551

Biol. Rev. (~ggz),67, pp. 551-593 Printed in Great Britain

T H E EVOLUTION OF EUTHERIAN SPERMATOZOA AND UNDERLYING SELECTIVE FORCES : FEMALE SELECTION AND SPERM COMPETITION BY E. R. S. ROLDAN', M. G O M E N D I 0 2 AND A. D . V I T U L L 0 3 Department of Molecular Embryology, A F R C Institute of Animal Physiology and Genetics Research, Babraham, Cambridge CB2 4 A T , UK Sub-Department of Animal Behaviour (Department of Zoology), University of Cambridge, Madingley, Cambridge CB3 8 A A , U K , and Museo Nacional de Ciencias Naturales, C S I C , c/Jose' Gutierrez Abascal 2, 28006-Madrid, Spain Unite' de Biologie de la Fe'condation, Station de Physiologie Animale, INRA, 78352 Jouy-en-Josas Cedex, France (Received

10December

1991,revised 7 July 1992,accepted 1 5 July 1992)

CONTENTS I. Introduction . . . . . . . . . . . . . . . 11. Aims . . . . . . . . . . . . . . . . 111. Morphology and dimensions of spermatozoa among Eutherian mammals: an overview IV. Evolutionary trends in sperm morphology and dimensions: five case studies among rodents . . . . . . . . . . . . . . . . ( I ) The genus Ctenomys (Caviomorpha: Ctenomyidae) . . . . . . (2) The genus Calomys (Myomorpha: Cricetidae) . . . . . . . (3) The Neotomini-Peromyscini (Myomorpha: Cricetidae) . . . . . . (4) The subfamily Arvicolinae (Myomorpha: Cricetidae) . . . . . . ( 5 ) The tribe Conilurini (Myomorpha: Muridae) . . . . . . . . V. Evolutionary changes in rodent spermatozoa: A model . . . . . . VI. Selective forces underlying changes in sperm morphology and dimensions . . . ( I ) Female selection . . . . . . . . . . . . . (2) Sperm competition . . . . . . . . . . . . VII. Conclusions . . . . . . . . . . . . . . . VIII. Summary . . . . . . . . . . . . . . . IX. Acknowledgements . . . . . . . . . . . . . X. References . . . . . . . . . . . . . . .

55 I 553 559 563 563

565 566 568 5 70 572 577 577 582 5 84 585 585 585

I. INTRODUCTION

T h e reproductive success of males depends mainly on the number of females, or more specifically of ova, that they fertilize (Clutton-Brock, I 988). This is particularly true among mammals, where more than 90 yo of the species are polygynous (Kleiman, 1977;Rutberg, 1983;Clutton-Brock, 1989)and only rarely do males invest in their offspring after insemination (Clutton-Brock, I 99I a). In general, mammalian males compete intensely for mating access to females and, since in many cases a few males are successful at monopolizing mating access to a number of females, the variance in male reproductive success tends to be greater than that among females (Clutton-Brock et d., 1988;Le Boeuf & Reiter, 1988).Under these circumstances, strong selective pressures have favoured the evolution of male characters that enhance mating success either by improving male competitive ability in intra-sexual contests or by making males more

552

E. R. S. ROLDAN, M. GOMENDIO AND A. D. VITULLO

attractive to females (Darwin, 1871; Fisher, 1930; Bateman, 1948; "rivers, 1972). As a result of these selective pressures males tend to grow faster than females and become larger as adults, and in many species male weaponry is larger and more elaborate than that of females (Clutton-Brock, 1991b). Sexual selection, however, does not deal solely with traits that enhance mating success: mere insemination of a female does not ensure fertilization. T h u s , it is likely that selective pressures have also acted upon features of the ejaculate that affect its fertilizing ability. When females mate with more than one male during a given reproductive cycle (i.e. polyandry), spermatozoa from rival males will compete within the female tract to fertilize the limited number of ova available (Parker, 1970; Smith, 1984). I n mammalian species in which sperm competition prevails, males tend to have larger testes in relation to their body size (Harcourt et al., 1981 ; Kenagy & Trombulak, 1986), their testes have a higher ratio of seminiferous tubules to connective tissue (Harvey & Harcourt, 1984), produce more spermatozoa (Moller, 1989), a greater proportion of the spermatozoa produced is motile ( M ~ l l e r ,1988), and males tend to copulate more frequently than in species in which females mate exclusively with one male (i.e. monandrous species) ( M d l e r & Birkhead, 1898; Ginsberg & Rubenstein, 1990). Experimental studies have shown that, when several males copulate with a female, the transfer of large numbers of spermatozoa is an effective strategy since the male who transfers more spermatozoa is more likely to sire offspring (Martin et al., 1974; Lanier et al., 1979; Dewsbury, 1984; Huck et al., 1985; Agren, 1990). T h e emphasis placed on the importance of high sperm numbers is in sharp contrast with our lack of knowledge about how sperm competition has influenced the evolution of sperm morphology and dimensions. Competition between spermatozoa from rival males is by no means the only obstacle that spermatozoa must face after ejaculation. I n order to fertilize the ova, spermatozoa must also overcome the barriers present in the female tract. T h e extent of these barriers is illustrated by the fact that out of millions of spermatozoa ejaculated into the female tract very few survive, and even fewer reach the vicinity of the ova (Suarez et al., 1990). These two selective pressures, sperm competition and female selection, are likely to have influenced the evolution of the morphology and dimensions of the sperm cell itself, but so far few studies have addressed this issue. T h e evolution of spermatozoa has been studied by using two different approaches : theoretical models and comparative studies. Theoretical models have dealt mainly with the origin of anisogamy, i.e. male and female gametes (Parker et al., 1972; Bell, 1978; Charlesworth, 1978; Maynard Smith, 1978; Parker, 1978; Hoekstra, 1980; review in Parker, 1984). T h e main conclusions drawn from these studies are that small gametes (male) may have been the ancestral form, and that anisogamy may have evolved from isogamy as the result of two opposing selective forces : zygote survival, which favours provisioning of gametes, and gamete competition, which favours maximization of the number of gametes at the expense of a reduction in gamete size. T h u s , anisogamy (two sexes) would be the evolutionary stable strategy to this conflict. T h e size of the female gametes would optimize survival of the zygote, whereas spermatozoa would be reduced in size to the minimum required to survive before fertilization. I n this way, sperm producers would have become adapted to parasitize the investment of ova producers. Comparative studies have been carried out in order to reconstruct the major

Sperm evolution in mammals

553

evolutionary changes undergone by spermatozoa. These studies have either concentrated on lower taxa or have outlined very general changes throughout the animal kingdom (e.g. Baccetti & Afzelius, 1976; Franzen, 1977; Afzelius, 1979; Baccetti, 1979, I 985, I 986, I 987 ; Jamieson, I 987 a). Species which show external fertilization and release spermatozoa into the water share a primitive type of spermatozoa which is rather simple in its morphology: a round head and a tail approximately 50 pm long with a 9 + 2 tubular structure. In a uniform environment like water spermatozoa only have to swim until they reach the ova, and this simple design is well adapted to such conditions. Although the same basic design is present in all spermatozoa a number of important changes have taken place throughout evolution. In terrestrial species with internal fertilization, spermatozoa have an elongated tail and experience a re-arrangement of mitochondria. The mammalian spermatozoon is a highly differentiated cell, and its morphology responds to the major functions that it has to perform. It is organized into two distinct structures: ( I ) a head which contains the acrosome, a secretory granule with enzymes to aid the spermatozoon when it penetrates through the oocyte vestments, and the nucleus containing the haploid genome which will be inserted into the oocyte at fertilization; and (2) a tail, containing the axoneme, mitochondria, and structural elements, which is responsible for the cell’s motility (Bedford & Hoskins, 1990). Mammals also possess nine accessory fibres in the flagellum which are probably required to swim in the more viscous fluids encountered in the female tract. The range of variation in sperm morphology is such that spermatozoa from different species can in many cases be readily recognized. Thus, spermatozoa from different species may differ in their dimensions and their overall morphology. Among mammals, the head shows the greatest variation in morphology: the simplest shape is round or oval, but in some species the head has hooks emerging from the apical end or extensions emerging from the base (see below). However, the head shows little variation with respect to its dimensions; it is the length of the tail that varies markedly between species (Cummins & Woodall, 1985). Given the diversity of mammalian sperm morphology and dimensions, these features have been used as taxonomical tools in some analyses (e.g. Rouse & Robson, 1986; Harding et al., 1987), as has been done with insect (reviewed in Jamieson, 19876) and fish spermatozoa (reviewed in Jamieson, 1991). Moreover, Eutherian species which can not be easily distinguished by their external phenotype have been shown to have very different spermatozoa (e.g. Gordon & Watson, 1986; Perez-Zapata et al., 1987; Breed et al., 1988). 11. AIMS

In this paper we will examine the evolutionary changes that spermatozoa have undergone in different groups of Eutherian mammals. We will concentrate specifically on the changes in head morphology and overall dimensions. T o achieve this aim, phylogenetic relationships inferred using other types of information, such as biogeographical, morphological, chromosomal and genic data, will be used as a basis. By superimposing the information available on sperm morphology and dimensions onto these phylogenetic trees we will examine the direction in which sperm changes have occurred. We will rely extensively on rodents because this group shows the greatest variability in sperm morphology and dimensions within Eutherian mammals (see below). The evolutionary trends emerging from this study will be integrated into

E. R. S. ROLDAN,M. GOMENDIO AND A. D. VITULLO

554 Table

Sperm dimensions and patterns of head morphology in rodent species

I.

Species

Head type"

Total sperm length (pm)

References

CAVIOMORPHA

CAPROMYID.AE Aca

3464

Jones (1975); Cummins & Woodall (1985)

Cazia porcellus

B7

106.61

Galeu musteloides

B7

44.25

Austin & Bishop (1958); Cummins & Woodall (1985) Jones (1973); Cummins & Woodall (1985)

Chznchilla laniger

Aca

46.83

Lagidium hoxi

Aca

41'0~

Aca

52.16 8495 52'39 52'42 j2.62

Myorastor coypus CAVIIDAE

C H I ~ C HLIDAE II Fawcett & Phillips (1969); Cummins & Woodall (1985) Jones (1975); Cummins & Woodall (1985)

CTESOMY IDAE Ctenomys argentinus Ctenomys australis Ctenomys holiviensis Ctenom3js conoweri Ctenom-vs dorhignyi Ctenomys jrater Ctenomys lewisi Ctenomys maulintis

Aca Aca

B8

j2.46 85.70

Ctenomys meudocinus Ctenomys opimus

B8 Aca

86.1 I 5265

Ctenomys perrensis Ctenonivs porteousi Ctenomys rionegrensis Ctenomys sp. Ctenomys steinbachi Ctenomys ralarum Ctenomys yolandae

Aca

5 1'43 83'68

B8 Aca

Aca Aca

Vitullo et al. (1988) Vitullo et al. (1988) Vitullo & Cook (1991) Vitullo et al. (1988) Vitullo et al. (1988) Vitullo & Cook (1991) Vitullo & Cook (1991) Feito & Gallardo (1976, 1982); Feito & Barros ( I 982) Vitullo et al. (1988) Feito & Gallardo (1982); Vitullo & Cook

j2.24

(1991)

B8 B8 B8

i

Vitullo et al. (1988)

B8

86.53 86.53 5 2'3 2 49'28 85'50

Aca

40'1 9

Jones ( I 975) ; Cummins & Woodall ( I 985)

Proechimys guairae

Aca

37.38

Jones (1975); Cummins & Woodall (1985)

OCTO~ONTIDAE Octodon degus

Aca

49.82

Aca

4.;'18

Rerrios et al. (1978); Cummins & Woodall (1985) Cummins & IVoodall (1985); Ortells (1 990)

Aca Aca

Vitullo & Cook (1991) Jones (1975); Cummins & Woodall (1985) Vitullo et al. ( I 988)

DASY'PROCTID-\E

12.1yoprocta pvatti ECHI~IYIDAE

Ocfodontomys gliroides

MYOMORPHA CRICETIDAE Arvicolinae Clrthrionomys glarrolus A%ficrotusagrrstis L141/licrotushirtus ( = M . agrestis hirtus) Microtus ochrogaster .Veqeofiher alleni Ondatra zibethicus S>>naptomyscooperi

B6 06

06 4cr Acr Acr

R6

86.70 103.50 I 17.00 94.40

74.90 67.70 99.70

Friend (1936) Austin (1957) Friend ( I 936) Hirth (1960) Hirth (1960) Friend (1936) Hirth (1960)

Sperm evolution in mammals Cricetinae Cricetulus griseus

Austin & Bishop (1958); Cummins & Woodall (1985) Austin & Bishop (1958); Cummins & Woodall (198 j ) Parkening (1990); E. R. S. Roldan, unpublished

258.32

Mesocricetus auratus

186.80

Phodopus sungorus

135'00

Neotominae Neotoma floridana Ototylomys phyllotis

138.10 137'00

Peromyscus (Osgoodomys) banderanus Peromyscus (Peromyscus)boylei Peromyscus (Haplomylomys) calijornicus Peromyscus (Peromyscus) crinitus Peromyscus (Peromyscus)dtficilis Peromyscus (Haplomylomys) eremicus

79.60 77.60 75'25 78.80 78.80 76.00

Peromyscus (Zsthmomys) jlavidus Peromyscus (Podomys)$oridanus Peromyscus (Peromyscus)furvus Peromyscus (Peromyscus)gossypinus Peromyscus (Peromyscus)grandis Peromyscus (Peromyscus)guatemalensis Peromyscus (Habromys) lepturus Peromyscus (Peromyscus)leucopus Peromyscus (Habromys) lophurus Peromyscus (Peromyscus) maniculatus Peromyscus (Peromyscus)megalops Peromyscus (Peromyscus) melanotis Peromyscus (Peromyscus) mexicanus Peromyscus (Peromyscus) nudipes Peromyscus (Ochrotomys) nuttalli Peromyscus (Zsthmomys) pirrensis Peromyscus (Peromyscus) polionotus Peromyscus (Megadontomys) thomasi Peromyscus (Peromyscus) truei Peromyscus (Peromyscus)zarhynchus Tylomys gymnurus

84.00

555

Hirth (1960) Helm & Bowers (1973); Cummins & Woodall (1985) Linzey & Layne ( I 974) Linzey & Layne (1974) Hirth (1960); Linzey & Layne (1974) Linzey & Layne, (1974) Linzey & Latne (1974) Linzey & Layne (1974); Elder & Hsu (1981)

Tylomys panamensis

Sigmodontinae Akodon azarae Akodon dolores Akodon molinae Akodon nucus

77'45 77'20 86,I 0 79.80

Linzey & Layne (1974) Hirth ( I 960) ; Linzey & Layne (1974)

1

Linzey & Layne

(I

974)

82.20

77.10 77'30 76.70 75'00

1

93'90

73'30 72'20 79'20 67.70 8490 76.10

Hirth (1960); Linzey & Layne (1974)

Linzey & Layne (1974)

Hirth (1960) Linzey & Layne (1974) Hirth (1960); Linzey & Layne (1974)

ii:;~ 1

Linzey & Layne (1974)

75.40) 87.00 87.00

103.30 81.60 86.60 75.80

Akodon varius Bolomys oscurus Bolomys temchuki

105'30 7458 79.60

Calomys callidus

7480

Calomys hummelincki

86.50

i

Helm & Bowers (1973); Cummins & Woodall (198j ) Helm & Bowers (1973); Cummins & Woodall (1985) E. R. S. Roldan & A. D. Vitullo, unpublished Semino et al. (1979) E. R. S. Roldan & A. D. Vitullo, unpublished Semino et al. (1979) E. R. S. Roldan & A. D. Vitullo, unpublished Roldan et al. (1985); E. R . S. Roldan & A. D. Vitullo, unpublished Perez-Zapata et al. (1987); A. D. Vitullo, unpublished

5 56

E. R. S. ROLDAN,M. GOMENDIO AND A . D. VITULLO

C'alomys laucha

Acr

55.80

Calomys miisculinus

B4

72.00

Calomys cenustus Eligmodontia typus Eunromys sp. Graomys griseoj?a.i~us Oryzomys delticola Ovyzomys destructor Oryzomys flaz'escens Oryzomys longicattdatus Ovyzoni>,spalustris O.~y)'rnyctertis rufrrs Osymycterus sp. Reithrodon auritiis Srapteromys tumidus Sigmodon hispidits

B4 C4 B4 B4 B4 B4 B4 B4 B4 B4 B4 B4 B4 B4

Roldan et al. (1985); E. R. S . Roldan & A. D. Vitullo, unpublished Roldan et al. (1985); E. R. S. Roldan & .4. D. Vitullo, unpublished

81.20

107.50 87.20 78.50 70.60 77'10 74.80 76.40 79'40 80.90 82.00

85.60 I 08.70

87.00

E. R. S. Roldan & A . D. \~itullo, unpublished

1 i

M. B Espinosa & A D Vitullo, unpublished Hirth (1960)

E. R. S. Roldan & A . D. Vitullo, unpublished Austin & Bishop (19j8); Hirth (1960)

G~O51YID\F.

Geomys pinrtus

110'50

Hirth (1960)

Dz C2 Dz Dz D2

I2400

B2

I 0 2 ' ~ O

DZ

I 15'00

CZ Cz D2 Dz

I 06.00

I 29.00

Breed Breed Breed Breed Breed Breed Breed Breed Breed Breed Breed Breed Breed Breed

I 06.00 17.00'1

Breed & Sarafis (1979); Breed (1983)

~

ML-RILIAE Hydromyinae Coniluriis penicillatus Hydromys chrysogaster Leggadina forrrsti Leporillus conditor .lfelomys littorulis Sotom>*salexis Sotomys cervinus Sotom>,s.fuseus Sotomys nritchelli Pseiidoniys apodemoides Pseirdomjv australis Pseudomys delicatiilus Pseiidom>,sjumeus Pseudomys gracilicaudattrs Pseudomys hermannsburgensis Pseudomys higginsi Psrudomys nanus Pseudomys novaehollandine Pseudnmys shortridgei 1-romys caudimaculatus Z>,zoni>.sargurzis

Amu

D2 Dz Dz L) 2 Dz I32

Amu

Dz Dz

I I j'00 I 28.00

I 10'00 I 10'00

98.00 120'00 I 22'50

88.00 128.00

127'00j 106.00 96.00 106.00 137'00

Breed Breed Breed Breed

& Sarafis (1979)

& Sarafis (1979); Breed (1984) (1980) & Sarafis (1979) & Sarafis (1979) & Sarafis (1979) (1980, 1984) (1980, 1984) & Sarafis (1979); Breed (1980) & Sarafis ( I 9 79) ; Breed ( I 983) & Sarafis (1979) (1980, 1983) (1980) (1980, 1983)

(1980, 1983)

(1980, 1983) & Sarafis (1979); Breed (1g84)

& Sarafis (1979)

1111r i m e ;lethoni>~schrysophilus type A

BI

130

-4etliomj s 1 hv-vwphrlus type B

Amu

67.50

.-lethonz>,s rzamayiten.sis

BI

89.00

.4podemu.s

fla~icollis sylt,at1cus Rnndicotu brnEalensis Req-?.lm>,s bozcersii Chiropodomys gliroides Hapalomj.s longicuudatris

BI

.-lpodeenius

BI CI

125.40 I 33.80

Gordon & If-atson (1986), Breed et a1 (1988) Gordon & \Vatson ( I 986), Breed et al (1988)

Gordon & IT-atson (1986), J XI Cummins, pers comm Friend (1936) Friend (1936)

149'50

C1

I 87.00

€31

I 12'00

BI

121'00

Breed & Yong (1986)

Sperm evolution in mammals Lenothrix canus Leopoldamys edwardsi Leopoldamys sabanus Mastomys coucha

CI CI CI CI

149'00

Mastomys natalensis

CI

148.00

Maxomys inas Maxomys surifer Maxomys whiteheadi Micromys minutus M u s musculus Niniventer cremoriventer Niniventer rapit Niviventer bukit Pithecheir parvus Rattus argentiventer Rattus colletti Rattus exulans Rattus fuscipes Rattus leucopus Rattus lutreolus Rattus norvegicus (Brown) Rattus norvegicus (White) Rattus rattus

BI BI BI Amu

152'50\

Rattus sordidus Rattus tiomanicus Sundamys muelleri

CI CI CI

154'50 I 70.00 I 62.00

-

76.10

BI BI

CI CI Amu CI CI CI CI CI CI CI CI CI

184'00

j

182.00

Breed & Yong (1986) Cummins & Woodall (1985); Gordon & Watson ( I 986) Gordon &Watson (1986); J. M. Cummins, pers. comm.

157'00

I

15'50

J

137.00 63.70 123.60 I I 9.00 I 42.00

Breed & Yong (1986) Friend (1936) Hirth (1960); Friend (1936)

151'50

Breed & Yong (1986)

91.50 183.00 I 5 8.00 I 76.00

Breed & Sarafis (1979) Breed & Yong (1986)

162'oo 147'00 I 63.00

557

\

j

190.10 I 88.70 165.00

Breed & Sarafis (1979) Friend (1936) Friend (1936) Friend (1936); Hirth (1960); Breed & Yong ( I 986) Breed & Sarafis (1979) Breed & Yong (1986) Breed & Yong (1986)

ZAPODONTIDAE Zapus hudsonius

Hirth, 1960

SCIUROMORPHA

SCIURIDAE Sciurus niger Tamiasciurus hudsonicus

-

IZZ'ZO

-

131.00

Hirth (1960) Hirth (1960)

* Head shapes: Aca, Type A in Caviomorpha; Acr, Type A in Cricetidae; Amu, Type A in Muridae. Type A are round or oval heads lacking any appendices or protrusions either at the basal (site of tail insertion) or apical (opposite to site of tail insertion) edges. In these cells the tail usually inserts centrally in the base of the head. Type B are either oval, pyriform or polygonal heads whose most conspicuous trait is the presence of a 'modified' apical or basal edge. The departures from the pattern seen in Type A consist in the appearance of one hook in Muridae (BI and Bz) and Cricetidae (B3 through B6), a large acrosome in Caviidae (B7) and one or two caudal extensions in Ctenomyidae (B8); in these cells the tail inserts either centrally or eccentrically. Type C includes heads which are roughly polygonal in shape but with a higher degree of elongation, further displacement of tail insertion and a modification in the base of the head; this type represents heads with one hook, except in the Conilurini (Cz) where two hooks are seen. Type D is a vastly modified polygonal and elongated head with three hooks in the apical edge. Key to taxa: ( I ) Murinae, (2) Hydromyinae, (3) Neotominae, (4) Sigmodontinae, (5) Cricetinae, (6) Arvicolinae, (7) Caviidae, (8) Ctenomyidae. For further details see Fig. 7 and the text. a new model which will describe the different evolutionary pathways that rodent spermatozoa have undergone. General evolutionary trends will be discussed in relation to the underlying selective forces. In particular, we will argue that two main selective pressures, namely selection in the female tract and sperm competition, may have played an important role in the evolution of sperm morphology and dimensions. We believe that at this stage the integration of information originated in fields as diverse as

558

E. R. S. ROLDAN, M. GOMENDIO AND A. D. VITLTLLO Sperm head

(a)

Artiodactyla

-

Carnivora

-

+a+ r-cI

No. of species

0

21

0

15

Chiroptera

-

Edentata

-

lnsectivora

-

Lagornorpha

-

0

1

Perissodactyla

-

W

0

2

Pinnipedia

-

*

0

3

-

m

Primates

OIM?

Proboscidea

-

0

Rodentia

-

W I

0

40

Cetacea

-

c)l

0

4

ct---c

0

28

A

= I " . 1 . .

I

Sciuridae

-/

Cricetidae

80

I . . - I

- - ,I

Muridae

29 2 151

8 .

120 160 200 240 280

-

I 0

OIM

I

W

Geomyidae

2 8

OIM

I

I

0 0

M OIM

I

I

2 65 1

56

Capromyidae

4 -

Caviidae

-

Chinchillidae

-

Ctenornyidae

-

Dasyproctidae

-

1

Echimyidae

-

1

Zapodontidae

W

W

W

+a+

1 1

2 2

17

2 0

40

80

120

160 200

240 280

Sperm length (prn)

Fig. I . Sperm morphology and dimensions in Eutherian mammals. ( a ) Morphology and dimensions of spermatozoa from different Eutherian orders; ( b ) Sperm morphology and dimensions in rodent families. and ranges. Sperm head shapes: 0, oval or round; hl, modified (either in the Values given are means apical or the basal region of the head). Sperm lengths from Cummins & Woodall ( 1 g 8 j ) , an updated list of published and unpublished information provided by D r J . M. Cummins, and personal unpublished measurements of South American cricetids.

(m)

evolutionary biology, reproductive biology and behavioural ecology will highlight new lines of research. New hypotheses will be developed in an attempt to stimulate future investigations. Information on species geographic distribution, karyotypes, and phvlogenetic

Sperm evolution in mammals

559

relationships constructed using chromosomal, genic and classic morphological data sets have been obtained from the literature and references are given in the relevant sections. The information on sperm dimensions of Eutherian mammals was drawn from the catalogue compiled by Cummins & Woodall (1985), and from an up-dated list of published and unpublished information kindly supplied by Dr J. M. Cummins. Additional measurements of spermatozoa from South American caviomorph and cricetid rodents were obtained as previously reported (Vitullo et al., 1988). Information on head morphology of Eutherian spermatozoa has been obtained from published descriptions and from our unpublished observations using methods reported elsewhere (Roldan et al., 1985). Table I presents a complete list of measurements and head shapes of the rodent spermatozoa used for analyses. 111. MORPHOLOGY AND DIMENSIONS OF SPERMATOZOA AMONG EUTHERIAN

MAMMALS: AN OVERVIEW

The analysis of published information on Eutherian sperm morphology reveals that most species have spermatozoa with round or oval heads, the rodents being a conspicuous exception to this trend (Fig. I a ; Fig. 2). Spermatozoa with round, oval or paddle-like heads have a widespread distribution among Eutherian mammals. In Artiodactyla, species of the families Bovidae (Retzius, 1909; Austin & Walton, 1960; Morgenthal, 1967; Howard et al., 1983), Camelidae (Merlian et al., 1979), Cervidae (Wislocki, 1949; Bierschwal et al., 1970; Dott & Utsi, 1971; Andersen, 1973; Haigh et al., 1975; Gosch et al., 1989), Giraffidae (Velhankar et al., 1973), Hippopotamidae (Morgenthal, I 967), and Suidae (Morgenthal, 1967) have been examined and all have spermatozoa with flat paddle-shaped heads. Among Carnivora, spermatozoa with round, oval or paddle-shaped heads have been found in Canidae (Steklenev, 1975), Felidae (Steklenev, 1975; O’Brien et al., 1986; Wildt et al., 1986, 1987; Howard & Wildt, 1990; Miller et al., 1990), Mustelidae (Steklenev, 1975; van der Horst et al., 1991), Procyonidae and Ursidae (Platz et al., 1990); in the suborder Pinnipedia (treated as a separate order by Cummins & Woodall, 1985, and used as such in Fig. I a ) , sperm heads are paddle-shaped (Retzius, 1909). Spermatozoa from three species of Cetacea have been described and all have oval heads: Globicephala melas (Retzius, 1909), Physeter catodon (Matano et al., 1976), and Tursiops truncatus (Fleming et al., 1981). Four families of Chiroptera have spermatozoa with roughly oval or paddleshaped sperm heads : Molossidae (Breed & Leigh, I 985), Phyllostomidae (Florman, 1968); Pteropodidae (Rouse & Robson, 1986; Cummins et al., 1988), and Vespertilionidae (Hirth, 1960; Florman, 1968; Breed & Inns, 1985). Molossid bats are somewhat peculiar due to the presence of ‘blisters’ on the cell surface over the acrosomal region (Breed & Leigh, 1985). Only two species of Edentata have been studied: Dasypus novemcinctus (Nagy & Edmonds, I 973) and Cabassous unicinctus (Heath et al., 1987); both have paddle-like sperm heads although those in the latter species are very wide and thin. Among Insectivora, species belonging to three families have spermatozoa with oval/paddle-shaped heads : Talpa europaea (Retzius, I 909), Erinaceus europeus (Bishop & Walton, 1960), and Sorex araneus (Ploen et al., 1979). A fourth species of Insectivora, Suncus murinus (Soricidae), has spermatozoa which exhibit a huge acrosome (Green & Dryden, 1976; Cooper & Bedford, 1976). Species of Hyracoidea (Bedford & Millar, 1978), Lagomorpha (Bishop & Walton, 1960),

5 60

E. R. S. ROLDAN, M. GOMENDIO AND A. D. V I n - L L o MESOZOIC

140 130 120 110100 90 80 70 I I l l 1 1 1 1

0 50

CEN 020 I C 40 30 20

10

0

Monotremata

\

,

I -

\

Lagomorpha Macroscel idea

I /

8 1 9

Scadentia

q25 Dermoptera

2i

,

8p 6 Q 1 i2

Chiroptera

27 28

lnsectivora Carnivora

29

30 31

R~Q q35~

89 9

36 37 38 39 Q40

f3,

Artiodactyla

Tubulidentata

?

Perissodactyla

----_

Hyracoidea Proboscidea

\

Sirenia

?

Fig. 2 . X phylogenetic tree shoiving relationships among major extant mammalian clades and examples of sperm head morphologies seen in the various clades. T h e solid horizontal bars indicate the age range of the clade on the basis of dated first appearance in the fossil record. Solid lines indicate the branching sequence and dashed lines indicate relatively more ambiguous relationships. T h e phylogenetic tree is a modification of that presented by Novacek ( 1 9 9 ~ )sperm ; head morphologies, not drawn to scale, were obtained from the literature: ( I ) Tachyglossus aculeatus (Austin, 196s); ( 2 ) Psezrdocheivzts cupyeus

Sperm evolution in mammals

561

Macroscelidea (Woodall, I 99 I ) , Perissodactyla (Dott, I 975), Proboscidea (Jainudeen et al., 1971; Jones et al., 1974), and Scadentia (Tupaia glis: Bedford, 1974) have spermatozoa with oval or paddle-like heads. Spermatozoa in species of the order Pholidota (Manislongicaudata : Ballowitz, I 907 ; Manis pentadactyla: Leung & Cummins, 1988) are unique; sperm heads in these species are not flattened but elongated and pointed, and with a round cross-section of about I pm in diameter. These sperm heads appear to be unlike that of any other Eutherian mammal described so far and, in fact, they resemble the sauropsid spermatozoa found in Monotremes, thus raising the question that perhaps the order Pholidota should not be joined with Edentata (cf. Fig. 2 ; Novacek, 1992). It is noteworthy, however, that some of the pleiomorphic spermatozoa from M . longicaudata illustrated by Ballowitz (1907) resemble the sperm heads found in most Eutherians. Finally, among Primates, spermatozoa from Ceboidea, Cercopithecoidea and Hominoidea have flat oval or paddle-shaped heads (Bedford, 1974; Martin et al., 1975; Gould & Martin, 1978; Gould, 1980). Prosimian spermatozoa have flat paddle-like heads too but, in addition, they have some features not shared with those of other primates, such as an extended apical segment of the acrosome (Bedford, 1974). Furthermore, whereas the elongated apical segment of the acrosome remains erect in Lemuridae (Bedford, I 974; Gould, I 980), in Lorisidae (e.g. Galago crassicaudatus, Nycticebus coucang) it deviates to form an asymmetrical cupped flange or cupola, which gives the sperm head a ‘hooked ’ shape when seen in profile (Bedford, I 974 ; Gould & Martin, 1978; Phillips & Bedford, 1987). This feature makes lorisoid sperm heads somewhat distinct and their spermatozoa might therefore be considered a ‘ modified ’ (Pteuridae) (Hughes, I 965) ; (3) Parameles nasuta (Paramelidae) (Hughes, 1965); (4) Macropus canguru (Macropodidae) (Hughes, I 965); ( 5 ) Phasolarctos cinereus (Phasolarctidae) (Hughes, 1965, 1977); (6) Vombatus ursinus (Vombatidae) (Hughes, I 965) ; (7) Sarcophilus harrisii (Dasyuridae) (Hughes, I 965); (8) Dasypus novemcinctus (Nagy & Edmonds, 1973); (9) Cabassous unicinctus (Heath et al., 1987); (10) Manis longicaudata (Ballowitz, 1907); ( I I ) Calomys laucha (Cricetidae: Sigmodontinae) (Roldan et al., 1985); (12)Musmusculus (Muridae: Murainae) (Friend, 1936); (13) Rattus novegicus (Muridae: Murinae, (Friend, 1936); (14) Pseudomys australis (Muridae: Hydromyinae) (Breed & Sarafis, 1979); ( I S )Microtus orchrogaster (Cricetidae : Arvicolinae) (Austin, I 957) ; (16) Cricetulus griseus (Cricetidae: Cricetinae) (Austin & Bishop, 1958; Yanagimachi et al. 1983); (17) Ctenomys maulinus (Ctenomyidae) (Feito & Gallardo, 1976); (18) Oryctolagus cuniculus (Bishop & Walton, 1960); (19) Elephantulus edwardii (Woodall, 1991); ( 2 0 ) Lemur fulvus (Prosimii) (Bedford, 1974); (21) Galago crassicaudatus (Prosimii), ( a ) planar view; (b)lateral view (Bishop & Austin, 1960; Bedford, 1974; Gould & Martin, 1978); ( 2 2 ) Saimiri sciureus (Ceboidea) (Bedford, 1974; Gould, 1980); (23) Macacca mztlatta (Cercopithecoidea) (Bedford, 1974; Gould, 1980); (24) Homo sapiens (Hominoidea) (Bedford, 1974); ( 2 5 ) Tupaiaglis (Bedford, 1974); (26) Mormopterus planiceps (Molossidae) (Breed & Leigh, I 985) ; (27) Glossophaga soricina (Phyllostomidae) (Florman, 1968); (28) Sturnira lilium (Phyllostomidae) (Florman, I 968) ; (29) Pteropus conspiculatus (Pteropodidae) (Rouse & Robson, 1986); (30) Pipistrellus subflawus (Verpertilionidae) (Hirth, 1960); (3 I ) Myotis sodali (Vespertilionidae) (Hirth, 1960); (32) Plecotus townsendii (Vespertilionidae) (Florman, 1968); (33) Talpa europaea (Talpidae) (Retzius, 1909); (34) Suncus murinus (Soricidae) (Green & Dryden, 1976; Cooper & Bedford, 1976); (35) Sorex araneus (Soricidae) (Ploen et al., 1979); (36) Panthera leo (Felidae) (Wildt et al., 1987); (37) Acinomyxjubatus (Felidae) (O’Brien et al., 1986); (38) Neofelis nebulosa (Felidae) (Wildt et al., 1986); (39) Canzs familiaris (Canidae) (Steklenev, 1975); (40) Mustelaputorius (Mustelidae) (van der Host et al., 1991); (41) Bos taurus (Bovidae) (Bishop & Walton, I 960); (42) Globicephala melas (Delphinidae) (Retzius, I 909); (43) Tursiops truncatus (Delphinidae) (Fleming et al., 1981); (44) Physeter catodon (Physeteridae) (Matano et al., 1976); (45) Equus caballus (Dott, 1975); (46) Procavia capensis (Bedford & Millar, 1978); (47) Elephas maximus (Jainudeen et al., 1971); (48) Loxodonta africana (Jones et al., 1974).

E. R. S. ROLDAN, M. GOMENDIO AND A. D. VITULLO type. At first glance, this cup-shaped reflection of the apical portion of the acrosome appears to resemble some modifications (‘ hooks ’) seen in spermatozoa from various rodent species (see below). However, the two types of sperm heads are totally different : when seen on a planar view, the apical segment of lorisoid sperm heads reflects over the dorsal surface whereas modifications in rodent sperm heads occur towards a lateral edge of the sperm head. T h e vast majority of rodent spermatozoa tend to have heads with a complex morphology (Fig. 2). T h e modifications that appear in the head of rodent spermatozoa may affect either the apical or the basal region. T h e modifications in the apical region include the presence of one or several hooks in Myomorpha and the enlargement of the acrosome among the Caviidae (Caviomorpha). T h e basal region may show nuclear caudal extensions in Ctenomyidae (Caviomorpha) or changes in the site of tail insertion in both Myomorpha and Caviomorpha. Total lengths of spermatozoa from different Eutherian orders are illustrated in Fig. I a . Spermatozoa from Eutherian mammals show an average total length of 69.23 2 4.1 3 p m (mean f S.E.M. ; n = 266 species) ; more importantly, Eutherian spermatozoa show a wide range in total sperm lengths: 33-258 pm. Rodents have relatively long spermatozoa when compared to other Eutherian groups. Thus, when rodents are excluded from this analysis the average total length of Eutherian spermatozoa is reduced (66.36k3.41 pm, n = 107) and, more revealing, the range in sperm lengths becomes narrower : 3 3-1 2 I pm. Rodents show a mean sperm length of 10I .08 & 3’I 7 p m (n = 151) and the widest range of sperm lengths seen in any Eutherian order (35-258 pm). Wide sperm length ranges are also seen in Chiroptera (45-109 pm), Insectivora (64-121 pm) and Primates (50-105 pm). Table I lists all the information available on sperm morphology and dimensions of rodent species that we used for analyses. Three species for which total sperm length is known ( Tatera leucogaster, Saccostornus carnpestris and Rhabdornys purnilio ; see Cummins & Woodall, 1985) were not considered because either the morphology of their heads or their taxonomic status were unclear. Fig. I b summarizes the information on total sperm length means and ranges of different rodent families. Unfortunately, there are only two species of sciuromorphs (Sciuridae) for which information is available (Fig. I b ) , thus precluding further analysis within this taxon. Average total sperm length in myomorphs (109.07& 3.33 pm; range = 56-258 ; n = I 2 3 ) is larger than that in caviomorphs (61.34f4.01; range = 35-107; n = 26). Averages and ranges differ between myomorph families (Fig. I 6 ) . Thus, spermatozoa from Cricetidae have a mean total length of 89.17 & 3.63 p m (n = 65) and a range of 56-258 pm, whereas spermatozoa from Muridae show a higher mean length (132.73 k 4 . 1 6 p m ; n = 56), but a considerably smaller range (64-1 97 pm). Within Caviomorpha, the families Caviidae and Ctenomyidae show a wide range of sperm lengths and have spermatozoa that on average tend to be longer than those of other families. It thus seems that the most common features of sperm cells among Eutherian mammals are an overall length of approximately 6 j p m and a flat oval or paddle-shaped head. In most Eutherian taxa the uniformity in sperm morphology and dimensions among different species, or the scarcity of information, preclude any analyses of evolutionary trends (Fig. 2 presents a general outline of mammalian evolution and the accompanying variations in sperm head morphology to illustrate the high degree of

Sperm evolution in mammals

563

uniformity in sperm head shapes seen across most Eutherian clades). We have therefore turned to rodents where the diversity of sperm morphs and dimensions makes such analysis possible. IV. EVOLUTIONARY T R E N D S I N SPERM MORPHOLOGY A N D DIMENSIONS: FIVE CASE S T U D I E S AMONG RODENTS

T o gain insight into the question of which is the ancestral type of spermatozoa in rodents, and therefore understand the direction of evolution in sperm morphology and dimensions, we have compared evolutionary relationships based on biogeographical, morphological, chromosomal and genic analyses with the information available on sperm head morphology and overall dimensions. Sufficient information for analyses was found for the following taxa : Ctenomys (Caviomorpha : Ctenomyidae), Calomys (Cricetidae : Sigmodontinae) and the Conilurini (Muridae : Hydromyinae). Additional, although less exhaustive examination was possible with Neotomine-Peromyscines (Cricetidae : Neotominae) and arvicolids (Cricetidae : Arvicolinae). We reasoned that sperm traits present in species considered primitive by other criteria could be considered ancestral (plesiomorphic) characters, and that direction of evolution may be inferred taking into account the patterns shown in more recent, derived species. ( I ) The genus Ctenomys (Caviomorpha : Ctenomyidae)

The caviomorph rodents encompass about I 73 extant species which have evolved in South America since the Middle or Upper Eocene following the arrival of an African ancestor (Reig, 1986, 1989; Reig et al., 1990). The genus Ctenomys, which consists of 56 recognized extant species, suffered an explosive evolution with high diversification and speciation during a short period of time (about 1-8 million years) during the Pleistocene (Reig, 1989; Reig et al., 1990). Early diversification in this genus occurred in the lowland Pampean region of eastern South America and the species then colonized the highlands of Argentina, Chile, Bolivia and Peru (Reig et al., 1990). Ctenomys species share a combination of attributes such as a subterranean life, patchy distribution, limited vagility, and small effective population numbers, which are to be taken into account to understand their pattern of diversification (Reig et al., 1990). Two different sperm types have been recognized in Ctenomys species (Feito & Gallardo, 1982). They have been described as symmetric or asymmetric according to the absence or presence of a nuclear caudal extension (NCE) which runs parallel to the tail. In symmetric spermatozoa the tail inserts centrally, whereas in asymmetric spermatozoa the tail is inserted eccentrically. The symmetric spermatozoon has an oval or paddle-shaped head; in the asymmetric spermatozoon, although the NCE gives the cell a distinctive appearance, the head is nevertheless paddle-shaped. Information on head morphology is now available for 32 species of Ctenomys (see Fig. 3): 22 species have symmetric spermatozoa whereas the remaining I o species have asymmetric sperm cells. Unfortunately, total sperm lengths are known for only 17 Ctenomys species (Table I ) . Symmetric spermatozoa have an average total length of 5 2 . 0 0 ~ 0 * 3pm 2 (range 49-28-52.65 ; n = IO), whereas asymmetric spermatozoa (85.56 +0*40p m ; range = 83-68-86.53 p m ; n = 7) are considerably longer (Mann-Whitney U ; P = 0-0006). Symmetric spermatozoa from Ctenomys are very similar in morphology and dimensions to those seen in the Octodontidae (Berrios et al., 1978; Herrera et al., 1978; Ortells,

5 64

E. R. S. ROLDAN,M. GOMENDIO ,4ND A. D. VI-rvLLo

BRAZIL

South

Pacific Ocean

South

Atlantic

Fig. 3. Geographical distribution of Ctenomys species with ( W ) symmetric and (A)asymmetric sperm types. Average total sperm length is indicated for each type. Species with symmetric spermatozoa: (I)C'. opimirs (Chile)', ( 2 ) C. robustus', (3) C.f n l z v ~ -(4) ~ , C. opimus (Bolivia)?; ( 5 ) C lezvisi*, ( 6 ) ( 7 . f v n t e r Y , (7) C. boliviensis', (8)C . steinbachi', (9)C.goodfellozd, (10)C. conoverid, (11)C.knightii', (12)C . l a t r d , (13)C . tuconad, (14)C . occultufl, (Ij ) C . tucumanus/, (16) C . a v g e n t i m d , (17)C . roigi', (18)c.dwbignyP, (19) C . perrensis", (20) C . torquatus', ( 2 1 ) C. minutus", ( 2 2 ) C. pearsoni', ( 2 3 ) C. talarztrn".'. Species with asymmetric spermatozoa: (24) Ctenomys sp.', ( 2 5 ) c'. yolandaed, (26) C . riongegrensise.d.f,(27) C . rneBdociniisd, (28)C.porteozisid, (29) C . azaraeb, (30) C.australisd, (31)C. maulinusb, ( 3 2 ) C. fodax', (33)C.r n a g e / ( a n i c u ~ " . ~ . Although spermatozoa from C . yolandne have two nuclear caudal extensions, and are therefore considered complex-asymmetric, the distinction betmeen simple and complex asymmetric forms is not relei-ant here. Spermatozoa from C . latro and C. tucumanus, although not examined by Gallardo (1976), \\ere reported by this author to b e asymmetric. Recent studies (Ortells, 1990) h a w not confirmed that report and we therefore have illustrated these species as having symmetric spermatozoa. Information on total sperm length and morphology were obtained from a Jones ( 1 9 7 j ) ; Feito & Gallardo (1982);'Altuna r t 01. (1985);'Vitullo e t al. (1988), 'Vitullo & Cook (rqgr),and 'Ortells (1990).

Sperm evolution in mammals

565

1990),a family closely related to the Ctenomyidae (Octodontidae: 47'5of 2.3 pm; n = Moreover, the symmetric Ctenomys sperm resemble in shape and dimensions the round/oval-headed spermatozoa found in most caviomorphs (42.15 & 2.04 p m ; range = 34.64-49.82; n = 7), and in most other Eutherians (see Figs I and 2). It is noteworthy that sperm morphology and dimensions are highly conserved within each of the two groups of Ctenomys species, i.e. there is little variability in sperm traits between species carrying a given type of spermatozoa (see above ranges of total sperm lengths for each sperm type; cf. Vitullo et al., 1988;Vitullo & Cook, 1991).In addition, the two groups show different geographical distribution (Fig. 3) : species with symmetric spermatozoa are present in the north-northwest area of distribution, whereas those species bearing asymmetric spermatozoa are found in the SouthSouthwest areas (Feito & Gallardo, 1982;Vitullo et al., 1988;Vitullo & Cook, 1991). Based on the different geographical distribution of these two groups, the little interspecific sperm variability within each group, and the lack of association between sperm types and chromosome numbers, we have previously suggested that the first steps in the diversification of Ctenomys species were probably accompanied by the appearance of the two distinctive sperm types (Vitullo et al., 1988).Since the short, symmetric spermatozoa are very similar to the spermatozoa found in a closely related family (Octodontidae) and in most caviomorphs, we have suggested that symmetric spermatozoa represent the ancestral condition (Vitullo et al., 1988). We have also speculated that further speciation has occurred through geographical dispersal and/or chromosomal speciation within each of the two groups of species while sperm traits remained constant within each group. Recent studies have also gathered evidence in favour of an early separation of two main Ctenomys lineages (Rossi et al., 1990)and an association between each lineage and a different sperm type (cf. Vitullo & Cook, 1991). Species with asymmetric spermatozoa were found to have a highly repetitive DNA sequence of about 370 kbp which in hybridization studies showed only a weak signal with DNA from species having symmetric spermatozoa, or from species of Octodontidae (Rossi et al., 1990). It thus seems that expansion of this sequence occurred in species with asymmetric spermatozoa after the divergence from species bearing symmetric spermatozoa. In addition, these findings support the idea that symmetric spermatozoa represent the ancestral condition in this genus. Studies of chromosome affinities have revealed that Ctenomys species group in five well-defined clusters which probably represent evolutionary units ; with minor exceptions, every cluster is characterized by a sperm morphotype (Ortells, I 990).These results support our hypothesis that explosive chromosomal evolution took place after two groups of species were separated as a consequence of the reproductive isolation promoted by the early appearance of two sperm variants (Vitullo et al., 1988). In conclusion, the symmetric 52pm long spermatozoa is likely to represent the ancestral condition in Ctenomys, whereas the asymmetric and longer spermatozoa could be considered as the derived (apomorphic) condition in these species. 2).

(2)

T h e genus Calomys (Myomorpha : Cricetidae)

South American cricetid rodents are grouped in the subfamily Sigmodontinae. Different views have been presented about the origin and antiquity of the Sigmodontinae in South America, but strong evidence exists to suggest that they

566

E. R. S. ROLDAN, M. GOMENDIO AND A. D. VITULLO

diversified locally from an invading North American ancestor that entered South America by Early Miocene times prior to the establishment of the Panamanian bridge (Reig, I 986). T h e 5 I genera and 249 species of South American Sigmodontinae can be grouped in seven different tribes. T h e Phyllotini represent 18 ' l o of the living species. T h e genus Calomys is the most primitive of the living phyllotine genera, and it is very close to the hypothetical ancestor of the tribe (Reig, 1986). Originating in the Puna region, these rodents dispersed to the north and to the eastern lowlands of South America. Geographical dispersal has been accompanied by chromosomal speciation (Fig. 4) which is thought to have occurred through a series of centric fusions and minor additional chromosome changes (e.g. inversions) (Vitullo et al., I 990). Biochemical data suggest that early divergence of species is ancient (at least about 6 million years ago; Gardenal et al., 1990). We have examined the spermatozoa from the following species (trapping localities in parenthesis): C. callidus (El Palmar, Entre Rios), C. laucha (Diego Gaynor and Pila, Buenos Aires), C. musculinus (Laguna Larga, Cordoba) and C . venustus (Donovan, San Luis and Cosquin, Cordoba), all from Argentina, and C. hummelincki (Los Cocos, Anzoategui) from Venezuela. Preliminary information on sperm morphology of some species has been already published (Roldan et al., 1985 ; Perez-Zapata et al., 1987). When spermatozoa of Calomys species are examined in the light of the pattern of chromosomal speciation (Fig. 4), it is evident that the species more closely related to the ancestral condition (i.e. C. laucha) has spermatozoa with oval, hookless heads and short (56pm) total length. Soon in chromosomal evolution, as seen in C. hummelincki, a species with a low degree of karyological transformation, spermatozoa acquire hooked heads and become longer (86pm). This condition is maintained in further chromosomally transformed species such as C. musculinus. In a group of closely inter-related species (C. venustus, C . callidus) a different type of head morphology and long sperm cells (about 80 pm) are evident. Thus, the joint analysis of sperm morphology and chromosomal evolution in Calomys clearly shows that spermatozoa with hookless oval heads and short tails represent the primitive condition from which enlargement and morphological transformation of the apical region soon emerged and became widespread in most living species. ( 3 ) The Neotomini-Peromyscini (Myomorpha : Cricetidae)

T h e Neotomine-Peromyscine rodents (subfamily Neotominae) are an assemblage of North American cricetids comprising about I I I species arranged in 1 2 genera (Carleton, 1980); these figures are likely to be an underestimate because of the continuous revision of the group (see Honacki et al., 1982; Carleton, 1989). T h e Neotomini-Peromyscini are related to the South American Sigmodontinae and, if the two groups derive from a common ancestral stock, they must have separated by Oligocene or earliest Miocene (Hibbard, I 968 ; and see previous section). Two phyletic lines are recognized for Neotomini-Peromyscini : T h e Neotomines, which include the genera Neotoma, Xenomys, Tylomys, Ototylomys and Nelsonia (Hooper, I 968), represent a minor phyletic line which evolved from the one which gave rise to the Peromyscines. T h e Peromyscines include Peromyscus, Reithrodontomys, Neotomodon, Ochrotomys, Onychomys, Baiomys and Scotinomys (Hooper, I 968), although generic status has been

Sperm evolution in mammals

567

C. lepidus

C.callosus

12n = 36 (68)1

2n = 36 (48)

5 INV

C. musculinus

I I

72 pm

I I I I

I2n = 48 (66) C.callidus

7 5 pm

2 n = 38 (56)

2n = 54 (66)

C.venustus 1 INV

81 ,urn

I I I 56 pm

-B

C. hummelincki 2 INV

.IILL.AR,R. P . (1978). T h e character of sperm maturation in the epididymis of the ascrotal hyrax, BEDFORI), P ~ n c a r t ocapensis and armadillo, Dasypus novemcinctuz. Biology of Reproduction 19, 396-406. 8~1.1.. G (1978). T h e evolution of anisogamy. Journal of Theoretical Biology 73, 247-270. BFI.I.IS,;21. A , , RAKER,R. R . & GAGE,M. J . G . (1990).Variation in rat ejaculates consistent with the kamikazesperm hypothesis. Journal of i2/7ammalogy 71, 479--480. HEHRIOS,31., F L ~ C H OJ .NE., & BARROS,C. (1978). Ultrastructure of Octodon degus spermatozoon with special reference to the acrosome. American Journal of an atom^, 151,39-54. BIT.RS:(I+W.AL, C . J . , X l A T T N m , E. C . , A l A R T I S , C. E., MURPHY, D. KORSCHEN, L. J . (1970). Somecharacteristics of deer semen collected by electroejaculation. Journal of the American I’eterinary Medical Association 157, 627 ~ 4 2.3 BIRDSALL, D. A. & NASH, D. (1973). Occurrence of successful multiple insemination of females in natural populations of deer mice (Peromyscus maniculatus). Evolzction 27, 106-1 10. BIRKHEAD, ‘r.R. (1988). Behavioural aspects of sperm competition in birds. Advances in the Study of Behaoiour

c.

18. 35-72.

BIRKHEAD, T. R. & HUNTER,F.WI. (1990). Mechanisms of sperm competition. Trends in Ecology and Evolution 5 , &j2.

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