
.
ANTELOPE
GENERA
,A
NOS. INDICATE
LIVING SPECIES PER
PHYLOGENETICBRANCH
February 1992
VRBA-MAMMALS
AND EVOLUTIONARY THEORY
lion years, the age of mammals, based on
the deep-sea record show large fluctuations
in a strong net cooling trend (Prentice and
Matthews, 1988). For such parts of the record where the data have sufficient resolution, smaller excursions in the form of periodic cycles are evident, as exemplified by
the regularalternations of glacials and interglacials, associated with summer sunshine cycles, duringthe Pleistocene (Fig. 2).
It is now generallyaccepted (e.g., Bergeret
al., 1984) that Earth's paleoclimate cycled
periodically between global cooling and
warming due to astronomical causes, although not always accompanied by polarice changes.ThreeMilankovitchcycles have
been documented: of about 100,000-,
40,000-, and 23,000-year periodicities.The
composite oxygen-isotopecurve for benthic
foraminifersfrom many partsof the world's
oceans in Fig. 3 represents the global climatic record over the past 6 million years.
The best evidence from the Pliocene and
Pleistocene shows that the cycles were accompanied not only by large-scale expansion and retreatof ice at the poles (Denton,
1985; Hays et al., 1976; Shackleton et al.,
1984), but also by major climatic and vegetational changes in the terrestrialtropics
(review in Rind and Peteet, 1985). African
evidence rangingfrom the East Africanlow
latitudes (Flenley, 1979; Hamilton, 1982;
Livingstone, 1975) all the way to the South
African Cape (Vogel, 1985), shows that the
last glacial maximum was substantially
colder than today (by 5-60C)and more arid,
with more-reducedforests and more-widespread grasslands. During the Holocene,
warmer and wetter conditions with higher
wood-to-grassratios than at present are reported from many African areas, especially
9,000-6,000 years ago (Vogel, 1985). Comparabledata from the earlierAfricanrecord
are discussedbelow. Similarcorrelationsare
evident from Pleistocene tropical strata in
Asia (e.g., Loffler, 1975; Walker and Flenley, 1979), Hawaii (Porter, 1979), and
America (Bradbury et al., 1981; Deevey, in
Lewin, 1984; Leyden, 1984; Prance, 1982).
5
THREE IPACEMAKERSIOF THE MILANKOVITCH
CLIMATE CYCLES
a
21.5 DEGREES
24.5 DEGREES
EARTH
OCSUN
10
. 200
Uo
--
-....-.-
mIIIV
Vz ii
:•
•:•.......
------0
S400VIV0
500
ICE VOLUME
GLACIAL CYCLES
800
900
1000
SUMMER SUNSHINE
(Cal/cm2/day)
FIG. 2.--Milankovitch cycles, ca. 100,000-,
41,000-, and 23,000-yearslong, resultrespecfromchanges
tively, a, fromthreepacemakers:
in orbitaleccentricity,
andin tiltandorientation
of earth'sspin axis. b, Changesin volume of
Earth'sice sheets.c, The effectof the intensity
of summersunshineat highnorthernlatitudes;
adaptedfromBroeckerand Denton(1990).
A high-resolution pollen record from the
high plain of Bogota, Colombia, covering
the past 3.5 million years, was found by
Hooghiemstra(1984) to correlatewell with
the deep-sea recordof Milankovitch cycles.
Longer-term climatic shifts.--These cycles, in some form, must have accompanied
the entire history of life (see Olsen, 1986,
for Triassic; Park and Herbert, 1987, for
Cretaceous). So far we have data only for
small parts of the fossil record. These show
that over longerperiods (one to several million years apart)there were major changes,
apparently due to tectonism, in the mean
and mode of these cycles and in polar-ice
volume.
6
JOURNALOFMAMMALOGY
Vol.73, No. I
1.5
<
2.0
Lu
w
<
2.5
,
)
Mz
3.0.w
0
3.5
DD
1
o
L
By convention,180/160 ratiosare reportedas
CO 4.0
6180=0
(180/160)sample- (180/160)REFERENCE
180=1008x16
1
1
2
3
-
0/ O)REFERENCE
4.511
0
,,,
LU
4
5
1
6
MILLIONSOF YEARS AGO
curvefor benthicforaFIG.3.--Globalclimaticchangeindicatedby a compositeoxygen-isotope
minifersfrommanymarinelocalities(adaptedfromVrbaet al., 1989).REFERENCE
in theformula
refersto the standardfor comparisonof oxygen-isotopic
ratiosamongcalcitesamples;it is PDB,a
belemnitefromthe Pee Dee Formation,SouthCarolina.
For example, duringthe past 3.5 million
years, there were two majorintensifications
of the cyclic cold extremes. The earlierone,
near 2.5 million yearsago, is evident in Fig.
3. It has been documented in areas around
the world, both in the oceans (Shackleton
et al., 1984; Thunell and Williams, 1983)
and on continents (see South American evidence in Hooghiemstra, 1984, and review
of data from all continents in Vrba et al.,
1989). Some modellingexperimentssuggest
that this event near 2.5 million years ago
was influenced by changes in ocean-atmosphere circulation patterns that were precipitatedby Panamaclosure(Maier-Reimer
et al., 1990). At this time the Arctic became
extensively glaciated (Shackleton et al.,
1984),with globalcooling(Vrbaet al., 1989).
A later period of major cooling intensification, variously suggested to have occurred between 0.9 and 0.7 million years
ago, may have been causally influenced by
uplift of western North America and of the
Himalayas and the Tibetan Plateau (Ruddiman et al., 1986). Ruddimanand Raymo
(1988) investigatedthe strengthand timing
of cyclic effectson the deep-sea recordover
the past 3.5 million years. They concluded
that between about 3.5-2.4 million years
ago the effectswere minimal, from 2.4 million years until 0.8-0.7 million years ago
the 41,000-year cycle dominatedwith moderate amplitude, and since then the highamplitude 100,000-yearcycle gained dominant power.
Climatic effects on species.--The Milankovitch climatic changeswere large(at least
for some periods and areas) relative to the
habitat adaptationsof most extant species.
And the less frequentchangesin cyclic mean
and mode must have been even more
stronglyfelt by the biota. Fig. 4 show some
possible kinds of consequences for species
throughone climatic cycle. Species may respond by undergoingno net change at all:
they may persist without branching, and
February1992
7
THEORY
AND EVOLUTIONARY
VRBA-MAMMALS
SPECIES PERSISTANCE
WITHSTASIS
WITHINTRA-
SPECIES
EXTINCPERSISTANCE
S P E C I A T IO N
TION
SPECIFIC
EVOLUTION
Sa
b
c
d
e
f
g
-
x LATITUDE
AT
tM
VI
ATTIME
T1
to environmental
of responsesof speciesandtheirdistributions
FIG.4.- Thethreecategories
change
aresummarizedin this hypotheticaldiagram:a, b, c, speciespersistence,withor withoutvicariance
and latitudinalshiftingof the distribution;
d, extinction;e, f, g, speciation.The climaticexcursions
indicatedcan represent,for instance,coolingto the left andwarmingto the right.
with no (or negligible) distribution change
(Fig. 4a). Species may respond by one of
three kinds of change that are represented
in all macroevolutionaryhypotheses,as they
are in the hypotheses of the habitat theory.
The first one is passive: they may respond
only by vicariance or shifting of their distributions, without branchingor extinction
(Fig. 4b and 4c). Then there are two kinds
of active responses with noticeable macroevolutionary results. Species can undergo
vicariance to the limit, namely become extinct (Fig. 5d). Or, vicariance can result in
speciation (Fig. 5e, 5f, and 5g).
I refer collectively to all distribution
movements (Fig. 5b-g) as distributiondrift.
The processes that bring about allopatryof
populations, by vicariance or by dispersal
over barriers, are a crucial element in the
habitat theory. Under the present view, a
phase of allopatryis the necessaryprecursor
to both speciation and extinction (Fig. 5dg), allopatrymostly resultsfrom vicariance,
and allopatry by vicariance is always initiated by physical environmental change. I
have argued that even most dispersal over
barriers is initiated by physical environmental change (E. S. Vrba, in litt.). Let us
first consider the passive response of distribution drift with simple unbranching
persistance, that is, without either speciation or extinction (Fig. 4b and 4c).
CONSTANTHABITATSOF SPECIESIN
DRIFTING DISTRIBUTIONS
Paleontological estimates of species' durations are minimum estimates based on
how long particular morphologies remain
relativelyunchangedand distinct in the record. The average duration of terrestrial
mammalianspecies is estimated to be about
2 million years (personalobservation of the
African record; Stanley, 1979), and longer
for many other taxa (Stanley, 1979). Cli-
8
Vol.73, No. 1
JOURNALOF MAMMALOGY
WARMER
------
COOLER
'
-
d
got.'j..L
:;
"'
A "4
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FOIRE5ST
(CLINIAT' II
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FIG.5.--Distributiondriftexemplifiedby a transectthroughan Africanareaand throughtime.
Thishypothetical
andhabitatsof speciesin fouradjacentbiomesdrifting
diagramshowsdistributions
over geography(left)as climatechanges(right).The horizontalaxis for the biome transectin this
examplecanrepresentequatorialto higherlatitudesfromrightto left.
matic and vegetationalchangesof largescale
(at least for some known periods, as reviewed brieflyabove, and more extensively
in Rind and Peteet, 1985, and Vrba et al.,
1989) swept back and forth over continents
with periodicityabout 1/20th, or less, of the
durationof the averagemammalianspecies.
This raisesthe question how the species survived as long as they did.
Hypothesis1: Most known species survived
many climatic cycles by the passive response of geographicshifting and vicariance of their distributions, while maintaining habitat fidelity.
As mentioned earlier, a species' habitat
specificity can be estimated by measuring
the limits of tolerance with respect to vari-
ables such as temperature, rainfall, substrate, food, and vegetation cover. Many
complex and linked characters of organisms, including adaptations for reproduction, feeding, thermoregulation, locomotion, and other functions, determine the
habitat specificity of a species. Under hypothesis 1, this basic set of coadapted habitat adaptationsis expected to resist break/
ing apart,and to show stabilitythroughlong
time.
One way to estimate the incidence of distribution drift, would be to sample a group
of organisms, such as the large mammals,
in the stratigraphiccolumn of a particular
locality that did fluctuateclimatically over
a given time interval or, better still, in several localities that are strategicallyplaced
over geography.The nature and timing of
February1992
VRBA-MAMMALS AND EVOLUTIONARYTHEORY
9
the associated climatic fluctuations should
be based on independent evidence, such as
of isotopic changes, snowline migrations,
lake-level fluctuations,pollen spectra,or invertebrateturnover. Fig. 5 shows diagrammaticallywhat might occur throughtime in
a given tropical African area if the hypothesis holds. Let us say that in the extreme
left column in Fig. 5 there is a rich and
complete fossiliferous sequence (the sedimentaryregime would have had to be rapid
enough to have buried successive samples
of large mammals for this example). Then
one should find five faunal and floral fossil
assemblages, from three biomes, superposed on each other in the same vertical
sequence, from (startingat the surface)desert, savanna grassland,savanna woodland,
again savanna grassland, and finally again
desert at the base. In this example, some
eurybiomic taxa, like the arrdvark0. afer,
would survive throughout. But, if a significantly greaterproportionof all taxa is present at some times and absent at others, in
consistent association with biome type, this
would corroboratethe hypothesis.
Evidence for distribution drift.--Abundant documentationof distributionchanges
through up to thousands of kilometers, in
diverse groupsof organisms,is discussed in
E. S. Vrba (in litt.). There is impressive evidence from all continents, for plants (Dupont and Hooghiemstra, 1989; Hooghiemstra, 1984; Huntley and Webb, 1989) and
for animals such as beetles (Coope, 1979;
Coope and Brophy, 1972), and from the
oceans (e.g., for marine plankton, Howard,
1985).
According to some of these results (e.g.,
Howard, 1985), large proportions of the
same communities drifted over geography
together.But, for severalreasons(E. S. Vrba,
in litt.), we should expect that to some ex-
Due to the complex interactions of factors
like topographywith climatic regimes, the
associations of different environmental
variables underwent recombination during
past times, and some recombinationamong
taxa in communities necessarily followed
suit. Otherreasons include species turnover
by speciation and extinction, and differences among species in how quickly their
distributions can spread in response to climatic change.
In agreement with these expectations,
there is some evidence that extant species
with Pleistocene records did occur in past
taxonomic associations differentfrom their
modem ones (e.g., Huntleyand Webb, 1989,
for North American trees; Bush and Colinvaux, 1990, for Central American forest
communities; Coope, 1979, and Coope and
Brophy, 1972, for beetles; Lundelius, 1989,
and Sutcliffe, 1985, for mammals). For this
reason, biome islands that have resulted
from vicarianceare unlikelyto be true community refugiain the strict sense of providing refuge for an association of taxa that is
identicalto that of the more widespreadparent community(Bushand Colinvaux, 1990).
I use the term refugium in the less strict
sense of a biome refugium;for instance, a
forest refugium surroundedby more open
vegetation might have preserved the characteristic forest vegetation physiognomy,
although its detailed taxonomic composition differed from that of the more widespread parent community.
Continuous sequences of high resolution
that record mammalian taxa through successive Milankovitch cycles are rare. Nevertheless, we can employ comparative tests
effectively, particularly with respect to
Pleistocene distributions. The evidence indicates (Rind and Peteet, 1985) that some
past interglacialtimes were warmerthan to-
tent the ecological associations of taxa were
different in the past from those today. One
reason is that each species has a particular
tolerance range for each habitat component
that may or may not be identical to that of
other species, and a combination of such
ranges for all its requirements that is unique.
day, as was the early Holocene period of the
current interglacial. We also know that the
height of the last glacial was considerably
colder in many terrestrial areas. The hy-
pothesis predicts that the northern distributional limits of most modern taxa were
farther north during the warmer periods,
10
Vol.73, No. I
JOURNALOFMAMMALOGY
and farthersouth duringglacials.Abundant
data corroborate the prediction. Sutcliffe
(1985) gave many examples from Europe.
For instance, hippopotamids are today
tropical. During the previous interglacial,
about 125,000 years ago, Hippopotamus
amphibius was present in Britain. During
past glacial times, many species that today
inhabit the Arctic tundra, like the collared
lemming, Dicrostonyx torquatus,occurred
in southern Europe. About the muskox,
Ovibosmoschatus,Sutcliffe(1985:97)wrote:
"At presentan inhabitantof the high Arctic,
where it can survive north of 800 latitude,
the formeroccurrenceof this tundraanimal
in central France, 300 south of its present
rangestrikinglyillustratesthe magnitudeof
the vegetational and faunal displacements
that must have accompaniedthe last major
glacial advance in Europe." Mammalian
distributiondriftof comparablemagnitudes
is evident from America (e.g., Martin and
Sneed, 1989).
GEOGRAPHIC
BIASESIN
TURNOVER
RATES
Under the term turnoverI subsume speciation, extinction, and distribution drift,
all resultingin species turnoverin particular
areas. The habitat theory includes several
hypotheses that addressthe question:For a
given time interval and set of taxa, can we
identify categories of areas on Earth some
of which have statistically significantly
higher turnover rates than others? In this
section I outline three such hypotheses,and
their predictions,without citing any empirical tests and evidence. In the subsequent
treatmentof the Americanand Africanfossil records, some tests and supportingevidence are discussed.
Hypothesesrelating to topographicdiversity. - Topographic diversity refers to the
number of patches of high and low elevation, and of differentsubstrates,per area. It
generallyimplies climatic diversity, and on
a land surface vegetational diversity (Fig.
6).
HIGH
TOPOGRAPHY
VICARIANCE
LOW
VICARIANCE
TOPOGRAPHY
SCOLDER
IV aA
il
c.
,
a-
0
,
,
-
,
L!
WARMER
GRASSLAND QWOODLAND
L1
FIG.6.-Areas of high topographicdiversity
(left)areexpectedto undergohigherratesof vicarianceof species'habitatsanddistributionsthan
areas of low topographicdiversity (right),with
climatic changes.
Hypothesis2: Of two areas of similar large
size, both subject over the same time to
Milankovitch cyclic extremes that remain habitable for organisms, the area
that is more diverse in topographywill
have higherincidences of selection pressures and vicariance per species.
The prediction is that higher rates of speciation,extinction,and distributiondriftwill
occur in the topographicallymore diverse
area than in the one that is less so. The
subpredictionof particularinterest is that,
ceterisparibus, topographicallydiverse areas (Fig. 6, left) are more likely to be factories of species diversity because there is
constant fragmentationof species' habitats
and distributions. To test this, one needs
measures of topographic and climatic diversity (generated,for example,by methods
of Nix, 1986, and N. Caithness, in litt.) for
February1992
VRBA-MAMMALS AND EVOLUTIONARYTHEORY
comparison with cladistic estimates of speciation rates. Such a test requires cladistic
and geographiccoverage that is sufficiently
broadto factorout potential influencesother than topography, such as those arising
from latitude, which is the subject of the
next two hypotheses.
Latitudinal asymmetries.-The habitat
theory also raises questions about latitudinal asymmetries in turnover rates. Let us
explore one hypothesis that applies to a
worldwith strongthermalcontrasts,namely
with an ice cap on one or both poles. Fig.
7 shows a hypotheticalcontinent cyclingbetween warming and cooling. Compare the
fate of the grasslandand woodland biomes
with the fate of the equatorialforest biome.
The grasslandand woodland biomes mainly
drift between north and south. The species
specific for these higher-latitudebiomes are
riding along on their "habitat plates," that
drift back and forth rapidly (in geological
terms)over the tectonicplatesthatdriftmore
slowly beneath. Due to local topographic
heterogeneities (Fig. 6), these species will,
of course, experience the pressures of environmental change. For instance, as the
grassland biomes drift equatorward upon
cooling, they are expected to leave behind
at high latitudes vicariant grasslandislands
surroundedby tundra. But in the equatorward direction they have space into which
to spread,and may connect acrossthe hemispheres. These biomes and their species do
not suffer much net loss of area at either
stroke of the climatic cycle.
In contrast,the forest biome duringcooling undergoesmuch more reductionin area
(as if drawninto a fissurecirclingthe equator) and more vicariance.Thus, ceterisparibus, we may expect different macroevolutionary histories at lower and higher
latitudes.
Hypothesis3: During periods of strong latitudinal thermal contrasts and little
change in Milankovitch amplitude, biomes closest to the equator should in general have higher speciation and extinc-
C--AN-ING
HA3,T'
7,
WIT
11
CISTRIRU-.CNS ON A CONT ,ENT
C CYCLES
TCIV.T
M
•- 7 i
•:•
j:-,.•
i?,
I??i:?~~??~I?.
,
i
.
zz
ARMAIN
. -. .
-,
EOUATOR
COOLING
:
:..--:..,
•
??
P
FOREST
VOZ-'IDLAn GRASSLAND NDA
FIG. 7.--Illustration of changing habitat distributions,with climaticcycles, on a hypothetical
continent.
tion ratesthan biomes at adjacent,higher
latitudes.
Under the habitattheory, vicarianceof species' habitats and distributions is basic to
lineage turnover.Hypothesis 3 implies that
vicariancebetween habitablealternativesis
highest in the tropics on the kind of world
prevalentat least since the Miocene, namely
one with an ice cap at one or both poles.
During such intervals the high latitudes are
unlikely to be centers of biotic vicariance:
Although alternative environments come
and go at high latitudes, in synchronywith
climatic cycles, only the interglacialalternative offers extensive areas that are habitable for organisms. The glacial extreme
causes mainly extinctions, and not burstsof
speciation. I suggested (Vrba, 1985) that
during ice-free phases such as the Cretaceous (Barronet al., 1981) the reversemight
be predicted; that is, more vicariance and
evolution at high than at low latitudes.
I stress that higher extinction and speciation rates at low latitudes are predicted
under conditions of little change in amplitude of the Milankovitch cycles for the fol-
12
JOURNAL OF MAMMALOGY
lowing reason. Recall that there were times
of major change in the mean and mode of
these cycles. At such times (e.g., the major
cooling change near 2.5 million years ago;
Fig. 3) the following is suggested.
Vol. 73, No. I
Alternativeviewpoints(reviewedin Vrba,
1985) predict a more even temporal distribution of turnover events. That is, they
predict a constant 'backgroundnoise' of
turnoveragainstthe time axis, showinggentle-to-steeper peaks in response to marked
Hypothesis 4: At the first major intensifi- physical changes. The most extreme turncation of the cold extreme of the Miover response to physical events, mass exlankovitch cycle, after a longer period of
tinction, is generallyacknowledged.
roughly constant cyclic amplitude, a
Hypothesis 5 is an extreme statement. It
massive preponderance of extinctions
is difficultto test. Paleontologicalrecovery
over speciations occurs at low latitudes.
of species' actual first and last appearances
Conversely,at such intensificationof the is beset taphonomic problems
by
(Behrenswarm cyclic extreme, more extinctions
and Hill, 1980). Even if there were
meyer
than speciations occur at high latitudes.
real turnover-pulses sufficiently separated
in time, the turnover events recorded in
THE TURNOVER-PULSEHYPOTHESIS
The turnover-pulsehypothesis(Fig.8) was many fossil sequencesmight be expectedto
a broadly distributed,gradualpatoriginallystatedas follows(Vrba,1985:232): present
tern against time (Signorand Lipps, 1982).
Hypothesis5: Speciationdoes not occurun- One possible approachis to use molecular
less forced (initiated) by changes in the rates of change togetherwith an exceptionphysical environment. Similarly,forcing ally good fossil record to obtain estimates
by the physicalenvironmentis required of divergencetimes (E. S. Vrba,in litt.). This
to produce extinctions and most migra- is what my colleaguesR. DeSalle, J. Gatesy,
tion events. Thus, most lineage turnover R. Vaisnys, and I are currentlydoing to test
in the history of life has occurredin puls- for speciation pulses. We are using a comes, nearly (geologically) synchronous bination of cladogramsbased on fossil-plusacross diverse phylogenies, and in syn- Recent morphology and on mtDNA
chrony with changes in the physical en- sequences of African antelopes, with inforvironment. Most turnover-pulses are mation on molecularevolutionaryratesand
small peaks involving few lineages or re- on paleoclimate. Because our data will not
strictedgeographicareas. Some are mas- have the resolutionto test the generalstatesive and of global extent.
ment of the hypothesis, we will test a more
restricted
version:
Under this hypothesis, biotic interactions, like predationor competition, occur- Hypothesis6:
Majorglobalclimaticchanges,
ring on their own in the absence of physical
that in the climatic recordoccurredfrom
changes, are not sufficientto cause speciaone to several millions of years apart,
tion or extinction. Physical changes are
accounted for the vast majority of speneeded to forcethe system offbalance.They
ciation events.
in turn cause a host of biotic changes. In
this view, speciation and extinction are two This predicts, first, that turnover-pulses
closely related possible responses to the should be statistically distinguishable in
common initiating cause of physical envimanygood datasets. If this propositionwere
ronmental change; and both are preceded true, we might expect >80% of all branchby a phase of allopatry (Fig. 4). Whereas ing eventsin ourbovid sampleto be bunched
physical changes are needed to initiate spe- temporally at a few time levels. A second
ciation and extinction, they are not suffi- prediction is that at each such time there
cient, as shown by the prevalenceof distri- should be independentevidence of climatic
bution drift (Fig. 5) without significant change, that is widespreadover the known
morphological evolution.
geographicdistribution ranges of the rele-
1992
February
AND EVOLUTIONARY
THEORY
VRBA-MAMMALS
13
MYC
/i
PULSE
TURNOVER
I
c~lJill
TIME
HOMINOIDS
ANTELOPES
TREES
MEAN
IGLOBAL
TEMPERATURE
BIRDS
in this hypotheticaldiagram,majorclimaticchangesat timesy and x
FIG.8.- Turnover-pulses:
initiatedturnoverpulses,that is, coincidentspeciationsand extinctionsin groupsas differentas
hominoids,antelopes,trees,andbirds.
vant taxa.A distributionof divergencetimes
that is indistinguishablefrom randomwould
contradictthe first prediction;and one that
is uncorrelatedwith major climatic changes
would contradict the second.
AND
SPECIALISTS,
GENERALISTS,
TURNOVER
RATES
Arguments that link breadth of resource
use to speciation and extinction rates are
not new (e.g., Eldredge, 1979; Eldredgeand
Cracraft, 1980; Rensch, 1959; Simpson,
1953; Stebbins, 1950; Vrba, 1980, 1984).
All basically suggest that lineages of specialists should be less speciose than lineages
of generalists. My arguments (especially
Vrba, 1987a) on this differ in crucial respects from others. I stress the historical
biomic ranges of clades and how species'
resourcepatchesare distributedacrossthose
ranges; subdivision of the concept of resource use with a focus on eurybiomy and
stenobiomy; and selection pressures from
physically initiated environmental changes
as the important causal agents rather than
biotic interactions.
The resource-usehypothesis.- Breadthof
resource-use is posited to relate to speciation and extinction rates as follows.
Hypothesis 7a: Clades of species, whose resources tended to persist as environmental extremes came and went duringtheir
histories, had low rates of vicariance,
speciation, and extinction. Such eurybiomic lineages include generalists,that
can flexibly use differentresourcesin different environments, and specialists
whose specialist patches persisted in alternative environments.
Hypothesis 7b: Clades of species, whose resources tended to disappear during one
of the recurrentenvironmental extremes
during their histories, had high rates of
vicariance, speciation, and extinction.
This category includes clades of specialists on one or more kinds of resources
that areconfinedto a narrowbiome range.
To test this hypothesis, I compared speciation rates of 20 monophyletic groups of
mammals with several ecological variables
of theirmodem survivors,includingfeeding
behavior, and dependance on vegetation
14
JOURNALOF MAMMALOGY
cover. The results (discussed in detail and
graphed in Figs. 3 and 4 of Vrba, 1987a)
supportedhypothesis7 as follows.All clades
that today comprise exclusive grazers and
all clades of exclusive browsers (one category among the clades mentioned in hypothesis 7b, whose resources have tended
to disappearduringone of the recurrentenvironmental extremes)showed consistently
higher speciation rates than did clades of
herbivoresin whicheach organismcan graze
and browse (hypothesis 7a). This suggests
that both biomic extremesof the astronomical cycles were active causal agents of speciation in African savanna mammals.
Myrmecophages,largecarnivores,and omnivores all belong among eurybiomic lineages whose resourceshave tended to persist as environmental extremes came and
went duringtheir histories (hypothesis 7a).
All such clades were found to have had low
speciationrates,as predicted(Fig. 3 of Vrba,
1987a).
TESTINGTHEHABITAT-THEORY:
Vol.73, No. I
3"
12.r
-iMN*
10
13
ro?~19
20~o
FIG.9.--Mammal taxa involved in the Great
American Interchangeacross the Panama landbridge in the late Pliocene (data from Marshall
et al. 1982). From south to north: 1. Glyptodontidae; 2. Myrmecophagidae;3. Megatheriidae;4.
Erethizontidae;5. Hydrochoeridae;6. Didelphidae; 7. Mylodontidae;8. Dasypodidae;9. Toxodontidae.From north to south: 10. Felidae;11.
LATE-PLIOCENE
AMERICA
South America was isolated from North
Americauntil about 3-2.5 million yearsago Soricidae;12. Cricetidae;13. Camelidae;14.
when the Panamanianlandbridgeemerged. Canidae; 15. Mustelidae; 16. Tapiridae;17. LeThis resulted in migrationsof mammals in poridae;18. Sciuridae;19. Tayassuidae;20. Proboth directions (Fig. 9), especially close to cyonidae;21. Ursidae;22. Gomphotheriidae;23.
2.5 million years ago, comprising the fa- Equidae;24. Cervidae.
mous Great American Interchange(Table
1). Information on South American fossil
mammals and chronology below is from ern and southernmammalfaunas. -There
Marshall (1985), Marshall et al. (1979,
arethreemajordifferencesbetweenthe postland bridgehistories of northernand south1982), L. G. Marshall and T. Sempere (in
litt.), Patterson and Pascual (1972), Simp- ern mammalian faunas (Fig. 10; Marshall
son (1980), Stehli and Webb (1985), Webb et al., 1982). First, more northern genera
(1969, 1976, 1985), and Webband Marshall moved south, than vice versa (arrows labelled a in Fig. 10; Table 1). The explana(1982). When I refer to post-landbridge,I
mean the periodfrom about 2.5-1.5 million
tion of Marshallet al. (1982) for this draws
years ago, that for South America L. G. on MacArthurand Wilson's (1967) equilibMarshall and T. Sempere (in litt.) recently rium theory, which predicts that more misubsumed under the ChapadmalalanLand grantsshould emigratefrom that of two arMammal Age (which includes the Uquian eas with the more diverse source pool of
of earlierwritings),and that in North Amer- taxa and greatersurfacearea.In the present
ica (Webb, 1985) includes the late Blancan case, generic diversity of pre-landbridge
and earlier Irvingtonian.
North America was indeed greater than
Differencesbetweenthe historiesof north- thatof SouthAmerica;and the areaof North
TABLEI.--Earliest recordsof immigrant mammalian genera in the GreatAmerican Interchange. Com
et al. (1979, 1982), Patterson and Pascual (1972), Webb(1985), and Webband Marshall (1982). "Prim
have come directlyfrom the other continent; "secondaryimmigrants" are genera that evolvedfrom prim
1982). Chronologymainly after L. G. Marshall and T. Sempere (in litt.) who include in the Chapadmalal
1.5 million years ago, the Uquian of previous writings(genera denoted here by "Uquian").
Land mammal age and
interval (in millions
of years ago)
Order
Family
Common name
Genus
Arrivalsin NorthAmericafromSouthAmerica
Hemphillian(9.5-5.0)
Blancan(5.0-1.8)
Irvingtonian
(1.8-late Pleistocene)
Huayquerian(9.0-6.0)
Montehermosan(6.0-2.5)
Edentata
Edentata
Edentata
Edentata
Edentata
Edentata
Rodentia
Rodentia
Sirenia
Edentata
Edentata
Edentata
Edentata
Rodentia
Marsupialia
Carnivora
Carnivora
Rodentia
Rodentia
Pliometanastes
Megalonychidae
ground sloths
Thinobadistes
Mylodontidae
ground sloths
Glyptodontidae
glyptodonts
Glyptotherium
armadillos
Dasypodidae
Kraglievichia
armadillos
Dasypodidae
Dasypus
Glossotherium
Mylodontidae
ground sloths
Erethizontidae
Erethizon
porcupines
Neochoerus
Hydrochoeridae
capybaras
Trichechidae
manatees
Trichechus
Megatheriidae
ground sloths
Nothrotheriops
Eremotherium
Megatheriidae
ground sloths
Myrmecophagidae giant anteater
Myrmecophaga
armadillos
Dasypodidae
Pampatherium
Hydrochoeridae
capybaras
Hydrochoerus
Didelphidae
opossums
Didelphis
Arrivalsin South Americafrom NorthAmerica
raccoons, etc.
Procyonidae
Cyonasua
raccoons, etc.
Procyonidae
Chapalmalania
Cricetidae
mice, etc.
Auliscomys
Cricetidae
mice, etc.
Bolomys
TABLE1.- Continued.
Land mammal age and
interval(in millions
of years ago)
Chapadmalalan(2.5-1.5)
Order
Carnivora
Carnivora
Carnivora
Carnivora
Carnivora
Carnivora
Carnivora
Carnivora
Rodentia
Rodentia
Rodentia
Rodentia
Rodentia
Rodentia
Rodentia
Rodentia
Rodentia
Artiodactyla
Artiodactyla
Artiodactyla
Artiodactyla
Artiodactyla
Artiodactyla
Artiodactyla
Artiodactyla
Artiodactyla
Perissodactyla
Perissodactyla
Perissodactyla
Proboscidea
Family
Mustelidae
Mustelidae
Mustelidae
Mustelidae
Ursidae
Canidae
Canidae
Felidae
Cricetidae
Cricetidae
Cricetidae
Cricetidae
Cricetidae
Cricetidae
Cricetidae
Cricetidae
Cricetidae
Tayassuidae
Tayassuidae
Camelidae
Camelidae
Camelidae
Cervidae
Cervidae
Cervidae
Cervidae
Equidae
Equidae
Tapiridae
Gomphotheriidae
Common name
skunks, etc.
skunks, etc.
skunks, etc.
skunks, etc.
bears
dogs, etc.
dogs, etc.
cats, etc.
mice, etc.
mice, etc.
mice, etc.
mice, etc.
mice, etc.
mice, etc.
mice, etc.
mice, etc.
mice, etc.
peccaries
peccaries
camels, etc.
camels, etc.
camels, etc.
deer, etc.
deer, etc.
deer, etc.
deer, etc.
horses
horses
tapirs
gomphotheres
Genus
Conepatus
Galera
Galictis
Stipanicicia
Arctodus(Arctotherium)
Protocyon
Dusicyon
Smilodon (Smilodontidion
Akodon
Dankomys
Graomys
Reithrodon
Oryzomys
Zygodontomys
Calomys
Euneomys
Scapteromys
Argyrohyus
Platygonus
Paleolama
Lama
Hemiauchenia
Antifer?
Habromeryx?
Hippocamelus
Ozotoceros
Hippidion
Onohippidium
Tapirus
?Stegomastodon
TABLE1.- Continued.
Land mammal age and
interval (in millions
of years ago)
Ensenadan(2.4-0.7)
Order
Carnivora
Carnivora
Carnivora
Carnivora
Carnivora
Carnivora
Carnivora
Rodentia
Rodentia
Artiodactyla
Artiodactyla
Artiodactyla
Perissodactyla
Family
Procyonidae
Canidae
Canidae
Mustelidae
Mustelidae
Felidae
Felidae
Cricetidae
Cricetidae
Tayassuidae
Tayassuidae
Camelidae
Equidae
Common name
raccoons, etc.
dogs, etc.
dogs, etc.
skunks,etc.
skunks,etc.
cats, etc.
cats, etc.
mice, etc.
mice, etc.
peccaries
peccaries
camels, etc.
horses
Genus
Nasua (Brachynasua?)
Cerdocyon
Canis (Theriodictis)
Lyncodon
Lutra
Felis (Puma)
Felis (Jaguarius)
Necromys
Ptyssophorus
Catagonus
Tayassu (Dicotyles)
Vicugna
Equus
18
JOURNAL OF MAMMALOGY
Vol. 73, No. 1
America is larger(24 x 106 km2) than that ther, the generic origination rate of North
of South America (18 x 106 km2). Never- Americanimmigrantsin the south also was
theless, I will suggestthat a differentexpla- greaterthan that of the North Americannanation may be the correct one.
tives that stayed behind in the north. Early
The second differencebetween the north- explanations invoked the competitive suern and southernfaunasconcernstheir sub- periorityof NorthAmericaninvaders,which
sequent histories in South America (arrows radiatedinto empty niches vacatedby comlabelled d in Fig. 10). Here the generic expetitively excluded South American taxa.
tinction ratesof SouthAmericannatives inMore recently, Marshall et al. (1982) concreasedmuch more, from pre- to post-land- cluded that this difference remains unexbridgetimes, than those of North American plained and is certainly not expected from
immigrants,althoughthese increasedas well MacArthurand Wilson's (1967) theory.
Theclimaticcontextof theinterchange.
(Marshall et al., 1982, discussed in detail
how they calculated extinction and specia- Let us now look at this evidence from the
tion rates,and gave the distributionof these point of view of the habitattheory.The recrates among land mammal ages). In conord in Fig. 3 may be interpretedto reflect
from
to
in
trast,
pre- post-landbridgetimes,
mainly global temperaturechangesover the
North America the genericextinction rates past 6 million years(Vrbaet al., 1989). Note
stayed roughly constant for both northern that the period from about 3.5-2.5 million
natives and southern immigrants (arrows yearsago, when the Panamanianlandbridge
labelled b in Fig. 10). Traditionalexplana- emerged,was one of strongnet cooling. The
tions for the South Americanextinction imrefrigerationevent close to 2.5 million years
balance (e.g., Simpson, 1950, 1980; Webb, ago was unprecedented in the entire Ce1976, for ungulates) invoked replacement nozoic (Prenticeand Matthews, 1988); and
of adaptively inferior South American na- after about 2.5 million years ago, the avtives, throughcompetitive exclusion, by the
erage of the climatic cycles became even
North American invaders.
colder.
That both the natives and the immigrants
Note also that the averagetemperatureof
in South America experienced higher ex- the period precedingthe 3-2.5 million year
tinction rates (arrowslabelled d in Fig. 10) interval was considerablywarmerthan the
is explained by Marshall et al. (1982) by current interglacial.Thus, it is realistic to
supersaturationabove the previous equilib- suggestforpre-landbridgetime an averagely
rium diversity:basing their argumentagain greaterextension of the tropical forest and
on MacArthurand Wilson (1967), they ar- dense woodland biomes than today. This
gued that the post-landbridgegeneric in- hypothesis is crudely indicated in Fig. 10,
crease in South America was greater than by solid shadingfor forestsand dense woodthat continent can carry, resulting in dis- lands, and circles for open woodlands and
proportionate extinctions (Marshall et al., grassland savannas. Especially in South
1982).
America, because of its mainly low-latitude
The third differenceis perhaps the most position, forest-woodland biomes should
interesting: In South America the generic have dominated with relatively little open
woodland and grasslandsavannas.
origination rate of North American immiWith the severe cooling change towards
grantsincreasedmuch more than that of the
South American incumbents (arrows la- 2.5 million years ago, Earth cooled at least
belled in e in Fig. 10). In contrast,in North as much as during the last glacial (ShackAmerica (arrowslabelled c in Fig. 10), the leton et al., 1984), and tropical forests are
genericoriginationratesof South American expected to have shrunk as much. This is
immigrants and North American incum- represented in Fig. 10 by Haffer's reconbents remained roughly constant (in both struction (1982, based on several papers in
cases lower than the extinction rates). Fur- Prance, 1982) of American forest refugia
1992
February
VRBA-MAMMALS
AND EVOLUTIONARY
THEORY
19
00000O
0000
o
o o0 0 0
GENERA:
GENERA:
EXTINCTION RATEOF LOCAL
00
0
RATE
000 o 0 o 0 o0o
•
Goer ?o
oaM
ORIGINATIONS
o
, o oo00
N.AM. NATIVES:
o
000......
S.AM. IMMIGRANTS:
a
oI
b
c
IMMIGRANT
GENERA
7/
o
0
o oo
o oo
a
0a
o
o0
oo
EQUATOR
o6
S.AM. NATIVES:
o000
N.AM.
IMMIGRANTS:
oo
o
ooI",00
"
d
e
"ooo
o
o/
PRE-LANDBRIDGE (> 2.5 MYR AGO)
o
o o0o
o
oo
POST-LANDBRIDGE (< 2.5 MYR AGO)
Generic data Marshall et al., 1982; MYR = millions of years ago;
Tropical forest refugia = 16
; from Haffer, 11982;
82
Ice
cean and tundra
unr
"000()r
=
Other mostly more open vegetation
=
FIG.10.-Comparisonof NorthAmericanand SouthAmericanmammalfaunasat the generic
times:arrowslabelleda indicatemigrationrates;b and d,
level, from pre- and post-landbridge
extinctionrates;c and e, originationrates.Widthsof arrowsrepresentmagnitudesof relativerates
(afterMarshallet al., 1982),and in b-e whetherratesremainedconstantor increasedfrompre-to
times.Hypothetical
extentof forestanddensewoodlandis indicatedby solidpattern,
post-landbridge
of moreopen vegetation,by smallcircles;the reconstructed
extentof tropicalforestsat about2.5
millionyearsago,post-landbridge,
followsHaffer's(1982)hypothesisfor the lastglacial.
18,000 years ago. But a contrasting view
should be noted here: Bush and Colinvaux
(1990:105) arguedthat, for instance in Panama, there "were never refugiafor tropical
rain forest taxa at any time duringthe Quaternary,ratherrain forest species existed in
unfamiliarcommunities in the Panamanian
lowlands."My hypothesis on earlyPliocene
glacial environments does not require a
diminution of rainforest as extreme as in
Haffer (1982), but only that at least woodlands with open patches had some continuity through the isthmus.
Thus, in the Americas this period was
marked by two major sets of physical
changes:tectonism culminatingin the final
emergenceof the landbridge,and net global
climatic cooling, unprecedentedin the Cenozoic. Previous explanations focussed on
the tectonic change, and on biotic interactions following faunal interchange.In contrast, the habitat theory focusses on both
physical changes,but downplaysthe role of
biotic interactions as initiating causes of
speciations and extinctions.
Previous analysts of the interchangenoted that fossil assemblages from American
rainforest are rare (Marshall et al., 1982).
This is the expectedresultof the well-known
taphonomic bias against bone fossilization
in rainforests, relative to that in dense
woodland, open woodland, or grassland
(Behrensmeyerand Hill, 1980). I will briefly
refer to some implications of this bias as I
20
JOURNAL OF MAMMALOGY
applythe habitattheoryto the observedimbalances in migration, extinction and origination rates (Fig. 10).
Vol. 73, No. I
imbalance favoring the north is nevertheless predictedbecausethe numeroussavanna specialistsparticipatingin the interchange
The habitattheoryof the migrationim- are expected to have come overwhelmingly
balance.-One of the predictions of the re- from the north, with its relatively much
source-usehypothesis 7a is that biome gen- larger pre-landbridgesavanna biome (Fig.
eralists are rare, while specialist species
10).
Under the habitat theory, as applied to
heavily predominate(Vrba,1987a).The few
biome generalistsfrom bothnorthand south this example, gross geographic areas and
are expected to spread their ranges upon taxic diversities of source pools are irrelecontinental joining, because their funda- vant. Total areas and taxic diversities are
mental habitatsare likely to continue on the
only expected to make a differenceat much
other side. In this respectthe predictionsfor smaller spatial scales than representedby
south and north are the same. However, these two continents.Under the habitattheover a period of global cooling, the distri- ory, both these gross variables are subdibutions of the numerous vegetation spe- vided into ecological components, and it is
cialists, whether on forest or on grassland the distinction between these components
savanna or on some narrow range in be- that makes the difference.
For this view to survive, an ecological
tween, are predicted mostly to move with
their habitats towards the equator. Simply analysisof the interchangetaxa (Fig. 9) near
put, from the north, biome generalists, 2.5 million years ago would have to demdense-vegetationspecialists,and the savan- onstratethat mostimmigrantsinto the north
na specialists from a relatively huge pre- really were relative biome generalists,and
landbridgesavannabiome (Fig. 10), should that most immigrants into the south were
have had a net vector of southwardmigra- specialists on more open biomes. My readtion near 2.5 million years ago. In contrast, ing of the literature,so far, suggeststhat a
from the south, only the rare biome gen- more detailed study might indeed find this
eralists are expected to move north, except to be so: several of the immigrantsfrom the
for the few savanna specialistsfrom the rel- south, firstrecordedin the North American
late Blancan (near 2.5 million years ago),
atively small pre-landbridge savanna biomes in South America.
have living relativesthat aregeneralistswith
In sum, the habitat theory precisely pre- respect to biomes and food (e.g., Macdondicts the more numerous northern immiald, 1984). For example, the single living
grantsto SouthAmericathanvice versa(Fig. species of capybara, Hydrochaeris hydro10). Note that this predictionfrom the hab- chaeris, today has a wide distribution in
itat theoryremainsrobusteven if the tapho- South America and Panama. Although alnomic bias againstfossil forms restrictedto ways found near water, it is known from
rainforest had operated: During times of open grasslandto rainforesthabitats.Living
global cooling, forest specialists are expect- armadillos, Dasypodidae, of which forms
ed to migrate towards the equator. While, like Dasypus and Kraglievichiaare first reprevious to the landbridge,SouthAmerican cordedin the North Americanlate Blancan,
forest specialists are likely to have greatly today mostly eat a broad range of insects,
outnumberedtheir North American coun- fungi, tubers, and carrion,and live in habterparts,this southerncontingentis not exitats from arid desert to rainforest. Some
pected to have participated in northward extinct edentates, like the giant ground sloths
migrationduringa cooling phase. Thus, any that entered the north at the same time (e.g.,
taphonomic bias against forest specialists the mylodontid Glossotherium that entered
should reduce the northern migrant total in the late Blancan, and the megatheriid
relative to the southern one. But a migrant Ereinotherium, which did so in the early
February1992
VRBA-MAMMALS AND EVOLUTIONARYTHEORY
Irvingtonian; other sloths had already entered North America during the late Miocene probablyby dispersalalongislandarcs),
and glyptodonts, are thought to be unspecialized herbivoresby severalof the analysts
of the Great American Interchange (e.g.,
Webb and Marshall, 1982).
In contrast, I suggest that the more numerous northern taxa, like cricetids, camelids, cervids, and equids, that firstappear
in the south near 2.5 million yearsago (Chapadmalalan),may well be found to include
a significantmajority of specialists on open
biomes (note that this does not requirethat
northern emigrants were all open-biome
specialists, nor even that the generalists
[peccaries,and some carnivoretaxa arelikely candidates] were rare, only that the specialist proportion of all migrantswas sufficiently higherfrom the north than that from
the south).Webb(1978) did arguethat many
northernemigrantsto the south were tracking savanna corridorsthroughthe isthmus.
He did, however, suggest the same for
southern emigrants as well.
The habitattheoryof the extinctionim-
balance.-A prediction for a time of exceptional cooling, accordingto hypothesis 4, is
that extinction rates for specialists on tropical forest and dense woodlands should be
highest, because their habitats disappearto
a greater extent, whereas the distributions
of specialists on open woodlands and grasslands are likely to find suitable habitats to
move into. Thus, as most specialists on
dense vegetationbeforethe interchangewere
South American, the highest post-landbridge extinction rate for South American
natives (arrows labelled d in Fig. 10) is as
predicted by the habitat theory. In fact, as
2.5 million years ago was a time of exceptional cooling especiallyrelativeto previous
mild climates, one should not be surprised
to find evidence of mass extinction of tropical specialists on dense vegetation at this
time. Furthermore, South American taxa
that did survive are expected to include a
disproportion of biome generalists. Any
taphonomic bias againstforms restrictedto
21
rainforestis expected to have decreasedthe
numberof recoveredfossil taxa particularly
among South American natives. That is, if
one could cancel this bias, the true postlandbridgeextinction rate of South American natives is expected to be even higher
(absolutely, and relative to that of North
Americanimmigrants)than it appearsto be
at present (arrowslabelled d in Fig. 10).
Competitive exclusion and other interspecific interactions have traditionally featured prominently in causal scenarios of
ecological replacementamong biotic groups
(see review in Benton, 1983), including in
the explanationsof the presentreplacement
pattern(e.g., Marshallet al., 1982; Simpson,
1950, 1980; Webb, 1976, for ungulates).
Under the habitat theory, the North American immigrantsneed not have been in any
way competitively superior to produce the
observed extinction imbalance. They only
needed to include a largeproportionof open
woodland-savanna genera to survive in
greaternumbers.That is, interspecificcompetition need not be invoked at all.
For this view to survive, an ecological
analysis of the interchangetaxa (Fig. 9) near
2.5 million years ago would have to demonstrate that most South American extinctions in the late Pliocene and early Pleistocene really were of taxa specialized on
disappearingforest or dense-woodland resources.
Thehabitattheoryof the originationim-
balance.-Generic originationratesof North
American immigrantsfar outweighedthose
of South Americannative survivors(arrows
labelled e in Fig. 10). First, I will consider
this under the assumption that North
American immigrantsreally did have a significantly higher origination rate. That is, I
assume here that even if taphonomic bias
against forest forms did diminish the recovered originationsfrom South American
natives disproportionately(and thus the recovered totals seem to favor northern immigrantsmore than was reallythe case), this
bias was insufficientto createthe imbalance
we see (arrows labelled e in Fig. 10) from
22
JOURNAL OF MAMMALOGY
balance (or from a reversed imbalance) in
reallife. That is, underthis assumptionthere
is a component of the observed difference
that requiresa nontaphonomicexplanation.
One possible explanationin this case is the
expectation, alreadymentioned, that South
Americantaxa that did survive this massive
climatic changeincluded a disproportionof
biomic generalists,with predictedlow speciation rates (hypothesis 7). As I discussed
above, this is indeed observed in African
mammals over this time period (Vrba,
1987a). A preliminarysurvey of the South
American survivors (see lists in Marshall,
1985; Simpson, 1980) suggests that this
might be found true upon ecological and
genealogical analysis. For instance, in the
Didelphinae, the opossums, all modem species of Didelphis as well as several other
living opossums seem to be generalistswith
respectto vegetation cover, food, and other
habitat variables.
One also would need to demonstratethat
the large diversificationsin South America
(Fig. 9), from northern-immigrantancestors, involved relatively more habitat specialists. The largest radiations occurred in
cricetine rodents, proboscideans, perissodactyls, artiodactyls,and carnivorans.The
multiplicationof cricetidspecies is the most
remarkableof all. A comparisonof modern
South American and African mammals (E.
S. Vrba,in litt.) shows that Africancricetids,
althoughknown in Africa for about 18 million years, attained less than one-third of
the species richness of the South American
cricetids,firstrecorded3.5-2.8 million years
ago accordingto Marshallet al. (1982) and
only about 2.5 million years ago according
to L. G. Marshalland T. Sempere(in litt.).
South American cricetines multiplied to
about 40 generaand > 200 species. Even if
they arrived earlierin the Pliocene by waif
transportand/or entered via several ancestral migrants, as variously suggested (e.g.,
Hershkovitz, 1972; Reig, 1978), the multiplication of their lineages in South America still seems remarkable.
The habitat theory suggestsone possible
explanation:This cricetiddiversificationin-
Vol. 73, No. I
cludes numerous specialist grazers with
habitats at high elevations, prime candidates for frequent habitat vicariance (Fig.
6). The earliest-knowncricetid records are
specializedgrazingforms (Marshall, 1985).
I suggest that, if this group is analyzed genealogicallyand ecologically,this radiation
may well be found to supportthe hypothesis
that biome specialization promotes high
speciation rates (hypothesis 7)--especially
in tropical areas (hypothesis 3) of high topographicdiversity (hypothesis2). The difference in cricetid diversification between
Africa and South America may be accounted for by the fact that South America today
has about 7 times as much montane grassland as Africa, with a further 3 times as
much montane area that is presently forested, but may not always have been so in
the Pliocene and Pleistocene (W. Duellman, in litt.).
Regardingthe observed origination imbalance as a whole, a second possibility is
that taphonomic distortion played a major
causal role. Consider, for instance, the following scenario of three sequential instancesof the same taphonomicbias. 1)Prelandbridge mammal diversity may have
been higherin SouthAmericathanin North
America (contraMarshallet al., 1982; as is
the case today, Honacki et al., 1982), with
a large proportion of southern forest specialists (and a smaller one from centraland
North America) unseen by paleontologists.
2) Although many southern forest specialists became extinct near 2.5 million years
ago, a large number may have survived
whose remainswerenot recovered.3) From
these southern survivors may have originated many new species that, due to taphonomic processes, were not recovered (another way to state this three-step scenario
is that there is a severe imbalance between
the recovery rates of North American and
South American fossil mammals). Perhaps
there was either an origination imbalance
favoring South America, or none at all. In
the case of this scenario,the questionwould
remain why the observed imbalance (arrows labelled e in Fig. 10) occurredin taxa
1992
February
23
THEORY
AND EVOLUTIONARY
VRBA-MAMMALS
recovered from woodlands and grasslands.
Part of the previous explanation might still
apply to that.
SHUNGURA
FORMATION
STRATIGRAPHY
TUFF
/
AGE
S(MYR)
PALEOENVIRONMENTS
ACCORDING TO
MICROMAMMALS
MORE XERIC
-
MORE MESIC
A COMPARISON
WITHLATEPLIOCENE
EVENTSIN AFRICA
One marvellous test would be if we could
rerunPanamaclosureas an experiment,but
with both continents displaced southward
so that the equatoris near Washington,DC.
Then these unequal migratory and evolutionary results are predicted to be exactly
reversed: that is, more immigrants from
south to north, more extinctions of North
American natives, and greaterradiation in
North America of South American immigrants.
Although that test is impossible, we can
apply one involving comparison with Africa. Remember, under the habitat theory,
climate and habitat specificities play a preeminent role. This is unlike the traditional
explanations, in which interspecific competition (and its effects) due to interchange
are preeminent.In Africa, climate and habitat specificities must have played a similar
role as in South America, while there was
no tropical interchangedue to continental
joining. Thus, four sets of observationsmust
apply to Africa as well if the hypotheses for
the American phenomenon are valid. First,
in Africaduringthe late Pliocenetherewould
have had to be large-scaleclimatic and vegetationalchangesresultingfromglobalcooling. Second, there should be evidence of
substantialmigrationof speciesmainly from
northern, and also from southern areas towards the equator near 2.5 million years
ago. Third,thereshouldbe evidenceof largescale extinction of tropicalAfrican"native"
forms, more than at higherlatitudes.Fourth,
there should be evidence of massive diversification of savanna specialists in the African tropics from the late Pliocene onwards. The needed detailed studies have not
yet been done. But the preliminary African
evidence already suggests support for all four
predictions. I will briefly mention two data
sets.
Evidence from fossils of micromam-
G
2.33 ? .03
F=0
C
2.95?.03
B-10
B
A
3.35
SARID, SEMI-ARIDSTEPPE, SCRUB
S DRY SAVANNA, SAVANNA-WOODLAND (OPEN)
MESIC SAVANNA, WOODLANDS
FOREST EDGE (CLOSED),
FOREST
GALLERY FOREST
8
FIG.11.- Relative micromammalfrequencies
in differenthabitatcategories(rectanglesat right)
indicate paleoenvironmentalchangein late Pliocene strataof the ShunguraFormation,Ethiopia.
The stratigraphicpositions of the fossil samples
are shown in relation to tuffs A-G (at left) with
radiometricdates(MYR = millionsof yearsagoAdapted from Fig. I of Wesselman, 1985).
mals.--Wesselman (1985) analyzedchanges
in frequencies of micromammals (rodents,
insectivores, bats, and other small mammals) in categories from mesic-closed to
open-xeric habitats from successive strata
of the ShunguraFormation, near the Ethiopian equator (Fig. 11). This work shows a
strong shift, somewhere between just > 2.5
and 2.4 million years ago, towards species
indicative of more open, arid, and seasonally colder environments. Near 2.9 million
years ago, Wesselman (1985) recordsmammals, such as Demidoffs bushbaby, Galago
demidovii, and several species of bats, that
are today restricted to closed-canopy rainforest. In contrast, near 2.5 million years
ago in the same stratigraphicsequence,there
24
JOURNAL OF MAMMALOGY
appear forms that are today semidesert- or
desert-adapted,such as a gerboaspecies(Jaculus), and a close relative of the naked
molerat, Heterocephalusglaber.
Wesselman's (1985) data contain evidence from near the African equator, over
the time period of the main American Interchange,that the climate cooled and aridifled markedly, that taxa immigrated from
high-latitude grasslands and steppes, and
that there were local extinctions and originations. Palynological data for the same
stratigraphicsequenceand time period also
indicate a change from more wooded to
more open conditions (Bonnefille, 1976,
1983).
Evidence from Bovidae. -The stratigraphic distribution of all subsaharanspecies of antelopes (Bovidae) over the time
interval 3.3-1.0 million years (Fig. 12) provides similarevidence.Taxawith globalfirst
records near 2.5 million years ago bear the
unmistakeablestamp of the spreadof grassland and aridification.Examplesare taxa of
the open-grasslandAlcelaphini, like the genus of giant hartebeests (Megalotragus),a
new species of springbuck(Antidorcassp.),
and the genus of giant buffaloes(Pelorovis).
Pelorovis,throughoutits subsequentrecord,
is associated with cold open environments
(Vrba, 1987b).
The ancestors of the lineages mentioned
so far, based on cladistic analyses,were African tropical endemics. But several other
taxa appearingnear 2.5 million years ago
seem to be immigrants from Eurasia(Fig.
12), like Antilope, the genus of the modem
Indian blackbuck, and possibly the genus
Oryx. Other immigrant taxa, like Equus,
also appear first in Africa near 2.5 million
years ago. Definitive fossils of the genus
Homo are firstrecordedat about 2.1 million
years ago, and stone tools (widely seen as
evidence of the hominine behavioral phenotype) first appear near 2.5 million years
ago (review in Vrba, 1988).
Evidence is mounting that many groups
of animals (in addition to micromammals
and antelopes)and plants experiencedturn-
Vol. 73, No. I
over close to 2.5 million yearsago. This part
of the African record, and indeed of the
global record, may upon additional study
be found to be a massive turnover-pulse,
namely a concentration across different
phylogeniesof migrations,extinctions, and
speciations coincident with global climatic
cooling (Vrbaet al., 1989). But this remains
speculative at present. A statisticaltest applied to the estimated dates of first appearances in Fig. 12 (Vrba, 1988, which cites
errorlimits for the relevantradiometricand
paleomagneticdates) indicatesthat a statistically significant number of first appearances of subsaharanBovidae fall between
ca. 2.6 and 2.4 million years ago.
CONCLUDINGCOMMENTS
A set of compatiblehypotheses, the habitat theory, offersan alternativeto the competition paradigm,namely to the traditional
emphasis on interspecies competition as a
cause of extinctions and on empty niches as
causal influencesin phylogeneticradiation.
The major featuresof the Great American
Interchangeof mammals, often claimed as
the best paleontological evidence for the
competition paradigm, may well turn out
to be more consistently and testably explained in a completely different way, by
the habitat theory.
It is apparentthat much of my argument
remains speculative and untested. I offer
these preliminaryideas neverthelessin the
hope that there is indeed room in our field
for the "bold ideas, unjustified anticipations, and speculative thought" that accordingto Popper (1968:280) "areour only
means for interpretingnature." Once the
habitat-theoryis tested rigorously,it may
turnout to be wrongat least in part.I would
be genuinely pleased if my "unjustifiedanticipations" were to stimulate studies that
indicate which parts of the habitat theory
are wrong,and which need to be sharpened
and added to.
The hypothesesand tests, presentedhere,
drawon diverse subdisciplines,such as systematics based on molecular and morpho-
1992
February
ANDEVOLUTIONARY
VRBA-MAMMALS
THEORY
25
OFAFRICAN
BOVIDAE
BIOCHRONOLOGY
EASTERN AND EASTERN-SOUTHERNSPECES
L
LLL28293031323334353637383940414243
o1.5
o
LL
---SOUTHERN ENDEMICSLL
L
LL
444w5545567565890061
0
MI
iM
ccI
S2.01
z
02.5-
I
I
3.0-
1 IMMIGRANT
L= LIVING
I
1
2
3 4
5
6
7 8
9101
12 13 14 15155 17I0
19D202122
46
4wVa49
23 24 25 2627
WW
50
51
53
of subsaharan
AfricanBovidaefrom3.3 to 1.0 millionyears.Eachline
FIG.12.-Biostratigraphy
a
and
48,whichmayeachreferto morethanonespecies.Numbered
representsspecies,except2, 24, 30,
taxa are Bovini: Syncerus (2), Simatherium (9), Hemibos (23), Pelorovis(32); Tragelaphini:Tragelaphus (4, 17, 18, 20, 22, 34, 47, 57), Taurotragus(51, 61); Reduncini:Kobus(3, 5, 13, 19, 28, 33),
Menelikia (16, 26, 27), Redunca (52); Hippotragini:Praedamalis (6), Oryx (30), Wellsiana (46),
Hippotragus(50); Neotragini:Madoqua(12), Oreotragus(53), Raphicerus(6); Antilopini:Antidorcas
(15, 29, 59), Gazella (11, 21, 36, 48), Antilope (25); Ovibovini: gen. indet. (24, refers to Shungura
recordonly), Makapania (49); Peleini:Pelea (8, 58); Aepycerotini:Aepyceros(1); Alcelaphini:?Damalops (7), Parmularius(10, 14, 39, 40, 43, 45), Megalotragus(31), Sigmoceros(35), Damaliscus (37,
38, 42, 56), Connochaetes(41), Rabaticeras(44, 55); Tribe indet.:gen. indet. (54). Adaptedfrom Fig.
3 in Vrba(1988),whichcitesreferencesfor chronologyandtaxonomy.
logical data, ecology, behavior, biogeography, paleontology, and climatology. I hope
that I have illustratedthat mammalogy,because it can now draw on an exceptionally
rich compound set of information, is an especially favorablebreedinggroundfor raising and investigating new hypotheses of
evolution. Researchon no othermajorgroup
of organismspromises for the 1990s such a
rapidinflux of disparateinformation- from
molecular to paleontological--as does
mammalogy. This must surely lead to bold
new ideas.
ACKNOWLEDGMENTS
It has been a pleasurefor me, and a greathonor, to be invited to deliver the keynote address
at the 70th Annual Meeting of The American
Society of Mammalogistsin 1990. I am grateful
to J. Brown,L. Marshall,and D. Webb for helpful comments on this paper. S. Hochgrafis re-
sponsible for the artworkon most of the figures.
It was partly researchedwhile holding National
Science Foundation grant BSR-8907673.
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