systematics of the desmodontinae and phyllonycterinae

SYSTEMATICS OF THE DESMODONTINAE AND PHYLLONYCTERINAE

(CHIROPTERA: PHYLLOSTOMATIDAE) BASED ON G-BAND

CHROMOSOMAL HOMOLOGIES

by

Rebecca A. Bass, B. S. in CYTO.

A THESIS

IN

ZOOLOGY

Submitted to the Graduate Faculty of Texas Tech University in Partial Fulfillment of the Requirements for

the Degree of

MASTER OF SCIENCE

Approved

Accepted

May, 1978

ACKNOWLEDGEMENTS

I thank my major professor, Dr. R. J. Baker, for his support,

encouragement, and commitment to my graduate training and research

endeavors. I gratefully acknowledge the other members of my committee.

Dr. R. C. Jackson and Dr. J. S. Mecham, for their advice and assistance,

Dr. D. C. Carter, P. G. Dolan, I. F. Greenbaum, R. L. Honeycutt, M.

A. O'Connell, J. C. Patton, and T. L. Yates also critically reviewed

this thesis. Laboratory assistance was provided by R. K. Barnett,

P. G. Dolan, I. F. Greenbaum, P. E. Imler, and M. A. Johnson. I

thank P. V. August, Dr. R. J. Baker, A. Capparella, J. C. Davidson,

Dr. H. H. Genoways, I. F. Greenbaum, R. L. Honeycutt, and M. A.

O'Connell for assistance in obtaining specimens. This research was

financed by National Science Foundation Grant No. DEB 76-20580, the

Institute of Museum Research, and Department of Biological Sciences,

Texas Tech University. The specimen from Venezuela was obtained

through support provided by the International Environmental Sciences

Program awarded to Dr. J. Eisenberg on the ranch of Sr. T. Blohm.

11

TABLE OF CONTENTS

ACKNOWLEDGEMENTS ii

LIST OF TABLES iv

LIST OF FIGURES v

I. INTRODUCTION 1

II. MATERIALS AND METHODS 5

III. RESULTS 7

IV. DISCUSSION 12

SPECIMENS EXAMINED 22

LITERATURE CITED 24

APPENDIX 29

111

LIST OF TABLES

TABLE Page

1. Biarmed autosomal elements of Macrotus identifiable

in eight other phyllostomatid genera 30

2. Acrocentric autosomal elements of Macrotus identifiable

in eight other phyllostomatid genera 31

IV

LIST OF FIGURES

FIGURE Page

1. G-band karyotypes of Macrotus waterhousii 33

2. G-band karyotype of Diaemus 35

3. G-band karyotype of Diphylla 35

4. G-band karyotype of Desmodus 35

5. G-band karyotype of Glossophaga 37

6. G-band karyotype of Monophyllus redmani 37

7. G-band karyotype of Erophylla sezekorni 39

8. G-band karyotype of Phyllonycteris aphylla 39

9. G-band karyotype of Brachyphylla cavernarum 39

10. G-band karyotype demonstrating presumed homologies

between Macrotus and Diaemus 41


between Diphylla, Desmodus, and Diaemus 43


between Glossophaga and Macrotus 45


among Glossophaga, Monophyllus, Erophylla,

Phyllonycteris, and Brachyphylla 47


between Diaemus and Glossophaga 49

15. C-band karyotype of Diaemus 51

16. Phylogenetic relationships of desmodontines, phyllonycterine,

and glossophagine bats 53

V

I. INTRODUCTION

Bats of the family Phyllostomatidae are so ecologically and

morphologically diverse and complex (Baker £t ad., 1976, 1977)

that there is considerable confusion and disagreement on the

evolutionary and systematic affinities of subfamilies and genera

(Smith, 1976). The problem ensues from the fact that several taxa

show little morphological similarity to other taxa. It is often

impossible to determine if the few morphological similarities between

some taxa are the result of a common evolutionary history or of

convergence. The genus Brachyphylla, which as been placed in four

different subfamilies, is a good example of this problem. The

morphological similarity of Brachyphylla to at least three of these

subfamilies is probably the result of convergence.

Characters that evolve slowly enough to show past evolutionary

relationships, yet still exhibit sufficient change to distinguish

separate evolutionary lineages, are needed to resolve systematic

affinities of questionable taxa. Such criteria should be of a type

that are not likely to produce similar character states in independent

lines of evolution.

Determination of homology based on G-banded chromosomes promises

to provide considerable insight into evolutionary history. Patton

(1976) found that homologous G-band segments could be identified

among the families Phyllostomatidae, Mormoopidae, and Noctilionidae.

Furthermore, he found sufficient changes in chromosomal arrangements

to show evolutionary affinities of these groups. Baker e_t al.

(1978) also demonstrated that G-band homology could be used to

identify chromosomal elements between the phyllostomatid subfamilies

Stenoderminae and Phyllostomatinae.

This thesis is concerned with determination of G-band homology

among the taxa of the phyllostomatid subfamilies Desmodontinae

and Phyllonycterinae, and the extent that these homologies document

evolutionary history. Desmodontines and phyllonycterines each

contains three genera. Members of the Desmodontinae are sanguinivorous

(Gardner, 1977b_) and occur from Mexico south through much of South

America (Koopman, 1976), whereas species of the Phyllonycterinae

are nectarivorous and frugivorous (Gardner, 1977) and restricted

to the Antilles (Baker and Genoways, 1978).

Desmodontinae — Vampire bats were first recognized as a distinct

group, Haematophillini, by Waterhouse (1839). Although Miller (1907)

recognized vampires as a distinct family (Desmodontidae), he suggested

a possible relationship with Rhinophylla (Phyllostomatidae) based

primarily on molar structure. Winge (1892) associated Brachyphylla

with the vampire bats, but otherwise Desmodus, Diaemus, and Diphylla

have been regarded as the only members of this group. Investigations

of acoustic orientation (Novick, 1963), host-ectoparasite relationships

(Machado-Allison, 1967), structure of the pectoral and pelvic girdles

(Walton and Walton, 1968), sperm morphology, immunologic and

electrophoretic analyses, and chromosomal analyses (Forman et al.,

1968) resulted in the relegation of the Desmodontidae to subfamilial

status in the family Phyllostomatidae. This is the current taxonomic

status of the vampire bats (Jones and Carter, 1976).

Phyllonycterinae — Phyllonycteris and Erophylla originally were

regarded as glossophagines (Allen, 1898) and later designated as

the subfamily Phyllonycterinae (Miller, 1907). The genus Brachyphylla

originally was believed to be closely related to Phyllonycteris

(Peters, 1861), but Gray (1866) erected the tribe Brachyphyllina

to distinguish this genus from other phyllostomatid bats. Dobson

(1878) regarded Brachyphylla as a desmodontid, whereas Allen (1898)

associated Brachyphylla with Phyllonycteris (Brachyphyllina) in the

Stenoderminae where it remained until Silva Toboada and Pine (1969)

concluded on the basis of morphology and behavior that Brachyphylla

is "the most 'ordinary' phyllonycterine." The genera Phyllonycteris,

Erophylla, and Brachyphylla are currently recognized in the subfamily

Phyllonycterinae (Jones and Carter, 1976). Based on karyotypic

analyses, affinity of the phyllonycterines and glossophagines was

suggested by Baker and Lopez (1970), Gardner (1977aL) , and Baker (1978)

I have examined and compared the G and C-band patterns of

phyllostomatid bats of the genera Desmodus, Diaemus, and Diphylla

(subfamily Desmodontinae), Glossophaga, Monophyllus (Glossophaginae),

Erophylla, Phyllonycteris, and Brachyphylla (Phyllonycterinae), and

Macrotus (Phyllostomatinae). All genera have a diploid number of 32;

FN=60 except Desmodus (2N=28; FN=52) and Macrotus (waterhousii, 2N=46;

FN=60).

An examination of chromosomal homology among these taxa offers

an opportunity to: 1) determine intergeneric relationships within

the subfamilies Desmodontinae and Phyllonycterinae; 2) examine

evolutionary relationships of the desmodontines, phyllonycterines,

and glossophagines to each other; 3) examine the cytogenetic

mechanisms employed in their evolution from the ancestral stock

thought to be most like that of Macrotus (Patton, 1976); 5) propose

a primitive karyotype for the Desmodontinae and Phyllonycterinae;

and 6) test phylogenies proposed by Baker (1967), Smith (1976), and

Gardner (1977a).

II. MATERIALS AND METHODS

Specimens examined in this study were taken from natural

populations by mist nets. Ear, lung, or embryo biopsies were taken

at the collection sites and stored in Ham's F-IO Nutrient Mixture

supplemented with 20% fetal calf serum, 1.8% Penicillin-Streptomycin

and 0.9% Mycostatin suspension. Fibroblast tissue cultures were

initiated from tissue biopsies. Cultures were maintained in media

as described above except without Mycostatin. Five cell-line samples

from each individual were frozen at -90°C in 5% dimethyl sulfoxide

in growth medium.

Replicated chromosomes were arrested at metaphase with

0.1-0.5 ml 0.0005% Velban in 15 ml of media for 10-20 minutes.

Cells were removed with 0.25% trypsin, and karyotypes were prepared

as described by Greenbaum et al. (1978) except that 0.22% culture

media was used as the hypotonic solution.

Slides to be C-banded were left 12-24 hours at room temperature

and treated with 0.2 N HCl for 20-30 minutes, 5% BaOH at 46^0 for

2-15 minutes, IX or 6X SSC at 60°C for 45 minutes (Sumner, 1972).

C-banded slides were stained in 4% Giemsa for 10 minutes.

Mitotic cells that revealed the banding patterns of all chromosomes

were photographed using 4 X 5 Plus-X Pan professional film and printed

on F-5 kodabromide singleweight paper. To facilitate comparisons

between chromosomes, cells were printed so that all pair 6/7

chromosomes were of equal length (fig. 1). Several banded karyotypes

were prepared for each specimen examined, and homologies were determined

based on differential longitudinal staining patterns of each chromosome.

The karyotypes of each species were compared on a side by side basis

to determine homologous chromosomes shared by the various taxa.

Only complete spreads with the diploid number characteristic of the

species were used in the comparisons.

Patton (1976) used G-band data from Macrotus waterhousii as

a standard for comparing several genera of phyllostomatoid bats.

For comparison of the other genera examined in this study, specimens

of M. waterhousii (2N=46; FN=60) were G-banded, from which a standard

was constructed (fig. 1). Biarmed autosomes of M. waterhousii are

shown in the first two rows of fig. 1, whereas acrocentric elements

and the sex chromosomes are shown in the remaining four rows.

Patton's (1976) standard karyotype of M. waterhousii was arranged

in a graded series with each autosomal arm consecutively numbered.

The numbering scheme employed in fig. 1 essentially follows that

of Patton (1976) except that Patton's chromosomes numbered 18 and 14

are my numbers 22 and 12, respectively.

III. RESULTS

Results of G-band studies are as follows: Diaemus youngii (fig. 2,

2N=32; FN=60), Diphylla ecaudata (fig. 3, 2N=32; FN=60), Desmodus

rotundus (fig. 4, 2N=28; FN=52), Glossophaga soricina (fig. 5, 2N=32;

FN=60), Monophyllus redmani (fig. 6, 2N=32; FN=60), Erophylla

sezekorni (fig. 7, 2N=32; FN=60), Phyllonycteris aphylla (fig. 8,

2N=32; FN=60), and Brachyphylla cavernarum (fig. 9, 2N=32; FN=60).

In figures 10-14, intergeneric G-band comparisons are made by

showing one element of each homologous pair for each species.

G-banded karyotypic comparisons include Macrotus to Diaemus

(fig. 10), Diphylla to Desmodus to Diaemus (fig. 11), Glossophaga

to Macrotus (fig. 12), Glossophaga to Monophyllus to Erophylla to

Phyllonycteris to Brachyphylla (fig. 13), and Diaemus to Glossophaga

(fig. 14). Elements considered as homologous between respective

species are paired to show the degree to which longitudinal banding

patterns are similar. Segments for which no homologous counterparts

could be identified between the karyotypes under consideration are

shown unpaired. A summation of proposed homologies among Diaemus,

Diphylla, Desmodus, Glossophaga, Monophyllus, Erophylla, Phyllonycteris,

and Brachyphylla with Macrotus is given in tables 1 and 2. C-banded

chromosomes of Diaemus are shown in fig. 15.

Diaemus-Macrotus — Five autosomal pairs (4/5, 6/7, 15/16, 19/20,

and 25/26) are unchanged between these two genera (fig. lOA). The

8

X and Y chromosomes also are indistinguishable between the two

genera (fig. lOA). Eight elements (3, 9, 12, 13, 18, 22, 27, 28)

that are acrocentric (as defined by White, 1945) in Macrotus appear

as arms of biarmed elements (18/3, 12/13, 27/9, 28/22) in Diaemus

(fig. lOB). Chromosome 8 (acrocentric in Macrotus) is subtelocentric

in Diaemus and differs from Macrotus by a pericentric inversion

(fig. lOB). The relationship of the elements in fig. IOC are more

complex. It is clear that chromosomal arms 21 and 17 of biarmed

elements of Diaemus are homologous to acrocentric elements of

Macrotus as indicated in fig. IOC. However, if the Macrotus biarmed

chromosomes 23/24 and 10/11 are homologous to individual chromosomal

arms are indicated (fig. IOC), either a pericentric inversion that did

not alter the banding patterns, or a centric transposition must have

occurred prior to translocation.

Homology of the Diaemus chromosome labeled 14 is unclear but

could be the result of a pericentric inversion in chromosome 14 of

the Macrotus condition and subsequent loss of translocation of a

small acentric fragment. Biarmed chromosome 1/2 of Macrotus is

homologous to two biarmed chromosomes of Diaemus. These chromosomal

arms appear to differ by fission-fusion and pericentric inversions.

Diphylla-Desmodus-Diaemus — Ten autosomal elements that appear

unchanged in Diphylla, Desmodus, and Diaemus are 18/3, 13/12, 17/10-11,

27/9, 23-24/21, 4/5, 6/7, 1, 2, and 14 (fig. U A ) . The X chromosomes

are also identical in these three genera. The Y chromosomes of Diaemus

and Diphylla appear identical (fig. IIA). Inasmuch as no male of

Desmodus was examined, homology of the banding pattern of the Y for

this genus is not known. Two identical autosomal elements, 15/16

and 19/20, in common between Diphylla and Diaemus contain additional

translocated segments in Desmodus (fig. IIB); here, the segment

translocated to the 15/16 is interpreted as chromosomal arm 28, and

that translocated to 19/20 appears to be chromosomal arm 22. In

Diphylla, elements 28 and 22 are biarmed and differ from the acrocentric

condition of Macrotus by a pericentric inversion. In Diaemus (fig. IIB),

chromosomal arms 28 and 22 are united, neither arm displaying the

inversions seen in Diphylla. In Diaemus chromosomes 25/26 and 8 are

separate elements, whereas in Desmodus and Diphylla, chromosome 25/26

appears to have been inverted (pericentric) and translocated to

chromosome 8.

Glossophaga-Macrotus — Five autosomal pairs (4/5, 6/7, 15/16,

19/20, and 25/26) and the X and Y chromosomes are identical between

Glossophaga and Macrotus (fig. 12A). Eight elements (3, 8, 9, 13,

17, 22, 27, and 28) that are acrocentric in Macrotus constitute

arms of biarmed elements (8/9, 17/3, 28/13, and 27/22) in Glossophaga

(fig. 12B). Chromosome 1/2 of Macrotus seems to have undergone a

fission, and chromosome 18 is translocated to arm 2. Chromosomal

arm 1 has probably undergone a pericentric inversion. It is clear

10

that chromosomal arms 12 and 21 of biarmed elements of Glossophaga

are homologous to acrocentric elements of Macrotus as indicated in

fig. 12C. If the Macrotus biarmed chromosomes 10/11 and 23/24 are

homologous to individual chromosomal arms of biarmed chromosomes of

Glossophaga as proposed (fig. 12C), either pericentric inversions

that did not alter the observed banding patterns or centric

transpositions must have occurred prior to fusion. Pericentric

inversions in acrocentric elements 14 and 29, as are characteristic

of Macrotus, could have given rise to the biarmed chromosomes

observed in Glossophaga (fig. 12C).

Glossophaga-Monophyllus-Erophylla-Phyllonycteris-Brachyphylla —

Proposed homologies for Glossophaga, Monophyllus, Erophylla,

Phyllonycteris, and Brachyphylla are shown in fig. 13. No differences

were observed among these five genera, and all chromosomes appear

homologous and unchanged in G and C-banding patterns. In construction

of fig. 13, chromosome 17/3 of Phyllonycteris was cut at the centromere

and aligned to save space.

Diaemus-Glossophaga — Proposed homologous elements between Diaemus

and Glossophaga are shown in fig. 14. Homologous autosomes unchanged

in banding patterns between the two genera are 4/5, 6/7, 15/16, 19/20,

25/26, 23-24/21, and the sex chromosomes. Homologous arms of biarmed

elements are shown in fig. 14B. Chromosomes 2 and 8 of Diaemus

11

involve inversions from the Macrotus condition as shown in fig. 10.

Chromosomes for which homology is suspect are shown in fig. 14C.

C-band patterns of Diaemus youngii are shown in fig. 15.

Diaemus was found to have the greatest amount of constituitive

heterochromatin. C-banded patterns of all other genera examined

revealed only minute amounts of centromeric constituitive

heterochromatin. Most of the constituitive heterochromatin in

Diaemus is telomeric; whereas no telomeric heterochromatin was

observed in any of the other genera. It appears that constituitive

heterochromatin does not play a major role in chromosomal evolution

of these bats.

IV. DISCUSSION

Primitive karyotype for the family Phyllostomatidae — One of the

most important aspects in a study of this nature is the determination

of primitive versus derived character states (plesiomorphic versus

apomorphic, Hennig, 1966). Based on outgroup comparisons, Patton

(1976) proposed a primitive karyotype for the family Phyllostomatidae

identical to that of Macrotus waterhousii (2N=46; FN=60), as shown in

fig. 1. The following discussion is an attempt to provide the most

parsimonious explanation for the changes required to derive the

chromosomal character states observed in living species from the

proposed primitive karyotype.

Chromosomal banding data from the Glossophaginae, Desmodontinae,

and Phyllonycterinae support Patton's (1976) hypothesized primitive

karyotype for the Phyllostomatidae. The proposed primitive karyotype

contains eight pairs of biarmed autosomes (1/2, 4/5, 6/7, 10/11,

15/16, 19/20, 23/24, and 25/26), and the remaining 14 pairs of

autosomes are acrocentric. Symplesiomorphies (shared derived

character states, Hennig, 1966) in the desmodontine, glossophagine,

and phyllonycterine lineages are represented by the retention of five

biarmed pairs present in Macrotus (4/5, 6/7, 15/16, 19/20, and 25/26).

Pairs 10/11 and 23/24 have been maintained as single linkage groups

but are altered by pericentric inversions in these three subfamilies.

One hypothesized primitive biarmed pair (chromosome 1/2) is not found

in any of the species of glossophagines, phyllonycterines, or

12

13

desmodontines. Chromosome 1/2 is maintained as a single element

in the families Mormoopidae and Noctilionidae (Patton, 1976) and

the phyllostomatid subfamilies Phyllostomatinae (Patton, 1976) and

Stenoderminae (Baker et^ al. , 1978) . Based on these data, the most

parsimonious explanation for the independence of chromosome arm 1

and 2 in the Glossophaginae, Phylloncterinae, and Desmodontinae

is a fission of the primitive 1/2 chromosome in the line which gave

rise to these three subfamilies.

Comparison of Glossophaga and Diaemus karyotypes (fig. 14)

suggests several independent fusions between primitive acrocentrics.

These data are best explained by karyotypic orthoselection for a

reduction of diploid number in these two lineages by Robertsonian

fusion, but involving different chromosomes in the two groups.

Chromosomal evolution of the Glossophaginae, Phylloncterinae and

Desmodontinae — Proposed chromosomal evolution for the phyllostomatid

subfamilies Glossophaginae, Phyllonycterinae and Desmodontinae is

shown in fig. 16. The primitive karyotype for the ancestor of these

subfamilies was similar to that of Macrotus waterhousii, with the

following changes: there was a fission in 1/2, biarmed chromosome

23/24 was inverted to an acrocentric and translocated to 21, biarmed

chromosome 10/11 was inverted to form an acrocentric, and acrocentric

14 was inverted resulting in a biarmed element. The karyotype of the

progenitor therefore had 2N=46; FN=58. I propose that at this point

14

two clades diverged to establish a glossophagine-phyllonycterine

lineage and a desmodontine lineage.

In the desmodontine lineage, acrocentric chromosomes fused

to form biarmed elements 18/3, 12/13, 17/10-11, and 27/9. Additionally,

chromosomes 1, 2, and 8 underwent pericentric inversions. These

events reduced the diploid number to 34 and the fundamental number

was increased to 60. These changes resulted in the karyotype proposed

as characteristic for the stock that gave rise to the three extant

vampire bat genera.

Based on nonpreferentially stained material, Gardner (1977a )

reported that the karyotypes of Diaemus and Diphylla are identical

and, incorporating morphological data, concluded that Desmodus and

Diaemus are related more closely to each other than either is to

Diphylla. However, my data reveal that the karyotypes of Diaemus

and Diphylla are not identical and suggest greater affinity between

Desmodus and Diphylla.

A translocation of the 25/26 to the short arm of the inverted 8

in common between Diphylla and Desmodus suggests that these genera

are more closely related to each other than either is to Diaemus.

Diphylla and Desmodus appear to have diverged after the establishment

of this synapomorphy (shared derived character, Hennig, 1966). The

only autapomorphy (unique derived character, Hennig, 1966) of Diaemus

is a fusion of 28 with 22 resulting from pericentric inversions in

acrocentric elements in the Diphylla lineage. In Desmodus, two

15

autapomorphies resulted from a translocation of 22 to the short arm

of 19/20 and of 28 to the short arm of 15/16.

In the glossophagine-phyllonycterine lineage, acrocentric

chromosomes have been fused to form biarmed chromosomes 8/9, 17/3,

28/13, 27/22, 18/2, and 12/10-11. These fusions, plus an inversion

in 29, changing an acrocentric to a biarmed chromosome, explain the

evolution of the karyotypes of Monophyllus, Glossophaga, Erophylla,

Phyllonycteris, and Brachyphylla (2N=32; FN=60).

Systematic implications — These data indicate that the Desmodontinae,

Glossophaginae, and Phyllonycterinae shared a common ancestor after

separating from the lineage that gave rise to the Phyllostomatinae.

Such a relationship is supported by the studies of Forman et_ al.

(1968) and Straney et . (1978). Convergence is not likely to

have occurred in such a large number of synapomorphic character

states (pericentric inversions in 14 and 10/11; pericentric inversion

in 23/24 with translocation to 21; and a fission of 1/2). The number

of synapomorphic character states in the glossophagines and

phyllonycterines not shared by the vampires indicate that these

two lineages diverged early in the scheme of their chromosomal

evolution.

The essentially identical karyotypes of the genera Glossophaga,

Monophyllus, Phyllonycteris, Erophylla, and Brachyphylla leave little

doubt that this karyotype was characteristic of their common ancestor

16

and not the result of convergence. These data could be interpreted

in two ways. Either the karyotype for the phyllonycterines and

glossophagines is like that of the progenitor for the entire

Glossophaginae and Phyllonycterinae, or this karyotype is derived

and the Phyllonycterinae represent an offshoot of a Glossophaga

and Monophyllus lineage.

The systematic implications of these two possibilities are

quite different. In the first case, the subfamily Phyllonycterinae

may still be valid although the glossophagines and phyllonycterines

would be more closely related to each other than either is to the

vampires. Furthermore, all of the variant diploid numbers in the

Glossophaginae of necessity would be derived from this karyotype.

In the second case, the Phyllonycterinae cannot be considered as

a subfamily but rather represents a branch of the Glossophaginae.

Allen (1898) was the first to propose that phyllonycterines were

a subgroup of Glossophaginae. The latter alternative can be tested

by G-band analyses of other genera of glossophagine bats. These data

might indicate that an intermediate karyotype gave rise to other

glossophagines, that Glossophaga, Monophyllus, Erophylla, Phyllonycteris,

and Brachyphylla shared a common ancestor within the subfamily

Glossophaginae, and that the phyllonycterines should be included

in the Glossophaginae.

The genus Brachyphylla has had a varied taxonomic history being

moved from one subfamily to another six times. Chromosomal data clearly

17

show that this genus is closely allied with Erophylla, Phyllonycteris,

Glossophaga, and Monophyllus and is not a stenodermine or desmodontine.

Based on cranial and exomorphology, Brachyphylla is more closely

related to the phyllonycterines than to the glossophagines and is

undoubtedly a product of the radiation that gave rise to Erophylla

and Phyllonycteris (Baker and Genoways, 1978).

Morphological data suggest that Desmodus and Diaemus are more

similar to each other than either is to Diphylla (Slaughter, 1970;

Smith, 1976; Gardner, 1977a.). The affinity of Diphylla and Desmodus

indicated by chromosomal data is in contrast with morphological

similarities. This contradiction suggests either that Diphylla has

undergone more rapid morphological change^ than have Desmodus and

Diaemus, or that morphological similarity of Desmodus and Diaemus

is the result of convergent evolution.

The number of autapomorphic character states in the Glossophaga

and Diaemus lineages indicates that these groups diverged at a very

early stage in the evolution of the two subfamilies. The only

subfamily from which G-banded karyotypes have not been analyzed is

the Carolliinae. Although Stock (1975) published G-banded karyotypes

of Carollia, no homologous chromosomes could be identified upon

comparison. This probably is due to the differences in banding

techniques and degree of banding rather than because there are no

homologous elements between the two. Diploid numbers in the Carolliinae

range from 20 to 36, and fundamental numbers range from 36 to 62 (Baker,

18

1973). The X-chromosome of Carollia species and Rhinophylla fischerae

is rearranged from the X characteristic of Macrotus but is metacentric

in Rhinophylla pumilio (as it is in Macrotus). It is clear that a

great deal of chromosomal evolution has occurred in Carollia (2N=20-21;

FN=36), with the evolution of a multiple-sex chromosome determining

mechanism (Baker, 1973). However, Rhinophylla pumilio (2N=36; FN=62)

is probably most like the primitive karyotype of the subfamily and

might share apomorphic character states with either the glossophagines

or desmodontines. Subsequent studies could indicate that the carollines

diverged from the glossophagine-desmodontine lineage and might actually

be more closely related to vampires than are the glossophagines and

phyllonycterines.

Patton (1976) proposed that acrocentric elements 8 and 9 of

the primitive karyotype were represented as a single linkage group

in Micronycteris nicefori, Tonatia minuta, Mimon crenulatum,

Phyllostomus discolor and P. hastatus. This would represent one

synapomorphic character state among the phyllostomatines, glossophagines,

and phyllonycterines. However, derived chromosomal elements 10-11,

23-24, 14 inverted, and fission of 1/2 (synapomorphies among the

glossophagines, phyllonycterines, and desmodontines) are not found

in the phyllostomatine clade. Therefore, I suggest that fusion of

the 8 and 9 in the phyllostomatine clade is a convergent event

(homoplasia) and does not indicate common ancestory with the

glossophagines.

19

Patton (1976) identified chromosomal arms 18/3 in the noctilionids

and mormoopids. Because this would represent a synapomorphic character

between Diaemus and the mormoopids, I question this homology. Patton

(1976) was not able to order some of the chromosomes of the Macrotus

standard by size differences due to overcontraction of the chromosomes.

Apparently chromosome 22 was misidentified as 18 (personal

communication); therefore, Patton's 18/3 would equal my 22/3 and

would not represent a synapomorphy among the noctilionids, mormoopids,

and desmodontines.

Trends in chromosomal evolution — The diploid number of 32 with an FN=60

was attained in Diaemus, Diphylla, and the glossophagine-phyllonycterine

lineages via different routes of chromosomal evolution. The fact that

many other phyllostomatid bats share these same diploid and fundamental

numbers seems best explained by convergent evolution.

The mechanisms of chromosomal evolution in phyllostomatid bats

are mainly fusion events of two acrocentric chromosomes. Those few

acrocentric chromosomes that were not fused have undergone pericentric

inversion resulting in biarmed chromosomes. It appears that the

ultimate direction of chromosomal evolution is conversion of an

acrocentric karyotype to a completely biarmed karyotype resulting in

reduction of the total number of linkage groups. Perhaps this is

advantageous by reducing the total number of different gametes

possible as meiotic products (Jackson, 1971). Thus, an immediate

effect of lowering the diploid number is a reduction in variability

20

that ensures a greater number of offspring with specific characteristics,

Variability is released from the gene pool at a slower rate if there

are fewer linkage groups. This would tend to slow the rate of

evolution in the group. Position effect of the centromere on the

genes located near the centromeric region inhibits crossing over in

these areas (Jackson, 1971). Reduced or localized chiasmata with the

establishment of supergenes may also be an important advantage.

Wilson et_ sd. (1975) hypothesized that in mammals magnitude

of karyotypic evolution is correlated with magnitude of morphological

change. Chromosomal and morphological data from the phyllonycterines

are contradictory to this hypothesis. Phyllonycteris and Erophylla

are sufficiently different morphologically from Glossophaga and

Monophyllus that classical systematists have placed them in separate

subfamilies, yet no karyotypic evolution has accompanied this

morphological divergence. Furthermore, Brachyphylla is so

morphologically distinct that it has been classified as a desmodontine,

stenodermine, and even placed in its own tribe (Brachyphyllina). This

morphological divergence has not been accompanied by gross structural

chromosomal changes dectable by G-band techniques. These data leave

little doubt that substantial morphological change is not always

associated with equally large amounts of karyotypic changes. For

instance, a study (Patton, 1976) of the G-band karyotypes of Tonatia

bid ens (2N=16) and T. minuta (2N=30) failed to reveal sufficient

chromosomal homology between the two taxa to such an extent that

21

routes of chromosomal change could not be proposed. However, on

morphological grounds, the two have long been considered congeneric.

Even though a general overview of higher taxa might correlate magnitude

of chromosomal rearrangements with magnitude of cranial and

exomorphological change, there are several cases where this is not

true.

The implication of the hypothesis of Wilson and his colleagues

(1975) is that mammals are utilizing chromosomal rearrangements

(resulting in regulator gene changes) in a cause and effect

relationship to accomplish the considerable anatomical variation

observed in the living forms of the Class. Data from the bat family

Phyllostomatidae clearly show that the proposed cause and effect

relationship does not always exist, and that selection for extensive

chromosomal change might be explained better by other hypotheses.

SPECIMENS EXAMINED

All specimens are deposited in The Museum, Texas Tech University

(TTU or TK) or Carnegie Museum of Natural History (CMNH). All

frozen cell lines are deposited in The Museum, Texas Tech University.

Brachyphylla nana, 1 female, Haitai: Dept. du Sud; 1 km E Lebrun,

TTU 22762.

Desmodus rotundus, 1 female, Venezuela: Guarico; 55 km S Calabozo,

TK 4530. 1 female, Mexico: Queretaro; 3 km N Jalpan, TK 5750.

1 female, Nicaragua: Zelaya; 4.5 km NW Rama, TK 7904.

Diaemus youngii, 1 male, Nicaragua: Managua; 0.75 mi N Masachapa,

TK 5436. 1 female,Nicaragua: Zelaya; 3 km NW Rama, TK 7850.

Diphylla ecaudata, 1 male, Mexico: Queretaro; 6.5 mi NE Pinal de

Amoles, TK 9120.

Erophylla sezekorni, 1 female, Jamaica: Westmoreland Parish;

Bluefields, CMNH 44519. 2 males, Jamaica: St. Ann Parish;

Orange Valley, CMNH 44514 and 44516.

Glossophaga soricina, 1 male, Jamaica: St. Ann Parish; Orange

Valley, CMNH 44318. 2 males, Jamaica: St. Ann Parish; Green

Grotto, CMNH 44308 and 44309.

Macrotus waterhousii, 1 male, Jamaica: St. Ann Parish; Orange Valley,

CMNH 44293. 6 males, Jamaica: St. Ann Parish; Green Grotto,

CMNH 4427 2-44276. 1 female, Jamaica: St. Ann Parish; Green

Grotto, CMNH 44277.

22

23

Monophyllus redmani, 1 female, Jamaica: Westmoreland Parish;

Bluefields, CMNH 44370. 4 males, Jamaica: St. Ann Parish;

Orange Valley, CMNH 44330-44333. 1 female, Jamaica: St. Ann

Parish; Orange Valley, CMNH 44334.

Phyllonycteris aphylla, 1 male, Jamaica: Westmoreland Parish;

Bluefields, CMNH 44536. 1 male, Jamaica: St. Ann Parish;

Orange Valley, CMNH 44523.

LITERATURE CITED

Allen, Harrison. 1898. On the Glossophaginae. Trans. Amer. Philos.

Soc: 237-266.

Baker, R. J. 1967. Karyotypes of bats of the family Phyllostomatidae

and their taxonomic implications. Southwestern Naturalist,

12(4): 407-428.

. 1970. The role of karyotypes in phylogenetic studies

of bats. Pp. 303-312. In: About bats. (B. H. Slaughter and D.

W. Walton, eds.). Southern Methodist Univ. Press, Dallas, Texas,

vii + 339.

. 1973. Comparative cytogenetics of the New World

leaf-nosed bats (Phyllostomatidae). Period. Biol., 75: 37-45.

. 1978. Karyology. ^H' Biology of bats of the New World

family Phyllostomatidae. Part III. (R. J. Baker, J. K. Jones,

and D. C. Carter, eds.). Spec. Publ. Mus., Texas Tech Univ.,

in press.

Baker, R. J. and H. Genoways. 1978. Zoogeography of Antillean bats.

Proc. Phila. Acad. Nat. Sci., in press.

Baker, R. J. and G. Lopez. 1970. Karyotypic studies of the insular

populations of bats on Puerto Rico. Caryologia, 23(4): 465-472.

Baker, R. J., J. K. Jones, Jr., and D. C. Carter, eds. 1976. Biology

of bats of the New World family Phyllostomatidae. Part I. Spec.

Publ. Mus., Texas Tech Univ., 10: 1-218.

24

25

Baker, R. J., J. K. Jones, Jr., and D. C. Carter, eds. 1977. Biology

of bats of the New World family Phyllostomatidae. Part II.

Spec. Publ. Mus., Texas Tech Univ., 13: 1-364.

Baker, R. J., R. A. Bass, and M. A. Johnson. 1978. Evolutionary

implications of chromosomal homology in four genera of stenodermine

bats (Phyllostomatidae: Chiroptera). Submitted for publication in

Evolution.

Dobson, G. E. Catalogue of the Chiroptera in the collection of the

British Museum. British Mus. (Nat. Hist.), xlii + 1-567 pp. +

30 pis.

Forman, G. L., R. J. Baker, and J. D. Gerber. 1968. Comments on the

systematic status of vampire bats (family Desmodontidae). Syst.

Zool., 17: 417-425.

Gardner, Alfred L. 1977^. Chromosomal variation in Vampyressa and

a review of chromosomal evolution in the Phyllostomidae

(Chiroptera). Syst. Zool., 26: 300-318.

Gardner, Alfred L. 1977b . Feeding habits. Pp. 293-350. ^ : Biology

of bats of the New World family Phyllostomatidae. Part II.

(R. J. Baker, J. K. Jones, and D. C. Carter, eds.). Spec. Publ.

Mus., Texas Tech Univ., 13: 1-364.

Gray, J. E. 1866. Revision of the genera of Phyllostomidae or

leaf-nosed bats. Proc. Zool. Soc. London: 111-118.

Greenbaum, I. F., R. J. Baker, and J. H. Bowers. 1978. Chromosomal

homology and divergence between sibling species of deer mice:

Peromyscus maniculatus and P. melanotis. Evolution, in press.

26

Hennig, W. 1966. Phylogenetic systematics. University of Illinois

Press, Urbana, 111., 263 pp.

Jackson, R. C. 1971. The karyotype in systematics. Ann. Rev.

Ecol. Syst., 2: 327-368.

Jones, J. K., Jr., and D. C. Carter. 1976. Annotated checklist,

with keys to subfamilies and genera. Pp. 7-38. _IS:' Biology

of bats of the New World family Phyllostomatidae. Part I.

(R. J. Baker, J. K. Jones, and D. C. Carter, eds.). Spec.

Publ. Mus., Texas Tech Univ., 10: 1-218.

Koopman, Karl F. 1976. Zoogeography. Pp. 39-47. ^ : Biology of

bats of the New World family Phyllostomatidae. Part I. (R. J.

Baker, J. K. Jones, and D. C. Carter, eds.). Spec. Publ. Mus.,

Texas Tech University., 10: 1-218.

Machado-Allison, C. E. 1967. The systematic position of the bats

Desmodus and Chilonycteris, based on host-parasite relationships

(Mammalia; Chiroptera). Proc. Biol. Soc. Wash., 80: 223-226.

Miller, G. S., Jr. 1907. The families and genera of bats. Bull.

U. S. Nat. Mus., 57: svii + 1-282.

Novick, A. 1963. Orientation in Neotropical bats. II. Phylostomatidae

and Desmodontidae. J. Mamm., 44: 44-56.

Patton, J. C. 1976. Evolutionary implications of the G-banded and

C-banded karyotypes of phyllostomatoid bats. Masters' thesis

in zoology, Texas Tech Univ., vi + 59.

Patton, J. C. and R. J. Baker. 1978. Chromosomal homology and

evolution of phyllostomatoid bats. Syst. Zool., in press.

27

Peters, W. 1861. Eine neue von Hm. Dr. Gundlach geschriebene

Gattung von Flederthieren aus Cuba. Monatsber. Konigl. Preuss.

Akad. Wiss. Berlin: 817-818.

Seabright, M. 1971. A rapid banding technique for human chromosomes.

The Lancet: 971-972.

Silva Toboada, G. and R. H. Pine. 1969. Morphological and behavioral

evidence for the relationship between the bat genus Brachyphylla

and the Phyllonycterinae. Biotropica, 1(1): 10-19.

Slaughter, B. H. 1970. Evolutionary trends of chiropteran dentitions.

Pp. 51-83. ^ : About bats. (B. H. Slaughter and D. W. Walton, eds.).

Southern Methodist Univ. Press, Dallas, Texas, vii + 339.

Smith, J. D. 1976. Chiropteran evolution. Pp. 49-69. _In: Biology

of bats of the New World family Phyllostomatidae. Part I.

(R. J. Baker, J. K. Jones, and D. C. Carter, eds.). Spec. Publ.

Mus., Texas Tech Univ., 10: 1-218.

Stock, A. D. 1975. Chromosome banding pattern homology and its

phylogenetic implications in the bat genus Carollia and

Choeroniscus. Cytogenet. Cell Genet., 14: 34-41.

Straney, D. 0., M. H. Smith, I. F. Greenbaum, and R. J. Baker. 1978.

Biochemical genetics. ^H* Biology of bats of the New World family

Phyllostomatidae. Part III. (R. J. Baker, J. K. Jones, and D. C.

Carter, eds.). Spec. Publ. Mus., Texas Tech Univ., in press.

Sumner, A. T. 1972. A simple technique for demonstrating centromeric

heterochromatin. Exp. Cell Res., 75: 304-306.

28

Walton, D. W. and G. W. Walton. 1968. Comparative osteology of

the pelvic and pectoral girdles of the Phyllostomatidae

(Chiroptera; Mammalia). J. Grad. Res. Center, Southern

Methodist Univ., 37: 1-35.

Waterhouse, G. R. 1838-1839. Mammalia. Pp. 1-97. In: The zoology

of the voyage of the H. M. S. Beagle under the command of Captain

Fitzroy R. N. during the years 1832 to 1836 (C. Darwin, ed.),

vol. 1, Part 2. Smith, Elder and Co., London.

White, M. J. D. 1945. Animal cytology and evolution. (First edition)

Cambridge Univ. Press.

APPENDIX

29

30

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Figure 2. Representative G-banded karyotype of

Diaemus youngii (2N=32; FN=60).


Diphylla ecaudata (2N=32; FN=60).


Desmodus rotundus (2N=28; FN=52).


Glossophaga soricina (2N=32; FN=60).


Monophyllus redmani (2N=32; FN=60).


Erophylla sezekorni (2N=32; FN=60).


Phyllonycteris aphylla (2N=32; FN=60)


Brachyphylla cavernarum (2N=32; FN=60)

Figure 10. Proposed homologous chromosomes between Diaemus and

Macrotus. A—Symplesiomorphic characters (Diaemus

right, Macrotus left). B—Apomorphic characters

(Diaemus center) representing fusion of Macrotus

acrocentric chromosomes and one pericentric

inversion (8). C—Represents those chromosomal

homologies in which more than one rearrangement

would be necessary to derive the condition in

Diaemus from the Macrotus condition.

Figure 11. Proposed homologous chromosomes of Diphylla (left),

Desmodus (center), and Diaemus (right). A—Represents

those chromosomes in which no G-banded pattern differences

were observed among the three genera. B—Represents

chromosomal rearrangements observed among the three

genera. Numbers refer to the scheme established in

fig. 10 for Diaemus to Macrotus.

Figure 12. Proposed homologies between Glossophaga and Macrotus.

'A—S3miplesiomorphic characters (Glossophaga right,

Macrotus left). B—Apomorphic characters (Glossophaga

center) representing fusion of Macrotus acrocentric

chromosomes and one translocation (18/2). C—Apomorphies

in which more than one event is required to derive

Glossophaga from Macrotus karyotypes and those in

which homologies could not confidently be determined

(14, 29).

/ . • ;

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17

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21

20

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Figure 13. Proposed homologous chromosomes between Glossophaga,

Monophyllus, Erophylla, Phyllonycteris, and Brachyphylla,

respectively. Chromosome 17/3 in Phyllonycteris was

cut at the centromere and aligned to save space.

Figure 14. Proposed homologous chromosomes between Diaemus (left)

and Glossophaga (right). A—Represents synapomorphic

(23-24/21) and symplesiomorphic characters. B—Represents

apomorphic characters that are the result of random fusion

events of acrocentric chromosomes. C—Represents apomorphic

characters in which homologous chromosomal arms could not

confidently be determined. No homology, of chromosome 29

of Glossophaga could be determined.

18 17 12 27 ®

1 l_

2 3 10/11

14

3

1

^ B |

1 1 29 1

c |

Figure 15. Representative C-banded karyotype

of Diaemus youngii.

Figure 16. Proposed phylogeny of phyllostomatid bats based on

G-band homology. Divergence of sister groups were

determined by autapomorphic character states.

c c

x: ^ u a. E >> o ' c (/) o .2 "><

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Fusion 18/3, 12/13, 17/10-11, 27/9

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Fusion 23-24/21 Fission 1/2 PI 14, 10/11

(2n = 46; FN = 58)

I

PRIMITIVE AUTOSOMAL KARYOTYPE

(2n = 46; FN = 60)

systematics of the desmodontinae and phyllonycterinae

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