Download Sexual size dimorphism lacking in small mammals

NORTH-WESTERN JOURNAL OF ZOOLOGY 10 (1): 53-59
Article No.: 131707
©NwjZ, Oradea, Romania, 2014
http://biozoojournals.ro/nwjz/index.html Sexual size dimorphism lacking in small mammals
Di LU1,2,§, Cai Quan ZHOU1,2, § and Wen Bo LIAO1,2,*
1. Key Laboratory of Southwest China Wildlife Resources Conservation (Ministry of Education),
China West Normal University, Nanchong, 637009, P. R. China.
2. Institute of Rare Animals and Plants, College of Life Sciences, China West Normal University, Nanchong, 637009, P. R. China.
*Corresponding author, W.B. Liao, Tel. +86-15281746506, Fax: +86-08173421909,
E-mail: [email protected]
§ - D. Lu and C.Q. Zhou have equal contribution in the paper
Received: 26. January 2013 / Accepted: 23. June 2013 / Available online: 14. December 2013 / Printed: June 2014
Abstract. Body size is arguably the most important morphological trait of animals. Males and females’ body
size differences as sexual size dimorphism (SSD) affect behavioural and ecological processes. We study sexual
size dimorphism in small mammals, collecting 95 species (22 Chiroptera, 66 Rodentia, 1 Scandentia, and 6
Soricomorpha) from published literatures. The sexual difference in size between the sexes is not-significant
either in 33 little female-biased SSD or in 62 little male-biased SSD species. The non-significant difference in
body size of 62 little male-biased SSD species showed that sexual selection did not drive the evolution of male
body size, with weaker correlated selection on female body size. Data analysis revealed a non-significant
correlation between female body length and litter size in 33 species, suggesting that fecundity selection in
favour of larger females is unlikely to play a role for explaining SSD lacking in small mammals.
Key words: sexual size, dimorphism lack, sexual selection, mammalian olfaction, small mammals.
Introduction
Body size is arguably the most important morphological trait of animals (Ralls 1977, Fathinia et al.
2012). Body size differences between males and
females differ significantly in animal kingdom
(Andersson 1994, Székely 2004, Kuo et al. 2009).
This phenomenon known as sexual size dimorphism (SSD), has attracted considerable research
effort in recent years (Monnet & Cherry 2002). SSD
is a prevalent and widespread phenomenon in
vertebrates, including fishes (Parker 1992), amphibians (Shine 1979, Schäuble 2004, VargasSalinas 2006, Fathinia et al. 2012, Liao & Lu
2010a,b, 2011a,b, Liao & Chen 2012, Liao 2013,
Liao et al. 2013a,b), reptiles (Clark 1964, Shine
1978, 1994, Berry & Shine 1980, Cox et al. 2007),
birds (Selander 1966, Székely et al. 2000, 2007), and
mammals (Crook 1972, Ralls 1977, Weckerly 1998,
Schulte-Hostedde et al. 2000, 2001, Issac 2005).
There are several hypotheses to explain SSD,
such as sexual selection, fecundity selection and
ecological-niche divergence. As the most supported hypothesis, sexual selection predicts that
intense selection drives body size evolution of the
selected sex, usually males, however only weaker
correlated selection on body size of the other sex
(Dale et al. 2007). Larger males can be more successful at acquiring mating opportunities, usually
through male-male combat, which result in the
evolution of larger male body size (Andersson
1994, Vargas-Salinas 2006, Serrano-Meneses et al.
2007). Fecundity selection predicts that larger females produce more young than smaller females,
resulting in higher lifetime reproductive success
and the evolution of larger female (Andersson
1994). Finally, SSD resulting from ecological-niche
divergence occurs when each sex has adapted to
different ecological niches (Slatkin 1984, Shine
1989). The evidence of resource availability suggests that food scarcity differentially constrains
the growth of the sexes. Diverging growth patterns between the sexes appear to be the primary
physiological mechanism leading to SSD (Isaac
2005).
In mammals, SSD is usually attributed to contest among individuals in polygynous mating systems, in which larger males achieve greater reproductive success (Shine 1978, Andersson 1994).
Most mammalian species exhibit male-biased SSD,
particularly those with polygynous mating systems (Halliday 1978, Eisenberg 1981, Boonstra et
al. 1993), but some species of mammals exhibit
female-biased SSD (Ralls 1976, 1977). For small
mammals, evidence from some genera of rodents
indicates that there is non-significant difference in
body size between males and females based on the
fact that individuals choose their mates by olfaction rather than contests (Eisenberg & Kleiman
1972, Blaustein 1981, Fan 1987, Schulte-Hostedde
2007, Sun et al. 2008). The present paper will test
whether there is difference in body size of 95 spe-
D. Lu et al.
54
cies using published data and museum measurement of China West Normal University, and discuss the reason of SSD lack in small mammals.
Materials and Methods
The use of body weight to measure SSD is inappropriate,
for the mass will vary with the breeding season and seasonal changes. Therefore, the body length is an appropriate alternative. So we reviewed the published literatures
and reference books of 16 and 64 species respectively to
obtain data on the size of adult body and litter, and
measured 15 species of preserved specimens from the
Zoological Museum of China West Normal University.
The body length of each individual was measured by
electronical caliper to the nearest 0.1 mm and the average
body length was taken. The data from literature were reliable because the same measurements method was performed, and all individuals were deposited in a standard
museum. The data were collected from 4 orders, across 95
species, and 11 families (Table 1).
Dimorphism ratios were calculated by dividing the
mean of females measured parameters to males’, to describe the magnitude of any sex differences in body size.
All variables were log10-transformed prior to analysis to
meet the assumption that the data were normally distributed. Sex comparisons of body length were performed by
general linear models (GLMs) with body length as dependent variables, and sexes as a fixed factor. We also
performed a linear regression with log10 to body length
as dependent variable, and sex as fixed factors to test for
sex differences in mean body length among the sampled
species. Correlation analysis was used to explore the relationship between female body length and litter size. All
statistical tests were two-tailed and were performed using
SPSS v. 17.0 software.
Results
There are 33 little female-biased SSD (defined as
females being larger but not significant than
males) and 62 little male-biased SSD species
among 95 species, individual body length ranged
from 37.8 to 250.2 mm in females, 35.6 to 258.0 mm
in male, while litter size ranged from 2.31 to 9.94
(Table 1). The mean females body size (88.65 ±
5.45) was slightly larger than males (85.47 ± 5.24)
in little female-biased SSD species, (GLMs, F1,65 =
0.177, P = 0.676). The little male-biased SSD species, average males (130.43 ± 6.82) and females
(125.037 ± 6.55), displayed similar outcomes
(GLMs, F1,123 = 0.326, P= 0.569). There was significant relationship between males and females body
size (33 little female-biased SSD species, r = 0.9953,
Y = 0.9953X – 0.008 Fig. 1(a); 62 little male-biased
SSD species, r =1.014,), Y = 1.014X – 0.012; Fig.
1(b)). Linear regression was used to analyze the relationship between female body size and litter
size, which revealed a non-significant relationship
(r = ﹣ 0.218, P = 0.222, Y = ﹣ 0.1977X + 1.0957;
Fig.2) in 33 species.
Discussion
Male-biased size dimorphic populations, in which
males are larger than females, approximately
cover 45% species of mammals (Lindenfors et al.
2007). However, little sexual dimorphism has been
shown in many more species, where male parental
investment is very small, particularly in the orders
of Insectivora, Chiroptera, and Rodentia (Ralls
1977). Results from this study showed nonsignificant difference in body size between males
and females of 95 species, suggesting there is only
little SSD within these studied specimens.
Generally, sexual selection is believed to be
the foremost cause of sexual dimorphism (Shine
1978; Isaac 2005). Two sexual dimorphisms processes are commonly divided as intrasexual selection, in which members of one sex compete to
mate with members of the other, and intersexual
or epigamic selection, in which members of one
sex choose to mate with members of the other
(Ralls 1977, Isaac 2005). It displays a predominantly polygynous mating system in most mammals, with males competing for access to breeding
females (Krebs & Davies 1981, Isaac 2005). Therefore, selection favours phenotypic adaptations that
enhance the ability of a male to prevail in male–
male contest, such as a rapid growth rate and larger males (Shine 1994, Schulte-Hostedde et al.
2001). In this study, SSD lack in small mammals
showed that sexual selection cannot be the principal cause of sexual size dimorphism. Female’s attention is directed by male’s odors, which transmit
a tremendous amount of information, such as a
male’s dominance status, physical condition and
oestrus (Zhao 2003, Sun 2005, Tang 2005, Zhang &
Shi 2007). The chemical signals of a male might
also advertise health or genetic quality to prospective mates (Penn & Potts 1998a). For example, that
a male’s secondary sexual displays honestly reveal
his parasite load have been found in numerous
studies (Clayton 1991, Kavaliers 1995a,b). Chemical signals, the intermediate of olfaction, could offer particularly effective indicators of an individual’s health and infection status, due to their im-
Sexual size dimorphism lacking in small mammals
55
Table 1. Body length (mm), litter size, sample size, and dimorphism ratio (female: male) for 95 species of small
mammals of Chiroptera, Rodentia, Scandentia, and Soricomorpha. (ZMCWNU - Zoological Museum of China
West Normal University, QTPIST - Qinghai-Tibetan Plateau Integrated Survey Team)
Female
SVL
Hipposideridae
Hipposideros armiger
Hipposideros pratti
Hipposideros bicolor
Hipposideros pratti
Molossidae
Tadaridae teniotis
Rhinolophidae
Rhinolophus affinis
Rhinolophus cornutus
Rhinolophus lepidus
Rhinolophus rouxi
Rhinolophus ferrumequinum
Rhinolophus pearsoni
Rhinolophus rex
Vespertilionidae
Myotis fimbriatus
Myotis laniger
Myotis pequinius
Myotis ricketti
Myotis daubenton
Miniopterus schreibersi
Nyctalus velutinus
Pipistrellus javanicus
Pipistrellus pulveratus
Tylonycteris pachypus
Male
Litter
Sample
SVL
size
size(F/M)
CHIROPTERA
f:m
References
94.5
94.0
46.5
90.5
96.7
91.0
44.7
90.4
10/9
20/7
8/9
26/14
0.98
1.03
1.04
1.00
Wang et al. (1990)
Wang et al. (1990)
Wu et al. (1993)
Wu et al. (1993)
90.0
90.9
7/6
0.99
Wang et al. (1990)
56.4
41.5
53.3
53.9
61.4
65.6
55.0
56.5
40.5
56.9
54.3
58.7
60.8
53.7
5/2
3/3
11/5
51/52
7/6
8/4
1/6
1.00
1.02
0.94
0.99
1.05
1.08
1.02
Wang et al. (1990)
Wang et al. (1990)
Wang et al. (1990)
Wang et al. (1990)
Wu et al. (1993)
Wu et al. (1993)
Wu et al. (1993)
44.2
40.3
58.2
68.4
39.1
58.1
71.9
47.9
45.9
37.8
43.0
40.5
61.0
69.6
39.6
58.4
75.4
45.7
49.4
35.6
15/7
6/5
12/1
5/4
11/11
60/60
20/20
10/10
7/3
23/16
1.03
1.00
0.95
0.98
0.99
1.00
0.95
1.05
0.93
1.06
Wang et al. (1990)
Wang et al. (1990)
Wang et al. (1990)
Wang et al. (1990)
Wu et al. (1993)
Wang et al. (1990)
Wang et al. (1990)
Wang et al. (1990)
Wang et al. (1990)
Wu et al. (1993)
28/33
17/21
495/670
104/160
68/129
179/178
11/15
21/22
16/9
12/12
7/6
9/11
5/5
9/8
10/11
10/10
9/11
7/10
11/11
3/5
1.04
1.00
0.98
0.93
0.97
0.96
0.97
0.96
0.99
0.96
0.98
1.02
1.01
1.01
1.06
0.99
0.99
1.00
1.02
1.02
0.91
0.90
0.96
1.09
0.94
Luo et al. (2000)
Luo et al. (2000)
Yuan et al. (2009)
Zhang (1986)
Luo et al. (2000)
Luo et al. (2000)
Luo et al. (2000)
Luo et al. (2000)
Luo et al. (2000)
Luo et al. (2000)
Luo et al. (2000)
Luo et al. (2000)
ZMCWNU
Luo et al. (2000)
Luo et al. (2000)
Luo et al. (2000)
Luo et al. (2000)
ZMCWNU
Luo et al. (2000)
Fan et al. (1996)
Li et al. (2004)
Liu et al. (2005)
Luo et al. (2000)
Wu et al. (1996)
Luo et al. (2000)
RODENTIA
Circetidae
Alticola roylei
Alticola semicanus
Cricetulus triton
Cricetulus barabensis
Cricetulus migratorius
Cricetulus longicaudatus
Cricetulus kamensis
Cricetulus eversmanni
Caryomys eva
Caryomys inez
Desmodillus auricularis
Eothenomys melanogaster
Eothenomys chinensis
Eothenomys olitor
Eothenomys proditor
Eothenomys custos
Eothenomys eleusis
Eothenomys eva
Eothenomys miletus
Microtus oeconomus
Microtus brandti
Microtus bedfordi
Microtus mandarinus
Microtus fortis
Meriones tamariscinus
98.5
110.4
153.5
91.2
100.5
89.6
91.7
107.9
93.693.0
96.0
99.8
115.8
87.3
103.9
104.1
94.6
94.0
111.9
115.0
115.9
112.4
110.8
127.1
149.2
94.5
110.4
156.1
98.4
103.6
93.2
94.2
112.4
94.2
97.3
98.2
97.6
114.6
86.1
97.6
105.6
95.3
93.8
109.7
112.3
127.9
116.6
101.5
140.5
159
6
9.94
5.84
4.59
2.31
2.42
8.20
3.45
5.19
40/21
378/415
8/17
D. Lu et al.
56
Table 1. (continued)
Sample
size(F/M)
98/124
12/17
52/48
44/45
10/13
9/7
58/60
23/27
32/30
f:m
References
0.95
0.93
0.96
0.98
0.98
0.99
0.94
0.92
0.94
Luo et al. (2000)
Luo et al. (2000)
Luo et al. (2000)
Luo et al. (2000)
Luo et al. (2000)
ZMCWNU
Luo et al. (2000)
Luo et al. (2000)
Luo et al. (2000)
3/3
0.95
ZMCWNU
Yang et al. (2000)
ZMCWNU
ZMCWNU
ZMCWNU
ZMCWNU
ZMCWNU
QTPIST (1986)
16/30
1.01
0.99
0.99
0.98
1.00
0.97
1.19
1.03
1.07
0.96
0.97
0.96
0.93
0.97
1.09
0.92
0.94
1.02
0.91
Wu et al. (1993)
Bao (1984)
ZMCWNU
ZMCWNU
ZMCWNU
Li et al. (1993)
Wu et al. (1993)
Wu et al. (1993)
Zhan (1985)
Zhang et al. (1998)
Wu et al. (1993)
8/6
14/15
11/10
4/8
7/7
0.99
0.99
1.00
1.07
0.97
ZMCWNU
QTPIST (1986)
Wu et al. (1993)
ZMCWNU
ZMCWNU
157.9
191.2
195.8
211.9
172.7
215.7
196.2
166.0
39/23
215.2
14/13
201.6
65/57
215.0
62/55
189.7
2.34
152/82
217.2
3.21
98/118
212.2
3.32
SCANDENTIA
0.95
0.89
0.97
0.99
0.91
0.99
0.92
Luo et al. (2000)
Luo et al. (2000)
Luo et al. (2000)
Guo et al. (2000)
Li et al. (1992)
Wang et al. (1996)
Yang et al. (2007)
Tupaiidae
Tupaia belangeri
165.0
176.0
3/3
SORICOMORPHA
0.94
Wu et al. (1993)
Soricidae
Crocidura suaveolens
Crocidura attenuata
Crocidura dracula
Suncus murinus
Anourosorex squamipes
Chimmarrogale himalayicus
65.8
78.7
92.9
105.0
86.0
107.4
64.4
77.7
94.2
119.5
82.9
102.3
1.02
1.01
0.99
0.88
1.04
1.05
Dong et al. (1989)
Dong et al. (1989)
Dong et al. (1989)
QTPIST (1986)
Wu et al. (1993)
Wu et al. (1993)
Meriones meridianus
Meriones erythrourus
Meriones unguiculatus
Pitymys leucurus
Pitymys sikimensis
Pitymys irene
Phodopus roborovskii
Phodopus sungorus
Rhombomys
Dipodidae
Eozapus setchuanus
Muridae
Apodemus chevrieri
Apodemus agrarius
Apodemus draco
Apodemus latronum
Berylmys bowersi
Leopoldamys edwardsi
Micromys minutus
Mus musculus
Mus pahari
Niviventer niviventer
Niviventer andersoni
Niviventer excelsior
Niviventer fulvescens
Rattus norvegicus
Rattus rattus
Rattus cremoriventer
Rattus losea
Rattus flavipectus
Rattus nitidus
Sciuridae
Callosciurus erythraeus
Dremomys lokriah
Dremomys pernyi
Eutamias sibiricus
Sciurotamias davidianus
Spalacinae
Myospalax rothschildi
Myospalax rufescens
Myospalax aspalax
Myospalax psilurus
Myospalax cansus
Myospalax baileyi
Myospalax fontanieri
Female
SVL
119.1
139.8
110.2
110.2
104.9
94.6
67.6
82.3
158.4
Male
SVL
125.6
149.9
114.7
112.1
106.6
95.3
71.7
89.3
167.9
86.7
91.3
99.5
105.1
96.6
104.5
236.0
250.2
75.2
73.3
90.8
136.6
170.5
150.5
132.6
161.3
154.4
155.5
138.4
155.9
152.1
98.7
105.9
97.7
106.1
237.0
258.0
63.3
71.0
85.0
142.3
176.2
156.1
142.1
166.0
142.1
168.9
146.7
152.9
167.9
210.3
180.6
184.3
147.5
217.8
213.0
181.7
184.9
137.7
223.8
Litter
size
5.19
7.01
6.22
5.93
6.03
5.69
5
6.5
5.38
4.00
4.00
6.96
9/9
9/20
4/8
3/1
6/9
5/4
20/30
7/7
3/5
8/14
7/12
11/18
4/11
6.78
6.00
7.00
3.00
3.60
5.13
3.50
4.05
9/15
6/11
7/10
31/31
19/10
5/3
Sexual size dimorphism lacking in small mammals
57
Figure 2. The correlation between female body length
and litter size inferred from 33 species. Litter size is
non-significantly correlated with female body length
across the 33 species (β=－0.1977).
Figure 1. Linear regression between Log10 female body
length and Log10 male body length for 33 little femalebiased (a) and 62 little male-biased (b) species. The sexual difference in size between the sexes is not significant
either in little female-biased (a: β = 0.9953) or in little
male-biased (b: β=1.014) species. The gray line represents a slope of 1, in which male and female size would
be equal. Each dot represents a single species based on
the mean body size of males and females.
mediate and often more labile nature compare to
morphological traits. Furthermore, chemical signals provide information about an individual’s
genetic compatibility at loci that control immune
recognition of parasites (Wakelin 1997, Penn &
Potts 1998a, 1998b, 1998c). Olfactory function may
play a considerable role in the identification of social status, and sexual receptiveness and act on individual, group, age, and sex recognition in small
mammals (Doty 1972, Theissen & Rice 1976). In
our study, SSD lacking small mammals and males
select mates through chemical odor instead of contest among individuals. The patterns had been
shown in many small mammals (Eisenberg et al.
1972, Blaustein 1981, Tai et al. 2001, Johnston 2003,
Zhang et al. 2003, Xie et al. 2008). Generally, sexual
dimorphism ， a phenotypic difference between
males and females of the same species, included
differences in morphology, size, ornamentation
and behavior, but also included mammalian olfaction (same as Blaustein 1981). Olfactory function
may play a key role in both intersexual (epigamic)
and intrasexual election in small mammals (Johnston 2003, Dechmann & Safi 2005).
Traditionally, female-biased SSD in mammals
has been attributed to the fecundity advantage
hypothesis, whereby selective pressures favour
larger and more fecund females (Cox et al. 2007,
Serrano-Meneses et al. 2007). In our study, there
was no significant relationship between female
size and fecundity, suggesting that fecundity advantage hypothesis cannot result in SSD of 33 little
female-biased SSD. This was consistent with the
study of Ralls (1976) that found this condition as
rarely the result of fecundity selection pressure
acting on mammals with female-biased SSD. SSD
lacking in little female-biased SSD might be related to odors because certain odors in small
mammals are probably functionally equivalent to
secondary sexual characteristics such as bird
plumage, deer antlers, or the bowers of bower
birds (Eisenberg 1972, Blaustein 1981).
We conclude that many species of small
mammals are regarded as showing little sexual
size dimorphism and lacking such obvious behavioral repertoires or conspicuous secondary characteristics may in fact be extremely sexual dimor-
58
phism through scent (Blaustein 1981; Johnston
2003). Our results, however, do not support that
the fecundity selection and the sexual selection
hypotheses contribute to sexual size dimorphism
in 95 species of small mammals. One feasible explanation of this phenomenon is that nocturnal, olfactory and gregarious lifestyle is adopted in
many species of small mammals (Brown & Macdonald 1985, Dechmann & Safi 2005).
Phylogenetic hypothesis is one faithful supplementary to study sexual size dimorphism in 95
species of small mammals (Björklund 1990,
Serrano-Meneses & Székely 2006). Nonetheless,
the molecular and morphological phylogenies we
collected from published literatures are inconsistant, to prevent us to conduct phylogenetic analyses to the selected specimens. Further integrated
works are needed to clarify the evolution of sexual
dimorphism and nocturnal biological habits in
small mammals.
Acknowledgments. Special thanks to anonymous
reviewers for critically reading the first manuscript.
Financial support was provided by the Foundation of Key
Laboratory of Southwest China Wildlife Resources
Conservation (Ministry of Education), China West
Normal University, P. R. China (XNYB01-3). We also owe
our sincere gratitude to the administrators of Zoological
Museum of China West Normal University, who gave us
their help to measure mammal specimens.
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