held 27-30 October 1999 at the University of Wisconsin-Madison.
These 8 talks were in a session entitled "Bat Phylogeny and the Comparative Method"
held Friday the 29th 2:00 - 4:30 P.M.
The session was co-organized by Theodore Garland, Jr. and Ariovaldo Pereira da Cruz-Neto.
The comparative method and why phylogeny matters
Theodore Garland, Jr.
University of Wisconsin-Madison
The last 15 years have witnessed a revolution in the way species differences
are studied: the "comparative method" has been revitalized by new analytical
tools that use phylogenies and by increased phylogenetic information. Most
typically, modern analyses obtain information about one or more phenotypic
traits (e.g., wing area, metabolic rate, relative brain size, frequency
of echolocation calls, social system, diet, home range area) for a series
of species, and then "map" this information onto a phylogenetic tree that
has been obtained from independent data (e.g., DNA sequences), analyzed
with an appropriate tree-reconstruction algorithm. Usually, to avoid circularity,
the traits of interest are not used to construct the phylogeny. Phylogenetically
based statistical methods (review in Am. Zool. 39:374-388) attempt to account
for the fact that related species tend to resemble each other, and hence
that their phenotypes cannot be considered as independent and identically
distributed data points for analyses. These techniques allow traditional
topics in comparative and ecological physiology, functional morphology,
and behavioral ecology to be addressed with greater rigor. Examples include
studies of the form of allometric relationships, prediction of values for
unmeasured species, correlated character evolution and coadaptation, and
whether characteristics of organisms vary consistently in relation to behavior,
ecology or environmental characteristics, which can constitute evidence
of adaptation (results of natural selection). These methods can also address
topics that are unapproachable without phylogenetic information, such as
where and when a trait first evolved, its value in hypothetical ancestral
species, and whether rates of evolution have differed among evolutionary
lineages (clades). Although most powerful with complete phylogenetic information,
the procedures can incorporate uncertainty about topology (polytomies:
Syst. Biol. 48:547-558), branch lengths, and the way characters have evolved.
Three general methods will be discussed: reconstruction of ancestral states
(Evolution 51:1699-1711), phylogenetically independent contrasts (Am. Nat.
125:1-15), and Monte Carlo computer simulations to obtain phylogenetically
correct null distributions (Syst. Biol. 42:265-292). Free software to implement
these techniques is available from the author.
Phylogenies and where they come from: conflict, concurrence, and the comparative method
John A. W. Kirsch
The University of Wisconsin Zoological Museum
The types of characters and algorithms used to generate phylogenetic
trees bear an intimate, and often unrecognized, relation to each other:
not all characters are suited to the same analytical method, and vice versa.
Parsimony, for example, has as its first assumption the independence of
unit features, an assumption that may at least in principle be met by disparate
anatomical characters but rarely by the sequence of bases in a single gene.
On the other hand, analogues of the plausible models for DNA evolution
- such as those accounting for the influence of transition:tranversion
ratios, saturation, base-compositional bias, differential weighting of
portions of a gene, etc. - are unknown for anatomy and enhance the power
of computer methods appropriate for molecules. Yet, conservative assumptions
that base changes are unordered and non-polarized effectively renders sequence
analysis "phenetic" (in the sense of "based on overall similarity"). In
this, the results resemble those of distance-generating methods (serology,
DNA hybridization). As regards bat phylogeny, molecular trees confirm the
monophyly of many family-level groups inferred from anatomy, and appear
to "solve" several conundra such as the affinities of Mystacina; but they
differ from tradition markedly at higher levels, especially concerning
the time-honored subordinal dichotomy between megabats and microbats, uniformly
recovering a sister-group relation between Pteropodidae and Rhinolophoidea.
Because widely-applied combinability tests assess only length differences
rather than branching orders among trees, and because few techniques are
capable of combining data when taxa or characters differ among studies,
it is premature to adopt the results of a global or "total-evidence" analysis
until the algorithmic or other reasons for such conflicting results are
understood. The more general lesson is that differing trees corresponding
to various classes of data may have equal legitimacy. The dilemma this
poses for comparative-methodologists is that whereas a single tree can
be provided, it may not be the (most) correct one; several phylogenetic
hypotheses need to be examined. However, the plausibility or otherwise
of the reconstructions of character-evolution on multiple trees may contribute
to a considered choice amongst phylogenies.
Bat phylogeny: refinements in the morphological perspective
William A. Schutt, Jr.1,2 and Nancy B. Simmons1
1 Department of Mammalogy, American Museum of Natural History,
New York, NY
2 Natural Science Division, Southampton College of Long Island University, Southampton, NY
Although much recent systematic work has been based on molecular data,
analysis of morphology continues to provide considerable insight into bat
relationships. Recently published studies of higher-level bat phylogeny
by Simmons and her colleagues have provided strong support for monophyly
of many traditionally recognized groupings. However, the level of taxonomic
sampling in these studies, which used families and subfamilies as the terminal
taxa, resulted in significant polymorphism in the data set. Particularly
problematic taxa include many of the large and diverse families (e.g.,
Pteropodidae, Phyllostomidae, Molossidae, and Vespertilionidae). Sampling
at the family/subfamily level has also made combining morphological and
molecular data sets difficult since in many cases, molecular data are sampled
at the species level. To address these problems, we are assembling a new
morphological data set designed to test higher-level bat relationships
using multiple species-level exemplars. Taxa have been chosen so as to
insure availability of morphological specimens (i.e., skins, skulls, and
fluid-preserved specimens) and tissue samples from the same species. Our
data set presently includes over 350 morphological characters sampled,
as far as possible, in over 50 species representing all chiropteran families.
Characters have been drawn from multiple anatomical systems including the
musculoskeletal system, tongue, face and ears, pelage and patagia, reproductive
tract, respiratory and digestive systems, and brain. Preliminary phylogenetic
results are broadly congruent with previous studies, with some interesting
exceptions. Future work on this project will include addition of data from
more species, filling in data[ gaps in many hard-to-study anatomical systems,
and investigation of new characters. In collaboration with the Van Den
Bussche lab, we are also working to analyze our morphological data in the
context of combined analysis with molecular sequence data from the same
Phylogenetic analysis of multiple independent data sets: to combine or not?
Ronald A. Van Den Bussche1, Steven R. Hoofer1, William A. Schutt, Jr.2,3, and Nancy B. Simmons3
1Department of Zoology, Oklahoma State University, Stillwater,
2Natural Science Division, Southampton College of Long Island University, Southampton, NY
3Department of Mammalogy, American Museum of Natural History, New York, NY
With multiple independent data sets being generated for phylogenetic
analyses, several questions are emerging regarding how they should be analyzed.
For example, is it necessary for data sets to have similar numbers of characters
to prevent "swamping out" the phylogenetic information in smaller data
sets? Controversy also exists regarding how different data partitions should
be analyzed. Three approaches (total evidence, separate analyses, and conditional
combination) have been proposed for elucidating phylogenetic hypotheses
for organisms based on multiple data partitions. Although several statistical
methods exist for testing whether different data partitions can be combined
as well as for testing congruence among phylogenetic hypotheses resulting
from separate analyses, the performance of these tests has not been thoroughly
examined nor have these tests been applied on a broad taxonomic scale.
Therefore, little information is available regarding the prevalence of
significant heterogeneity among data partitions. To elucidate higher-level
phylogenetic relationships within Microchiroptera, for all taxa under study
we are generating approximately 2.7 kb of DNA sequences from three adjacent
mitochondrial genes and 350 morphological characters. Because our goal
is to provide a well resolved, well-supported phylogenetic tree for Microchiroptera,
it is necessary to compare the phylogenetic information present in each
of these data sets. The specific purpose of this study was to evaluate
the phylogenetic affinities of the New Zealand short-tailed bat (Mystacina
tuberculata) based on molecular and morphological characters. Toward this
end we (1) performed separate phylogenetic analyses and evaluated congruence
among different data sets, (2) utilized three statistical tests of homogeneity
for determining whether a "total evidence" approach could be utilized,
and (3) examined the effect of data partitions of different size and evolutionary
constraints on the resulting phylogenetic trees.
The phylogeny of echolocation
James M. Hutcheon, Theodore Garland, Jr., and John A.W. Kirsch
Department of Zoology and University of Wisconsin Zoological Museum, Madison
Ongoing controversies in bat systematics concern not only the interrelationships
of chiropteran families, superfamilies, and sub-orders, but also the identity
of the nearest likely outgroup of bats. Echolocation is frequently pointed
to by all sides in this debate as relevant to their particular phylogenetic
hypotheses. Under the standard or "flight first" hypothesis, where powered
flight is considered the most general uniting feature of chiropterans,
pharyngeal sonar is viewed as a synapomorphy of Microchiroptera, never
having evolved in Megachiroptera; the "echolocation first" scenario, in
contrast, mandates the loss of this capacity in megabats. Recent molecular
work, however, challenges the categorical distinction between microbats
and megabats, allying at least Rhinolophoidea with the Pteropodidae, and
thus raises the possibility that echolocation evolved twice among chiropterans.
But echolocation is not a unitary anatomical feature nor is it expressed
in the same manner in all bats which possess it. The comparative method
provides a means of assessing the evolution of traits by taking relationships
- as expressed in a phylogenetic tree - into account, thus reducing spurious
correlations caused simply by shared ancestry. Body mass, foraging strategy,
and echolocation call-frequency are considered to be associated. Examining
the hypothesis that foraging strategy in bats is related to body mass in
a phylogenetic context provides an opportunity to account for what might,
in fact, be a phylogenetic constraint. Likewise, although everyone "knows"
that megachiropteran bats are larger than many microbats, does variance
in body size represent a statistically significant difference, or do mean
differences between suborders fall within the expected variance of an evolutionary
process? Finally, reference is often made to the large number of extant
bat species, with the explicit assumption that echolocation, flight, or
both represent a key innovation(s) allowing for the diversification observed
in bat species today. However, while the notion of echolocation as a key
innovation has been marshalled as an argument to support all of the competing
phylogenetic theories, it this hypothesis has not been the subject of a
rigorous, statistical assessment.
Size matters: scaling and the evolution of flight and echolocation in bats
Hector T. Arita
Instituto de Ecologia, UNAM; Apdo. Postal 27-3 (Xangari); CP 58089 Morelia, Mich.; MEXICO
The maximum body mass for bats is three orders of magnitude lower than
the weight of the largest terrestrial mammals and one order of magnitude
below the theoretical limit for a flying vertebrate. I suggest that three
types of constraints could be limiting the size of bats: (1) those associated
with flight; (2) those associated with echolocation, especially the coupling
of flight and echolocation in aerial-hawking species; (3) phylogenetic
constraints. Flight alone might limit the size of megabats, but other constraints
(associated with diet, roosting habits or viviparity) could be acting as
well. At least in some aerial insectivorous microbats, wing flapping and
echolocation sound production are coupled to save energy, so one echolocation
call corresponds in time to one wing beat. In theory, pulse repetition
rate (PRR) and wing-beat frequency (WBF) should scale with body mass with
the same exponent to yield PRR/WBF ratios equal to one. However, the exponents
vary among taxa, showing that some bats donít couple the two functions.
I traced changes in body mass, PRR, and WBF along N. Simmonsí phylogeny
of bats to infer the possible effects of diet, echolocation call design,
and phylogenetic constraints on body size among different bat lineages.
I found three generalized patterns: First, high-intensity echolocation
and its coupling with flight constrain size in aerial-feeding insectivores.
Second, in lineages with species using low-energy echolocation ("whispering"
bats), some species have attained comparatively large sizes, notably among
frugivores and carnivores. However, even these bats are much smaller than
the largest Megachiroptera. Finally, lineages of bats using high-duty,
constant-frequency echolocation calls show a secondary reduction in body
size. I conclude that: (1) flight constrains size in all bats, (2) an additional
constraint must be limiting the size of Megachiroptera, (3) size in Microchiroptera
is constrained by echolocation, (4) aerial insectivores are particularly
small, apparently because of energetic constraints, (5) size in frugivores
and gleaners are limited to a lower degree by echolocation constraints,
and a phylogenetic constraint might be acting, (6) a different mechanism
must be limiting body size in bats with high-duty echolocation.
Bat life-histories: testing models of life-history evolution in mammals using a comparative phylogenetic approach
Kate E. Jones* and Ann MacLarnon
School of Life Sciences, Roehampton Institute London, London, SW15 3SN, UK
The evolution of bat life-histories (Mammalia: Chiroptera) was examined to investigate patterns of life-history covariation and to test Charnovís (1991) mammalian model of life-history evolution. Life-history data was collected from the literature for 308 bat species. Data were tranformed into phylogentically independent data using Felsensteinís (1985) method of independent comparisons, modified by Pagel (1992) and implemented by the computer program CAIC (Purvis & Rambaut 1995). As no single estimate of the phylogenetic relationships for all the taxa under investigation was available, we calculated a ëphylogenetic supertreeí (Sanderson et al. 1998) from 53 different systematic studies to cover the taxa required. Branch lengths in the phylogeny were set to the same arbitrary value in the CAIC program and the adequate standardisation of the contrasts was checked prior to analysis (Garland et al. 1992). With phylogenetically independent contrasts, several of the bat life-history variables investigated were correlated with body mass but others were independent of body mass. The allometric scaling of the life-history variables was not significantly different within the two suborders of bats. Covariation of bat life-history traits was also examined. Although differences were found in the pattern of bat life-history covariation compared to other mammals, fundamental similarities remain; for example, low mortality rates are correlated with late ages at maturity. This means that the ëfast-slowí continuum found to operate in other mammals is also found among bat species. The life-history covariation found within bats supports, or at least not strongly refute, Charnovís (1991) model. Charnovís predicted values for the allometries and interrelationships of juvenile period length (a) and adult mortality (M), and his predicted invariants, are supported for bat species. However, annual fecundity (b) is not significantly correlated with body size as Charnov predicts. A more recent life-history model developed by Kozlowski and Weiner (1997) may explain some of the patterns observed for bat life-histories but empirical analyses have yet to be performed.
*Current Address: Department of Biology, Imperial College at Silwood
Park, Ascot, Berkshire, SL5 7PY, UK
The relationship between body mass, phylogeny,
diet, and basal metabolic rate in phyllostomid bats:
a computer-simulation approach
A. P. Cruz-Neto and A. S. Abe
Departamento de Zoologia, IB, UNESP, CP 199, CEP 13506-900, Rio Claro, SP, Brasil
Controversy exists as to what factors affect the basal metabolic rate (BMR) in mammals, once the pervasive effects of body mass have been controlled. For example, various authors have suggested that BMR varies also in relation to diet or phylogeny. We examined these factors in the bat family Phyllostomidae. We first used conventional analysis of covariance (ANCOVA) to test the effects of diet on BMR, while controlling for effects of body mass. This conventional analysis assumes that all species evolved simultaneously from a single common ancestor (i.e., a star phylogeny with equal-length branches) and a Brownian motion model of character evolution. In this analysis, diet exerted a strong effect on mass-corrected BMR. We next used a phylogenetically informed analysis involving Monte Carlo simulations along a specified phylogenetic tree and under different models of character change. The PDSIMUL computer program (Syst. Biol., 1993, 42:265-292) was used to simulate the evolution of body mass and BMR thousands of times, and these data were then analyzed in the same way as for the one set of real data. The F statistic for the real data set was compared to the distribution of F statistics from the computer-simulated data. In this analysis, no effect of diet on BMR was observed, irrespective of the evolutionary model assumed. In both conventional and phylogenetically informed analyses, body mass exerted a strong effect on BMR: larger-bodied species had lower mass-specific metabolic rates. Owing to the fact that diet is perfectly confounded with phylogeny in the set of 19 species examined, even if diet did exert an effect on BMR in the phylogenetic analysis, it would not be possible to separate this effect from the possibility that these phyllostomid bats differ for some other reason besides diet. This points to the need for careful selection of study species if one hopes to elucidate the effects of ecological or behavioral factors on aspects of bat biology.
Supported by Grants from Conselho Nacional de Desenvolvimento Científico
e Tecnológico (CNPq) and from Fundação de Amparo à
Pesquisa do Estado de São Paulo (FAPESP grant 97/02731-8) to A.
P. Cruz-Neto. A. S. Abe was supported by a FAPESP grant (1994/6026-9).