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A re-assessment of Rensch's rule in tuco-tucos (Rodentia: Ctenomyidae: Ctenomys) using a phylogenetic approach
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Original Investigation
A re-assessment of Rensch’s rule in tuco-tucos (Rodentia: Ctenomyidae: Ctenomys) using a phylogenetic approach Pablo Ariel Martínez a , Claudio Juan Bidau b,∗ a b
Departamento de Botânica, Ecologia e Zoologia, Centro de Biociencias, Universidade Federal do Rio Grande do Norte, Natal, Brazil Parana y los Claveles, 3304, Garupa, Misiones, Argentina
a r t i c l e
i n f o
Article history: Received 15 September 2014 Accepted 30 November 2014 Handled by Daisuke Koyabu Available online xxx Keywords: Body mass Model II regression Phylogenetic reduced major axis Scaling Sexual size dimorphism
a b s t r a c t Sexual size dimorphism (SSD) is affected by a large number of factors, mating system being one of the most relevant. Almost 70 species of subterranean rodents of the genus Ctenomys are considered highly polygynic, and polygyny jointly with absence of paternal care of the young, favours high SSD. In this respect, Rensch’s rule predicts that SSD scales with body size so that when males are larger than females SSD tends to increase with body size. We studied SSD and Rensch’s rule in 28 taxa of Ctenomys using a phylogenetic approach employing the method of phylogenetic reduced major axis (pRMA) to perform reduced major axis (RMA) model II regression in the form of log 10(male mass) on log 10(female mass). The RMA regression slope (ˇ) was statistically tested to accept or reject the null hypothesis that ˇpRMA = 1.0. A slope significantly >1.0 would signal concordance with Rensch’s rule. Our results showed that despite a high degree of male-biased SSD as expected from polygynic species, Rensch’s rule is not verified in this rodent group. The causes of the non-concordance with Rensch’s rule as well as its taxonomic level of application are discussed in terms of current models of SSD. © 2014 Deutsche Gesellschaft für Säugetierkunde. Published by Elsevier GmbH. All rights reserved.
Introduction One of the most conspicuous and common forms of difference between males and females of animals is sexual size dimorphism (SSD) (Andersson, 1994; Fairbairn, 1997, 2013; Fairbairn et al., 2007; Ralls and Mesnick, 2009). SSD may be male-biased as in most mammals and birds (MBSSD) (Lindenfors et al., 2007; Székely et al., 2007), or female-biased (FBSSD) as in the majority of invertebrates and some vertebrates (Blanckenhorn et al., 2007; Kupfer, 2007). In mammals, MBSSD is the rule although a number of exceptions are known in several orders (Ralls, 1976). A closely associated problem of SSD is that of Rensch’s rule. This rule states that the degree of SSD increases with increasing average body size in taxa were males are the larger sex while it decreases if SSD is biased towards females (Rensch, 1950, 1960; Fairbairn, 1997; Bidau and Martí, 2008a,b). Empirical analyses of many animal groups proved numerous exceptions to Rensch’s rule especially in cases of FBSSD and even when verified, there is controversy with respect to the causal mechanisms involved (Fairbairn, 1997; Gordon, 2006; Lindenfors et al., 2007; Martinez et al., 2014). SSD occurs in close correlation with mating strategies but Rensch’s
∗ Corresponding author. Tel.: +54 3764 4593561; fax: +54 3764 4593561. E-mail address: [email protected] (C.J. Bidau).
rule does not, and causal explanations for these phenomena are needed (Fairbairn, 2013; Martinez et al., 2014). Many large-scale studies of SSD in mammals have been performed in taxa displaying large body sizes which concurrently, are the most size-dimorphic such as Primates, Pinnipedia, ungulates, and others (Weckerly, 1998). Size dimorphism between males and females of small-sized mammals, although frequently small (Lu et al., 2014) may be as pronounced as in larger taxa (Moors, 1980; Schulte-Hostedde, 2007; Bidau and Medina, 2013). In the case of rodents, SSD is usually male-biased with the notable exceptions of sciurids and microtines (Bondrup-Nielsen and Ims, 1990; SchulteHostedde, 2007; Nandini, 2011). Subterranean rodents are represented worldwide (except for Australia and Antarctica) and constitute an extraordinary example of evolutionary convergence with species from different suborders and families having developed strikingly similar adaptations to the underground lifestyle (Nevo, 1999; Lacey et al., 2000; Begall et al., 2007). Studies of all aspects of body size of subterranean rodents are of interest because of the constraints imposed on size by the underground environment. These animals need to dig for shelter and food resources which constitutes an energetically highly demanding activity; thus, subterranean rodents have probably a larger demand of resources than aboveground ones which may impose strict constraints on final body size (McNab, 1979; Vleck, 1979; Nevo et al., 1986; Luna et al., 2002; Medina et al., 2007; Zelová et al., 2010;
http://dx.doi.org/10.1016/j.mambio.2014.11.008 1616-5047/© 2014 Deutsche Gesellschaft für Säugetierkunde. Published by Elsevier GmbH. All rights reserved.
Please cite this article in press as: Martínez, P.A., Bidau, C.J., A re-assessment of Rensch’s rule in tuco-tucos (Rodentia: Ctenomyidae: Ctenomys) using a phylogenetic approach. Mammal. Biol. (2014), http://dx.doi.org/10.1016/j.mambio.2014.11.008
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Zhang et al., 2012). The former is reflected in the unusual and disparate responses of underground rodents to environmental factors (Nevo et al., 1986; Medina et al., 2007; Zhang et al., 2012). Thus, it is plausible that these constraints on body size could differentially affect sexual size dimorphism. Within this assemblage of subterranean mammals, the genus Ctenomys shows the most extensive and recent radiation. Tucotucos include 68 named species and several innominate forms most of which occur in Argentina (Giménez et al., 2002; Bidau, 2006, 2014; Mirol et al., 2010; Gardner et al., 2014). SSD is usually malebiased in this genus which is expected because of the polygnic mating system of its species (Bidau and Medina, 2013). Tuco-tuco species are, with one or two exceptions (Ctenomys sociabilis, C. rionegrensis) normally solitary, highly territorial, and very aggressive rodents (Nevo, 1979, 1999; Reig et al., 1990; Zenuto et al., 2007; Beery et al., 2008; Zenuto, 2010; Tassino et al., 2011). Both sexes show intraspecific aggressive behaviour as common in specialised diggers (Smorkatcheva and Lukhtanov, 2014) although in well studied cases such as C. talarum males may be more aggressive than females, and levels of aggression may depend on population density (Zenuto et al., 2007; Zenuto, 2010). Also, at least in one case, C. peruanus, males are territorial but females are not (Nevo, 1979). Nevertheless, the fact that both sexes are usually involved in contests with conspecifics, it is plausible that this behaviour imposes further constraints on the difference in size between the sexes. Another factor that has been involved in body size variation in tuco-tucos, is intensity of predation (Medina et al., 2007): larger individuals may avoid predation by raptors better than smaller ones. Since both sexes would benefit from large size in regions of intense predation, sexual size dimorphism could be affected by this factor. In a previous paper, SSD was analysed in species and populations of Ctenomys (Bidau and Medina, 2013); results suggested that Rensch’s rule occurred in this genus. However, analyses were performed without consideration to phylogenetic relationships between species, and the approach was a populational one (see “Discussion”). Many organismal characteristics (e.g. body size) are frequently strongly associated with phylogeny: usually species cannot be regarded as drawn independently from the same distribution because they belong to a hierarchical phylogeny: a “phylogenetic signal” is the tendency of evolutionarily related organisms to resemble each other (Blomberg et al., 2003). Thus, several methods have been developed to take into consideration phylogenetic non-dependence (e.g. Felsenstein, 1985; Revell, 2012). A recent comprehensive molecular phylogeny of Ctenomys (Parada et al., 2011) allowed us to re-examine SSD and Rensch’s rule in tuco-tucos using a phylogenetic approach.
talarum) we included subspecies because they differ widely in habitat and body size (Table 1). In a third case, that of C. perrensi, three distinct chromosomal forms which are probably good biological species (Giménez et al., 2002; Mirol et al., 2010), were also incorporated. For analytical purposes mean body masses of each taxon were log 10-transformed. SSD of each taxon was first calculated as the raw ratio between the arithmetic means of male and female body mass (Fairbairn, 1997). However, the distribution of raw ratios is asymmetrical: values below 1.0 only vary between 1 and 0, while values higher than 1.0 have no upper limit. According to Lovich and Gibbons (1992), Smith (1999) and Fairbairn (2007), the fact of this asymmetry tends to exaggerate the perception of the degree and variance of SSD for ratios higher than 1.0. Logarithmic transformation of raw ratios in the form of log(male size/female size) or log(female size/male size) is also frequently used in studies of SSD, although it does not resolve all statistical problems produced by raw ratios (Smith, 1999). The only SSD index that satisfies all the characteristics of a good SSD estimator as outlined in Smith (1999) and Fairbairn (2007) is the SDI of Lovich and Gibbons (1992). SDI is calculated as the ratio of the larger to the smaller sex to which 1 is substracted. The result is arbitrarily assigned a negative value when males are larger than females, and a positive value when females are the larger sex. Since all these indices are widely used in the literature, we calculated the three of them for our dataset, for the sake of comparison (Table 1). To test the validity of Rensch’s rule within the Ctenomyidae we used phylogenetic reduced major axis (pRMA) regression with the aid of the “phytools” package (Revell, 2012), in the R.3.0.2 platform, using the phylogeny of Parada et al. (2011).pRMA regressions in the form of log 10(male body mass) on log 10(female body mass) were performed to evaluate the slope which is an estimator of the scaling of SSD with body mass. We used a Model II regression method since ordinary least-squares (OLS) regression is inadequate for this type of analysis (Fairbairn, 1997). The use of pRMA regression is also justified because RMA is symmetric (contra OLS) which means that a single regression line defines the bivariate relationship independently of which variable is X and which is Y, and this is the case of SSD comparisons (Smith, 2009): Rensch’s rule is supported when the slope ˇpRMA is significantly > 1.0, while slopes < 1.0 signal its reversion (Abouheif and Fairbairn, 1997; Fairbairn, 1997). To test H0 that ˇ = 1.0 (absence of Rensch’s rule or its converse) we calculated Clarke’s T statistic with adjusted degrees of freedom (Clarke, 1980; McCardle, 1988). Finally, because the taxonomic scale of application of Rensch’s rule may produce contrasting results, we performed intraspecific analyses of scaling of SSD with body size in two Ctenomys species, C. perrensi and C. talarum that were compared to similar tests applied to body size data of three other subterranean rodent species (Plateau zokor, Palestine blind mole rat, and yellow-faced pocket gopher) obtained from the literature.
Material and methods We obtained data of body mass for males and females of 28 Ctenomys taxa from the sources indicated in Table 1. Although body mass data for both sexes is available for more species (Bidau and Medina, 2013) we limited our study to those included in the recent phylogeny by Parada et al. (2011). All body mass measurements were obtained in the field from adult, sexually mature individuals. In the case of specimens measured by one of the authors (see Medina et al., 2007; Bidau and Medina, 2013) sexual maturity was assessed through the analysis of the reproductive status of individuals. For males, only those with scrotal testes were considered while for females, maturity was determined by inspection of vulva, uterus and ovaries. Pregnant females were excluded from the study. It was verified that data obtained from other sources matched these criteria. Although most taxa included in this study are recognised as Linnean species, in two cases (C. opimus and C.
Results Phylogenetic analysis of Rensch’s rule in Ctenomys Body mass of the analysed Ctenomys taxa varied widely (Table 1). The smallest males belonged to C. talarum talarum and the largest, to C. conoveri. Mean mass was 269.75 g, and the coefficient of variation was CV = 62.24. In the case of females, the smallest mass corresponded to C. pundti, and the heaviest females belonged to C. conoveri. Mean mass of the whole sample was 211.50 g, and CV = 49.22. Male and female body masses are highly significantly correlated (r = 0.89) but a paired samples t-test revealed a highly significant difference between both sexes (p = 0.001; df = 26). Regarding SSD, it was essentially male-biased as had been previously reported (Bidau and Medina, 2013) but a few cases of
Please cite this article in press as: Martínez, P.A., Bidau, C.J., A re-assessment of Rensch’s rule in tuco-tucos (Rodentia: Ctenomyidae: Ctenomys) using a phylogenetic approach. Mammal. Biol. (2014), http://dx.doi.org/10.1016/j.mambio.2014.11.008
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Authority
Common name
Male body mass (g)
Female body mass (g)
MBM/FBM
log(M/F)
Lovich & Gibbons
Reference
C. argentinus C. australis C. boliviensis C. conoveri C. coyhaiquensis C. flamarioni C. frater C. fulvus C. haigi C. lami C. magellanicus C. mendocinus C. minutus C. opimus opimus C. opimus luteolus C. pearsoni C. perrensi 1 C. perrensi 2 C. perrensi 3 C. pundti C. rionegrensis C. saltarius C. sociabilis C. talarum occidentalis C. talarum talarum C. torquatus C. tuconax C. tucumanus
Contreras & Berry. 1982 Rusconi. 1934 Waterhouse. 1848 Osgood, 1943 Kelt and Gallardo, 1994 Travi. 1981 Thomas. 1902 Philippi. 1930 Thomas. 1917 Freitas. 2001 Bennett. 1836 Philippi. 1869 Nehring. 1887 Wagner. 1848 Thomas.1900 Lessa &Langguth. 1983 Thomas. 1898 Thomas. 1898 Thomas. 1898 Nehring. 1920 Langguth & Abella. 1970 Thomas. 1912 Pearson and Christie, 1985 Justo. 1992 Thomas. 1898 Lichtenstein. 1830 Thomas. 1925 Thomas. 1900
Argentine tuco-tuco Southern tuco-tuco Bolivian tuco-tuco Conover’s tuco-tuco Coyhaique tuco-tuco Tuco-tuco of the dunes Forest tuco-tuco Tawny tuco-tuco Haig’s tuco-tuco Lami tuco-tuco Magellanic tuco-tuco Mendoza tuco-tuco Tiny tuco-tuco Highland tuco-tuco Highland tuco-tuco Pearson’s tuco-tuco Goya tuco-tuco Goya tuco-tuco Goya tuco-tuco Small tuco-tuco Rio Negro tuco-tuco Salta tuco-tuco Social tuco-tuco Western Talas tuco-tuco Talas tuco-tuco Collared tuco-tuco Robust tuco-tuco Tucuman tuco-tuco
193 349 650 900 140 248 290 223 229 238 254 107 237 457 270 220 222 335 284 98 179 190 213 118 89 229 351 240
155 366 420 520 116 194 215 220 152 193 222 100 186 284 138 212 90 230 268 77 150 191 207 157 107 190 393 169
1.25 0.95 1.55 1.73 1.21 1.28 1.35 1.01 1.51 1.23 1.15 1.07 1.27 1.61 1.96 1.04 2.47 1.46 1.06 1.27 1.19 0.99 1.03 0.75 0.83 1.21 0.89 1.42
0.0952 −0.0207 0.1897 0.2382 0.0817 0.1066 0.1300 0.0059 0.1780 0.0910 0.0607 0.0294 0.1052 0.2066 0.2935 0.0161 0.3921 0.1633 0.0252 0.1047 0.0768 −0.0023 0.0124 −0.1240 −0.0800 0.0811 −0.0491 0.1523
−0.2452 0.0487 −0.5476 −0.7308 −0.2069 −0.2784 −0.3488 −0.1363 −0.5066 −0.2332 −0.1500 −0.0700 −0.2742 −0.6092 −0.9565 −0.0377 −1.4667 −0.4565 −0.0597 −0.2727 −0.1933 0.0053 −0.0290 0.3305 0.2022 −0.2053 0.1197 −0.4201
Bidau and Medina (2013) Bidau and Medina (2013) Anderson (1997) Osgood (1943) and Anderson (1997) Kelt and Gallardo (1994) T.R.O. Freitas. pers. comm. Anderson (1997) Pine et al. (1979) Pearson (1984) T.R.O. Freitas. pers. comm. Medina et al. (2007) Bidau and Medina (2013) Anderson (1997) Anderson (1997) Bidau and Medina (2013) E. Lessa. pers. comm. Medina et al. (2007) Medina et al. (2007) Medina et al. (2007) Medina et al. (2007) E. Lessa. pers. comm. Medina et al. (2007) Pearson and Christie (1985) Medina et al. (2007) Medina et al. (2007) E. Lessa. pers. comm Bidau and Medina (2013) Medina et al. (2007)
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Please cite this article in press as: Martínez, P.A., Bidau, C.J., A re-assessment of Rensch’s rule in tuco-tucos (Rodentia: Ctenomyidae: Ctenomys) using a phylogenetic approach. Mammal. Biol. (2014), http://dx.doi.org/10.1016/j.mambio.2014.11.008
Table 1 Ctenomys taxa analysed in this paper. Mean body mass of males and females is given in grams. Raw sexual size dimorphism (SSD) is expressed as the ratio of the arithmetic means of males and females. (MBM/FBM): log(MBM/FBM) = log(MBM) − logFBM; Lovich & Gibbons: (M/F) − 1 or (F/M) − 1 (arbitrary negative values when M > F, and positive when F > M).
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Fig. 1. Phylogenetic reduced major axis (pRMA) regression of log 10(male body mass) on log 10(female body mass) for the Ctenomys sample analysed in this paper. Insert: Ctenomys magellanicus. Source: From Brehm, A., 1900. Brehms Tierleben. Allgemeine Kunde des Tierreichs. Die Säugetiere. Bibliographisches Institut, Leipzig & Wien. p. 598).
female-biased SSD were observed (Table 1). The highest malebiased dimorphism occurred in C. opimus luteolus, and the lowest in C. fulvus. Mean SSD for the whole sample was 1.28, and its CV = 22.76. The scaling of SSD with body mass was analysed by pRMA regression and original data. In both types of analyses the results are equivalent since the model residuals do not show phylogenetic signal ( = 4.2e−5). ˇpRMA was not significantly different from 1.0 (isometry), signalling the non-consistence with Rensch’s rule ( = 1.12, a = −0.18, r2 = 0.747, t = 1.138, df = 20.93, p = 0.268) (Fig. 1). The negative value of the a intercept indicates that, despite the few exceptions, the general tendency for SSD in Ctenomys is to be malebiased. A simple visualisation of the lack of scaling of SSD with body mass is to regress log 10(SSD) on log 10(male body mass): the regression slope is b = 0.066 which is not significantly different from 0 (t = 0.70, df = 26, p = 0.49). Scaling of SSD with body size in Ctenomys perrensi and C. talarum Most tuco-tuco species show very limited geographic distributions thus, it is difficult to sample enough populations to perform statistical comparisons of SSD variation. Two exceptions are C. perrensi, a complex of chromosomally differentiated populations of Corrientes province (Argentina), and C. talarum, a widespread Argentine species. The three traits analysed in C. perrensi (body mass, total body length and head plus body length) show a significant increase of SSD with body size consistent with Rensch’s rule (Table 2). It should be noted that in the case of TBL and HBL, the 1.0 value falls within the 95%CI although very near the lower end of the interval suggesting that an increase in degrees of freedom would leave this value outside the confidence limits. Conversely, in C. talarum the slope of the RMA regression of log 10 male HBL on log 10 female HBL is not significantly different from 1.0, i.e. no Rensch’s rule (Table 2). Discussion Ever since Darwin (1871) sexual dimorphism has been mainly attributed to sexual selection although today it is considered that classic natural selection (Darwin, 1859) can explain instances of dimorphism (Shine, 1991; Isaac, 2005). But, are sexual and natural selection two distinct processes? Sexual selection theory was defined by Darwin (1871) as “selection in relation to sex” which is viewed today as the result of competition for mating
opportunities (Carranza, 2009, 2010). Furthermore, Darwin (1859) defined natural selection in terms of survival while developing the theory of sexual selection to explain the secondary sexual characters that do not contribute to survival in an obvious way. In principle, sexual selection involves two processes: intrasexual selection or competition between individuals of the same sex for mates, and epigamic or intersexual selection that involves some form of choice by individuals of one sex, for individuals of the other (Andersson, 1994; Kokko et al., 2006; Clutton-Brock, 2007, 2009). Both processes may occur in either sex (Clutton-Brock, 2007, 2009, 2010; Carranza, 2009). Despite its importance, sexual selection is one of Darwin’s most controversial theories (Wallace, 1889; Fisher, 1930; Andersson, 1994; Clutton-Brock, 2007, 2010; Carranza, 2009, 2010; Roughgarden and Akc¸ay, 2010; Shuker, 2010; Rosvall, 2011). However, there are still difficulties in trying to differentiate sexual and natural selection leading some authors to propose the abandonment of the distinction and concentrate, as stated by Clutton-Brock (2010) “on contrasts in the components, intensity and targets of selection between males and females”. The associated problem of Rensch’s rule has also been extremely contentious since its formulation by Bernhard Rensch (1950, 1960). Interestingly enough, it was later proved that none of the examples of insects and birds provided by Rensch, follows the rule. There are several problems related to this apparent evolutionary pattern. First, its generalisation is not guaranteed. As Webb and Freckleton (2007) stated, the rule is only half right because species with female-biased SSD consistently break the rule. This is true of birds (Tubaro and Bertelli, 2003; Webb and Freckleton, 2007) and insects (Bidau et al. 2013). The second problem is that of mechanism: what factors could determine Rensch’s rule? While SSD can be readily explained through the action of sexual selection (Maynard-Smith, 1982, 1998; Reiss, 1989), the allometric relationship (scaling) between SSD and size requires a higher variability of size in males and a differential response to body size selection in males and females, a conflictive situation since both sexes share the vast majority of their genes (Fairbairn, 1997). The last hypothesis lacks empiric support and other proposed models are also not convincing (Reiss, 1986, 1989; Dale et al., 2007). Finally, the taxonomic scale of application of Rensch’s rule is another confounding factor. Although Rensch (1950) formulated his pattern as a seemingly interspecific trend, it is interesting that it has been often verified at the intraspecific level in groups where higher taxonomic units are not consistent with the rule. This was observed in the Greater Horseshoe bat (Rhinolophus ferrumequinum) (Wu et al., 2014), Panthera tigris subspecies (Martinez et al., 2014), domestic dog, cattle, and chicken (Polák and Frynta, 2010; Remeˇs and Székely, 2010; Frynta et al., 2012), and a melanopline grasshopper (Bidau and Martí, 2008a,b). As shown here and in Bidau and Medina (2013) at least one tuco-tuco species follows Rensch’s rule intraspecifically although the other one tested (C. talarum), does not at least for the analysed trait. Because the subterranean habit may impose selective pressures on growth and body size different from aboveground species, we considered three other subterranean rodents distantly related to tuco-tucos (Table 2). Again, the results are variable: both spalacids conform to Rensch’s rule while the pocket gopher species does not (Table 2). It could be inferred that the subterranean lifestyle does not impose a single scaling pattern of SSD at the intraspecific level but that conformity to Rensch’s rule or not, is a species-specific characteristic. At higher taxonomic levels the validity of the rule is questionable. Lindenfors et al. (2007) analysed Rensch’s rule in mammals of all extant orders (4269 species). The whole mammalian sample follows Rensch’s rule but one may wonder the utility of this information and the conclusions that can be drawn from it. Furthermore, of all mammalian orders, only Diprotodontia and Primates showed
Please cite this article in press as: Martínez, P.A., Bidau, C.J., A re-assessment of Rensch’s rule in tuco-tucos (Rodentia: Ctenomyidae: Ctenomys) using a phylogenetic approach. Mammal. Biol. (2014), http://dx.doi.org/10.1016/j.mambio.2014.11.008
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Table 2 Slopes of reduced major axis regressions (log 10 male size on log 10 female size) for intraspecific comparisons of several traits of five species of subterranean rodents. N: number of populations; R2 : coefficient of determination; ˇRMA: slope of the RMA regression; 95%CI: confidence interval. Classification
Common name
N
Trait
R2
ˇRMA
Eospalax baileyi
Spalacidae, Muroidea
Plateau zokor
Nannospalax ehrenbergi2 Cratogeomys castanops3
Spalacidae, Muroidea Geomyidae, Geomyoidea
Palestine blind mole rat Yellow-faced pocket gopher
Ctenomys perrensi4
Ctenomyidae, Octodontoidea
Perrens’s tuco-tuco
Ctenomys talarum5
Ctenomyidae, Octodontoidea
Talas tuco-tuco
21 21 12 11 11 24 24 24 15
Body mass Head + body length Body mass Total body length Head + body length Body mass Total body length Head + body length Head + body length
0.049 0.358 0.868 0.602 0.711 0.315 0.199 0.227 0.019
1.831 1.472 1.247 0.976 1.059 2.780 1.438 1.320 0.915
Species 1
95%CI 0.973–2.688 1.205–1.879 1.044–1.692 0.512–1.440 0.630–1.488 1.762–3.797 0.869–2.007 0.807–1.833 0.372–1.458
Source of data: 1 Zhang et al. (2012), 2 Nevo et al. (1986), 3 Russell and Baker (1955), 4 Bidau and Medina (2013); 5 this paper.
a pattern consistent with Rensch’s rule although in the latter it is really only present in the Catarrhyni (Leutenegger and Cheverud, 1982). Again, these broad analyses are of relative value: the Carnivora do not follow Rensch’s rule and this is also true for some of its families such as Felidae (Martinez et al., 2014) and Canidae (Bidau and Martínez, in preparation) while Mustelidae shows the converse to the rule (Moors, 1980). With respect to rodents, this order has not been thoroughly studied regarding SSD with the exception of squirrels and allies, which show a mixture of male- and female biased SSD (SchulteHostedde, 2007; Hayssen, 2008). A recent study of ground squirrels demonstrates that this group does not follow Rensch’s rule (Matˇeju˚ and Kratochvil, 2013). Tuco-tucos (Ctenomyidae) had been the subject of a SSD study only once (Bidau and Medina, 2013). This family is of interest with respect to SSD and sexual selection for two main reasons: first, these rodents are polygynic, a factor that promotes high SSD. The polygynic nature of tuco-tucos’ mating system has been revealed by studies of male–male contests, sperm competition, testis size, and penial morphology (Zenuto et al., 1999a,b; Graziani and Lacey, 2004; Bidau and Medina, 2013; Rocha-Barbosa et al., 2013). Second, it has been also shown that their large size variation exhibits a converse Bergmannian pattern along the distribution of the genus (Medina et al., 2007). The latter is relevant because it has been suggested that Rensch’s rule may be influenced by geographic body size variation (Blanckenhorn et al., 2006). In the previous study of Ctenomys SSD (Bidau and Medina, 2013) a different approach to that of the present paper was adopted namely, although a larger number of species were included in the study, they were not considered as units for regression analyses. Instead, a number of species were represented by several populations thus, the analyses were performed between populations (N = 97) and not species. With this approach, Rensch’s rule was verified (Bidau and Medina, 2013). However, since some species were over-represented in number of populations (e.g. C. talarum and C. perrensi) and these showed intra-specific Rensch’s rule, it is plausible that they were driving the regression equations towards the obtained results. In the present paper, we used an acrossspecies phylogenetic approach that revealed that, despite the considerable degree of SSD shown by the genus as expected from polygynic species, the slope of the RMA regression of log 10(male body mass) on log 10(female body mass) was not different from the null hypothesis of ˇ = 1.0 (confirmed by further evidence extracted from the analysis as shown in Results). This means that no allometry for SSD exists in tuco-tucos at the across-species level although the rule is probably verified at the intraspecific level, at least in some species. Why should scaling of SSD would differ between taxonomic levels (among species vs. populations within a species)? The most obvious answer is that different mechanisms, either proximate or ultimate, operate at intraspecific and interspecific levels. This distinction would imply that scaling of SSD within species is not a good predictor of the same phenomenon at the across-species
level. While different species of a genus have independent evolutionary histories since their initial divergence, populations within a species share a common gene-pool. If different populations are exposed to different environmental conditions in different parts of the species’ range, phenotypic plasticity could produce different responses of body size in males and females in each case, producing concordance with Rensch’s rule, its converse, or complete isometry (Blanckenhorn et al., 2006, 2007). These species-specific responses would be completely independent of the mode of scaling (if any) of SSD and body size at higher taxonomic levels. Despite the obvious conclusion that the Ctenomyidae do not follow Rensch’s rule as many other mammalian higher taxa, the present results add up to the growing idea that Rensch’s rule is hardly a rule at all (in the sense of Bergmann’s, Allen’s, or Gloger’s rule) but a pattern that may be present occasionally and perhaps, mainly at the intraspecific level. Of course, when it undoubtedly occurs, as in Catarrhyni Primates, it must be explained and since it is directly related to SSD, explanations based on sexual selection could apply. We suggest that further studies of Rensch’s rule must be performed at the intraspecific level especially in species of large geographic distributions (e.g. canids and felids within the Carnivora) to assess the importance of Bergmannian or counterBergmannian patterns on the shaping of SSD. Ethical standards The present work complies with the laws of the countries (Argentina and Brazil) in which it was developed. Conflict of interest The authors declare that they do not have conflict of interest. Acknowledgements We are extremely grateful to our colleagues Enrique Lessa (Montevideo) and Thales R.O. de Freitas (Porto Alegre) for invaluable body size data of Uruguayan and Brazilian Ctenomys species, respectively. Thanks are also due to two anonymous reviewers whose suggestions improved the manuscript. Pablo A. Martinez would like to thank the National Council of Technological and Scientific Development–CNPq for their financial support. References Abouheif, E., Fairbairn, D.J., 1997. A comparative analysis of allometry for sexual size dimorphism: assessing Rensch’s rule. Am. Nat. 149, 540–562. Anderson, S., 1997. Mammals of Bolivia: taxonomy and distribution. Bull. Am. Mus. Nat. Hist. 234, 1–652. Andersson, M., 1994. Sexual Selection. Princeton University Press, Princeton.
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Original Investigation
A re-assessment of Rensch’s rule in tuco-tucos (Rodentia: Ctenomyidae: Ctenomys) using a phylogenetic approach Pablo Ariel Martínez a , Claudio Juan Bidau b,∗ a b
Departamento de Botânica, Ecologia e Zoologia, Centro de Biociencias, Universidade Federal do Rio Grande do Norte, Natal, Brazil Parana y los Claveles, 3304, Garupa, Misiones, Argentina
a r t i c l e
i n f o
Article history: Received 15 September 2014 Accepted 30 November 2014 Handled by Daisuke Koyabu Available online xxx Keywords: Body mass Model II regression Phylogenetic reduced major axis Scaling Sexual size dimorphism
a b s t r a c t Sexual size dimorphism (SSD) is affected by a large number of factors, mating system being one of the most relevant. Almost 70 species of subterranean rodents of the genus Ctenomys are considered highly polygynic, and polygyny jointly with absence of paternal care of the young, favours high SSD. In this respect, Rensch’s rule predicts that SSD scales with body size so that when males are larger than females SSD tends to increase with body size. We studied SSD and Rensch’s rule in 28 taxa of Ctenomys using a phylogenetic approach employing the method of phylogenetic reduced major axis (pRMA) to perform reduced major axis (RMA) model II regression in the form of log 10(male mass) on log 10(female mass). The RMA regression slope (ˇ) was statistically tested to accept or reject the null hypothesis that ˇpRMA = 1.0. A slope significantly >1.0 would signal concordance with Rensch’s rule. Our results showed that despite a high degree of male-biased SSD as expected from polygynic species, Rensch’s rule is not verified in this rodent group. The causes of the non-concordance with Rensch’s rule as well as its taxonomic level of application are discussed in terms of current models of SSD. © 2014 Deutsche Gesellschaft für Säugetierkunde. Published by Elsevier GmbH. All rights reserved.
Introduction One of the most conspicuous and common forms of difference between males and females of animals is sexual size dimorphism (SSD) (Andersson, 1994; Fairbairn, 1997, 2013; Fairbairn et al., 2007; Ralls and Mesnick, 2009). SSD may be male-biased as in most mammals and birds (MBSSD) (Lindenfors et al., 2007; Székely et al., 2007), or female-biased (FBSSD) as in the majority of invertebrates and some vertebrates (Blanckenhorn et al., 2007; Kupfer, 2007). In mammals, MBSSD is the rule although a number of exceptions are known in several orders (Ralls, 1976). A closely associated problem of SSD is that of Rensch’s rule. This rule states that the degree of SSD increases with increasing average body size in taxa were males are the larger sex while it decreases if SSD is biased towards females (Rensch, 1950, 1960; Fairbairn, 1997; Bidau and Martí, 2008a,b). Empirical analyses of many animal groups proved numerous exceptions to Rensch’s rule especially in cases of FBSSD and even when verified, there is controversy with respect to the causal mechanisms involved (Fairbairn, 1997; Gordon, 2006; Lindenfors et al., 2007; Martinez et al., 2014). SSD occurs in close correlation with mating strategies but Rensch’s
∗ Corresponding author. Tel.: +54 3764 4593561; fax: +54 3764 4593561. E-mail address: [email protected] (C.J. Bidau).
rule does not, and causal explanations for these phenomena are needed (Fairbairn, 2013; Martinez et al., 2014). Many large-scale studies of SSD in mammals have been performed in taxa displaying large body sizes which concurrently, are the most size-dimorphic such as Primates, Pinnipedia, ungulates, and others (Weckerly, 1998). Size dimorphism between males and females of small-sized mammals, although frequently small (Lu et al., 2014) may be as pronounced as in larger taxa (Moors, 1980; Schulte-Hostedde, 2007; Bidau and Medina, 2013). In the case of rodents, SSD is usually male-biased with the notable exceptions of sciurids and microtines (Bondrup-Nielsen and Ims, 1990; SchulteHostedde, 2007; Nandini, 2011). Subterranean rodents are represented worldwide (except for Australia and Antarctica) and constitute an extraordinary example of evolutionary convergence with species from different suborders and families having developed strikingly similar adaptations to the underground lifestyle (Nevo, 1999; Lacey et al., 2000; Begall et al., 2007). Studies of all aspects of body size of subterranean rodents are of interest because of the constraints imposed on size by the underground environment. These animals need to dig for shelter and food resources which constitutes an energetically highly demanding activity; thus, subterranean rodents have probably a larger demand of resources than aboveground ones which may impose strict constraints on final body size (McNab, 1979; Vleck, 1979; Nevo et al., 1986; Luna et al., 2002; Medina et al., 2007; Zelová et al., 2010;
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Zhang et al., 2012). The former is reflected in the unusual and disparate responses of underground rodents to environmental factors (Nevo et al., 1986; Medina et al., 2007; Zhang et al., 2012). Thus, it is plausible that these constraints on body size could differentially affect sexual size dimorphism. Within this assemblage of subterranean mammals, the genus Ctenomys shows the most extensive and recent radiation. Tucotucos include 68 named species and several innominate forms most of which occur in Argentina (Giménez et al., 2002; Bidau, 2006, 2014; Mirol et al., 2010; Gardner et al., 2014). SSD is usually malebiased in this genus which is expected because of the polygnic mating system of its species (Bidau and Medina, 2013). Tuco-tuco species are, with one or two exceptions (Ctenomys sociabilis, C. rionegrensis) normally solitary, highly territorial, and very aggressive rodents (Nevo, 1979, 1999; Reig et al., 1990; Zenuto et al., 2007; Beery et al., 2008; Zenuto, 2010; Tassino et al., 2011). Both sexes show intraspecific aggressive behaviour as common in specialised diggers (Smorkatcheva and Lukhtanov, 2014) although in well studied cases such as C. talarum males may be more aggressive than females, and levels of aggression may depend on population density (Zenuto et al., 2007; Zenuto, 2010). Also, at least in one case, C. peruanus, males are territorial but females are not (Nevo, 1979). Nevertheless, the fact that both sexes are usually involved in contests with conspecifics, it is plausible that this behaviour imposes further constraints on the difference in size between the sexes. Another factor that has been involved in body size variation in tuco-tucos, is intensity of predation (Medina et al., 2007): larger individuals may avoid predation by raptors better than smaller ones. Since both sexes would benefit from large size in regions of intense predation, sexual size dimorphism could be affected by this factor. In a previous paper, SSD was analysed in species and populations of Ctenomys (Bidau and Medina, 2013); results suggested that Rensch’s rule occurred in this genus. However, analyses were performed without consideration to phylogenetic relationships between species, and the approach was a populational one (see “Discussion”). Many organismal characteristics (e.g. body size) are frequently strongly associated with phylogeny: usually species cannot be regarded as drawn independently from the same distribution because they belong to a hierarchical phylogeny: a “phylogenetic signal” is the tendency of evolutionarily related organisms to resemble each other (Blomberg et al., 2003). Thus, several methods have been developed to take into consideration phylogenetic non-dependence (e.g. Felsenstein, 1985; Revell, 2012). A recent comprehensive molecular phylogeny of Ctenomys (Parada et al., 2011) allowed us to re-examine SSD and Rensch’s rule in tuco-tucos using a phylogenetic approach.
talarum) we included subspecies because they differ widely in habitat and body size (Table 1). In a third case, that of C. perrensi, three distinct chromosomal forms which are probably good biological species (Giménez et al., 2002; Mirol et al., 2010), were also incorporated. For analytical purposes mean body masses of each taxon were log 10-transformed. SSD of each taxon was first calculated as the raw ratio between the arithmetic means of male and female body mass (Fairbairn, 1997). However, the distribution of raw ratios is asymmetrical: values below 1.0 only vary between 1 and 0, while values higher than 1.0 have no upper limit. According to Lovich and Gibbons (1992), Smith (1999) and Fairbairn (2007), the fact of this asymmetry tends to exaggerate the perception of the degree and variance of SSD for ratios higher than 1.0. Logarithmic transformation of raw ratios in the form of log(male size/female size) or log(female size/male size) is also frequently used in studies of SSD, although it does not resolve all statistical problems produced by raw ratios (Smith, 1999). The only SSD index that satisfies all the characteristics of a good SSD estimator as outlined in Smith (1999) and Fairbairn (2007) is the SDI of Lovich and Gibbons (1992). SDI is calculated as the ratio of the larger to the smaller sex to which 1 is substracted. The result is arbitrarily assigned a negative value when males are larger than females, and a positive value when females are the larger sex. Since all these indices are widely used in the literature, we calculated the three of them for our dataset, for the sake of comparison (Table 1). To test the validity of Rensch’s rule within the Ctenomyidae we used phylogenetic reduced major axis (pRMA) regression with the aid of the “phytools” package (Revell, 2012), in the R.3.0.2 platform, using the phylogeny of Parada et al. (2011).pRMA regressions in the form of log 10(male body mass) on log 10(female body mass) were performed to evaluate the slope which is an estimator of the scaling of SSD with body mass. We used a Model II regression method since ordinary least-squares (OLS) regression is inadequate for this type of analysis (Fairbairn, 1997). The use of pRMA regression is also justified because RMA is symmetric (contra OLS) which means that a single regression line defines the bivariate relationship independently of which variable is X and which is Y, and this is the case of SSD comparisons (Smith, 2009): Rensch’s rule is supported when the slope ˇpRMA is significantly > 1.0, while slopes < 1.0 signal its reversion (Abouheif and Fairbairn, 1997; Fairbairn, 1997). To test H0 that ˇ = 1.0 (absence of Rensch’s rule or its converse) we calculated Clarke’s T statistic with adjusted degrees of freedom (Clarke, 1980; McCardle, 1988). Finally, because the taxonomic scale of application of Rensch’s rule may produce contrasting results, we performed intraspecific analyses of scaling of SSD with body size in two Ctenomys species, C. perrensi and C. talarum that were compared to similar tests applied to body size data of three other subterranean rodent species (Plateau zokor, Palestine blind mole rat, and yellow-faced pocket gopher) obtained from the literature.
Material and methods We obtained data of body mass for males and females of 28 Ctenomys taxa from the sources indicated in Table 1. Although body mass data for both sexes is available for more species (Bidau and Medina, 2013) we limited our study to those included in the recent phylogeny by Parada et al. (2011). All body mass measurements were obtained in the field from adult, sexually mature individuals. In the case of specimens measured by one of the authors (see Medina et al., 2007; Bidau and Medina, 2013) sexual maturity was assessed through the analysis of the reproductive status of individuals. For males, only those with scrotal testes were considered while for females, maturity was determined by inspection of vulva, uterus and ovaries. Pregnant females were excluded from the study. It was verified that data obtained from other sources matched these criteria. Although most taxa included in this study are recognised as Linnean species, in two cases (C. opimus and C.
Results Phylogenetic analysis of Rensch’s rule in Ctenomys Body mass of the analysed Ctenomys taxa varied widely (Table 1). The smallest males belonged to C. talarum talarum and the largest, to C. conoveri. Mean mass was 269.75 g, and the coefficient of variation was CV = 62.24. In the case of females, the smallest mass corresponded to C. pundti, and the heaviest females belonged to C. conoveri. Mean mass of the whole sample was 211.50 g, and CV = 49.22. Male and female body masses are highly significantly correlated (r = 0.89) but a paired samples t-test revealed a highly significant difference between both sexes (p = 0.001; df = 26). Regarding SSD, it was essentially male-biased as had been previously reported (Bidau and Medina, 2013) but a few cases of
Please cite this article in press as: Martínez, P.A., Bidau, C.J., A re-assessment of Rensch’s rule in tuco-tucos (Rodentia: Ctenomyidae: Ctenomys) using a phylogenetic approach. Mammal. Biol. (2014), http://dx.doi.org/10.1016/j.mambio.2014.11.008
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Authority
Common name
Male body mass (g)
Female body mass (g)
MBM/FBM
log(M/F)
Lovich & Gibbons
Reference
C. argentinus C. australis C. boliviensis C. conoveri C. coyhaiquensis C. flamarioni C. frater C. fulvus C. haigi C. lami C. magellanicus C. mendocinus C. minutus C. opimus opimus C. opimus luteolus C. pearsoni C. perrensi 1 C. perrensi 2 C. perrensi 3 C. pundti C. rionegrensis C. saltarius C. sociabilis C. talarum occidentalis C. talarum talarum C. torquatus C. tuconax C. tucumanus
Contreras & Berry. 1982 Rusconi. 1934 Waterhouse. 1848 Osgood, 1943 Kelt and Gallardo, 1994 Travi. 1981 Thomas. 1902 Philippi. 1930 Thomas. 1917 Freitas. 2001 Bennett. 1836 Philippi. 1869 Nehring. 1887 Wagner. 1848 Thomas.1900 Lessa &Langguth. 1983 Thomas. 1898 Thomas. 1898 Thomas. 1898 Nehring. 1920 Langguth & Abella. 1970 Thomas. 1912 Pearson and Christie, 1985 Justo. 1992 Thomas. 1898 Lichtenstein. 1830 Thomas. 1925 Thomas. 1900
Argentine tuco-tuco Southern tuco-tuco Bolivian tuco-tuco Conover’s tuco-tuco Coyhaique tuco-tuco Tuco-tuco of the dunes Forest tuco-tuco Tawny tuco-tuco Haig’s tuco-tuco Lami tuco-tuco Magellanic tuco-tuco Mendoza tuco-tuco Tiny tuco-tuco Highland tuco-tuco Highland tuco-tuco Pearson’s tuco-tuco Goya tuco-tuco Goya tuco-tuco Goya tuco-tuco Small tuco-tuco Rio Negro tuco-tuco Salta tuco-tuco Social tuco-tuco Western Talas tuco-tuco Talas tuco-tuco Collared tuco-tuco Robust tuco-tuco Tucuman tuco-tuco
193 349 650 900 140 248 290 223 229 238 254 107 237 457 270 220 222 335 284 98 179 190 213 118 89 229 351 240
155 366 420 520 116 194 215 220 152 193 222 100 186 284 138 212 90 230 268 77 150 191 207 157 107 190 393 169
1.25 0.95 1.55 1.73 1.21 1.28 1.35 1.01 1.51 1.23 1.15 1.07 1.27 1.61 1.96 1.04 2.47 1.46 1.06 1.27 1.19 0.99 1.03 0.75 0.83 1.21 0.89 1.42
0.0952 −0.0207 0.1897 0.2382 0.0817 0.1066 0.1300 0.0059 0.1780 0.0910 0.0607 0.0294 0.1052 0.2066 0.2935 0.0161 0.3921 0.1633 0.0252 0.1047 0.0768 −0.0023 0.0124 −0.1240 −0.0800 0.0811 −0.0491 0.1523
−0.2452 0.0487 −0.5476 −0.7308 −0.2069 −0.2784 −0.3488 −0.1363 −0.5066 −0.2332 −0.1500 −0.0700 −0.2742 −0.6092 −0.9565 −0.0377 −1.4667 −0.4565 −0.0597 −0.2727 −0.1933 0.0053 −0.0290 0.3305 0.2022 −0.2053 0.1197 −0.4201
Bidau and Medina (2013) Bidau and Medina (2013) Anderson (1997) Osgood (1943) and Anderson (1997) Kelt and Gallardo (1994) T.R.O. Freitas. pers. comm. Anderson (1997) Pine et al. (1979) Pearson (1984) T.R.O. Freitas. pers. comm. Medina et al. (2007) Bidau and Medina (2013) Anderson (1997) Anderson (1997) Bidau and Medina (2013) E. Lessa. pers. comm. Medina et al. (2007) Medina et al. (2007) Medina et al. (2007) Medina et al. (2007) E. Lessa. pers. comm. Medina et al. (2007) Pearson and Christie (1985) Medina et al. (2007) Medina et al. (2007) E. Lessa. pers. comm Bidau and Medina (2013) Medina et al. (2007)
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Please cite this article in press as: Martínez, P.A., Bidau, C.J., A re-assessment of Rensch’s rule in tuco-tucos (Rodentia: Ctenomyidae: Ctenomys) using a phylogenetic approach. Mammal. Biol. (2014), http://dx.doi.org/10.1016/j.mambio.2014.11.008
Table 1 Ctenomys taxa analysed in this paper. Mean body mass of males and females is given in grams. Raw sexual size dimorphism (SSD) is expressed as the ratio of the arithmetic means of males and females. (MBM/FBM): log(MBM/FBM) = log(MBM) − logFBM; Lovich & Gibbons: (M/F) − 1 or (F/M) − 1 (arbitrary negative values when M > F, and positive when F > M).
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Fig. 1. Phylogenetic reduced major axis (pRMA) regression of log 10(male body mass) on log 10(female body mass) for the Ctenomys sample analysed in this paper. Insert: Ctenomys magellanicus. Source: From Brehm, A., 1900. Brehms Tierleben. Allgemeine Kunde des Tierreichs. Die Säugetiere. Bibliographisches Institut, Leipzig & Wien. p. 598).
female-biased SSD were observed (Table 1). The highest malebiased dimorphism occurred in C. opimus luteolus, and the lowest in C. fulvus. Mean SSD for the whole sample was 1.28, and its CV = 22.76. The scaling of SSD with body mass was analysed by pRMA regression and original data. In both types of analyses the results are equivalent since the model residuals do not show phylogenetic signal ( = 4.2e−5). ˇpRMA was not significantly different from 1.0 (isometry), signalling the non-consistence with Rensch’s rule ( = 1.12, a = −0.18, r2 = 0.747, t = 1.138, df = 20.93, p = 0.268) (Fig. 1). The negative value of the a intercept indicates that, despite the few exceptions, the general tendency for SSD in Ctenomys is to be malebiased. A simple visualisation of the lack of scaling of SSD with body mass is to regress log 10(SSD) on log 10(male body mass): the regression slope is b = 0.066 which is not significantly different from 0 (t = 0.70, df = 26, p = 0.49). Scaling of SSD with body size in Ctenomys perrensi and C. talarum Most tuco-tuco species show very limited geographic distributions thus, it is difficult to sample enough populations to perform statistical comparisons of SSD variation. Two exceptions are C. perrensi, a complex of chromosomally differentiated populations of Corrientes province (Argentina), and C. talarum, a widespread Argentine species. The three traits analysed in C. perrensi (body mass, total body length and head plus body length) show a significant increase of SSD with body size consistent with Rensch’s rule (Table 2). It should be noted that in the case of TBL and HBL, the 1.0 value falls within the 95%CI although very near the lower end of the interval suggesting that an increase in degrees of freedom would leave this value outside the confidence limits. Conversely, in C. talarum the slope of the RMA regression of log 10 male HBL on log 10 female HBL is not significantly different from 1.0, i.e. no Rensch’s rule (Table 2). Discussion Ever since Darwin (1871) sexual dimorphism has been mainly attributed to sexual selection although today it is considered that classic natural selection (Darwin, 1859) can explain instances of dimorphism (Shine, 1991; Isaac, 2005). But, are sexual and natural selection two distinct processes? Sexual selection theory was defined by Darwin (1871) as “selection in relation to sex” which is viewed today as the result of competition for mating
opportunities (Carranza, 2009, 2010). Furthermore, Darwin (1859) defined natural selection in terms of survival while developing the theory of sexual selection to explain the secondary sexual characters that do not contribute to survival in an obvious way. In principle, sexual selection involves two processes: intrasexual selection or competition between individuals of the same sex for mates, and epigamic or intersexual selection that involves some form of choice by individuals of one sex, for individuals of the other (Andersson, 1994; Kokko et al., 2006; Clutton-Brock, 2007, 2009). Both processes may occur in either sex (Clutton-Brock, 2007, 2009, 2010; Carranza, 2009). Despite its importance, sexual selection is one of Darwin’s most controversial theories (Wallace, 1889; Fisher, 1930; Andersson, 1994; Clutton-Brock, 2007, 2010; Carranza, 2009, 2010; Roughgarden and Akc¸ay, 2010; Shuker, 2010; Rosvall, 2011). However, there are still difficulties in trying to differentiate sexual and natural selection leading some authors to propose the abandonment of the distinction and concentrate, as stated by Clutton-Brock (2010) “on contrasts in the components, intensity and targets of selection between males and females”. The associated problem of Rensch’s rule has also been extremely contentious since its formulation by Bernhard Rensch (1950, 1960). Interestingly enough, it was later proved that none of the examples of insects and birds provided by Rensch, follows the rule. There are several problems related to this apparent evolutionary pattern. First, its generalisation is not guaranteed. As Webb and Freckleton (2007) stated, the rule is only half right because species with female-biased SSD consistently break the rule. This is true of birds (Tubaro and Bertelli, 2003; Webb and Freckleton, 2007) and insects (Bidau et al. 2013). The second problem is that of mechanism: what factors could determine Rensch’s rule? While SSD can be readily explained through the action of sexual selection (Maynard-Smith, 1982, 1998; Reiss, 1989), the allometric relationship (scaling) between SSD and size requires a higher variability of size in males and a differential response to body size selection in males and females, a conflictive situation since both sexes share the vast majority of their genes (Fairbairn, 1997). The last hypothesis lacks empiric support and other proposed models are also not convincing (Reiss, 1986, 1989; Dale et al., 2007). Finally, the taxonomic scale of application of Rensch’s rule is another confounding factor. Although Rensch (1950) formulated his pattern as a seemingly interspecific trend, it is interesting that it has been often verified at the intraspecific level in groups where higher taxonomic units are not consistent with the rule. This was observed in the Greater Horseshoe bat (Rhinolophus ferrumequinum) (Wu et al., 2014), Panthera tigris subspecies (Martinez et al., 2014), domestic dog, cattle, and chicken (Polák and Frynta, 2010; Remeˇs and Székely, 2010; Frynta et al., 2012), and a melanopline grasshopper (Bidau and Martí, 2008a,b). As shown here and in Bidau and Medina (2013) at least one tuco-tuco species follows Rensch’s rule intraspecifically although the other one tested (C. talarum), does not at least for the analysed trait. Because the subterranean habit may impose selective pressures on growth and body size different from aboveground species, we considered three other subterranean rodents distantly related to tuco-tucos (Table 2). Again, the results are variable: both spalacids conform to Rensch’s rule while the pocket gopher species does not (Table 2). It could be inferred that the subterranean lifestyle does not impose a single scaling pattern of SSD at the intraspecific level but that conformity to Rensch’s rule or not, is a species-specific characteristic. At higher taxonomic levels the validity of the rule is questionable. Lindenfors et al. (2007) analysed Rensch’s rule in mammals of all extant orders (4269 species). The whole mammalian sample follows Rensch’s rule but one may wonder the utility of this information and the conclusions that can be drawn from it. Furthermore, of all mammalian orders, only Diprotodontia and Primates showed
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Table 2 Slopes of reduced major axis regressions (log 10 male size on log 10 female size) for intraspecific comparisons of several traits of five species of subterranean rodents. N: number of populations; R2 : coefficient of determination; ˇRMA: slope of the RMA regression; 95%CI: confidence interval. Classification
Common name
N
Trait
R2
ˇRMA
Eospalax baileyi
Spalacidae, Muroidea
Plateau zokor
Nannospalax ehrenbergi2 Cratogeomys castanops3
Spalacidae, Muroidea Geomyidae, Geomyoidea
Palestine blind mole rat Yellow-faced pocket gopher
Ctenomys perrensi4
Ctenomyidae, Octodontoidea
Perrens’s tuco-tuco
Ctenomys talarum5
Ctenomyidae, Octodontoidea
Talas tuco-tuco
21 21 12 11 11 24 24 24 15
Body mass Head + body length Body mass Total body length Head + body length Body mass Total body length Head + body length Head + body length
0.049 0.358 0.868 0.602 0.711 0.315 0.199 0.227 0.019
1.831 1.472 1.247 0.976 1.059 2.780 1.438 1.320 0.915
Species 1
95%CI 0.973–2.688 1.205–1.879 1.044–1.692 0.512–1.440 0.630–1.488 1.762–3.797 0.869–2.007 0.807–1.833 0.372–1.458
Source of data: 1 Zhang et al. (2012), 2 Nevo et al. (1986), 3 Russell and Baker (1955), 4 Bidau and Medina (2013); 5 this paper.
a pattern consistent with Rensch’s rule although in the latter it is really only present in the Catarrhyni (Leutenegger and Cheverud, 1982). Again, these broad analyses are of relative value: the Carnivora do not follow Rensch’s rule and this is also true for some of its families such as Felidae (Martinez et al., 2014) and Canidae (Bidau and Martínez, in preparation) while Mustelidae shows the converse to the rule (Moors, 1980). With respect to rodents, this order has not been thoroughly studied regarding SSD with the exception of squirrels and allies, which show a mixture of male- and female biased SSD (SchulteHostedde, 2007; Hayssen, 2008). A recent study of ground squirrels demonstrates that this group does not follow Rensch’s rule (Matˇeju˚ and Kratochvil, 2013). Tuco-tucos (Ctenomyidae) had been the subject of a SSD study only once (Bidau and Medina, 2013). This family is of interest with respect to SSD and sexual selection for two main reasons: first, these rodents are polygynic, a factor that promotes high SSD. The polygynic nature of tuco-tucos’ mating system has been revealed by studies of male–male contests, sperm competition, testis size, and penial morphology (Zenuto et al., 1999a,b; Graziani and Lacey, 2004; Bidau and Medina, 2013; Rocha-Barbosa et al., 2013). Second, it has been also shown that their large size variation exhibits a converse Bergmannian pattern along the distribution of the genus (Medina et al., 2007). The latter is relevant because it has been suggested that Rensch’s rule may be influenced by geographic body size variation (Blanckenhorn et al., 2006). In the previous study of Ctenomys SSD (Bidau and Medina, 2013) a different approach to that of the present paper was adopted namely, although a larger number of species were included in the study, they were not considered as units for regression analyses. Instead, a number of species were represented by several populations thus, the analyses were performed between populations (N = 97) and not species. With this approach, Rensch’s rule was verified (Bidau and Medina, 2013). However, since some species were over-represented in number of populations (e.g. C. talarum and C. perrensi) and these showed intra-specific Rensch’s rule, it is plausible that they were driving the regression equations towards the obtained results. In the present paper, we used an acrossspecies phylogenetic approach that revealed that, despite the considerable degree of SSD shown by the genus as expected from polygynic species, the slope of the RMA regression of log 10(male body mass) on log 10(female body mass) was not different from the null hypothesis of ˇ = 1.0 (confirmed by further evidence extracted from the analysis as shown in Results). This means that no allometry for SSD exists in tuco-tucos at the across-species level although the rule is probably verified at the intraspecific level, at least in some species. Why should scaling of SSD would differ between taxonomic levels (among species vs. populations within a species)? The most obvious answer is that different mechanisms, either proximate or ultimate, operate at intraspecific and interspecific levels. This distinction would imply that scaling of SSD within species is not a good predictor of the same phenomenon at the across-species
level. While different species of a genus have independent evolutionary histories since their initial divergence, populations within a species share a common gene-pool. If different populations are exposed to different environmental conditions in different parts of the species’ range, phenotypic plasticity could produce different responses of body size in males and females in each case, producing concordance with Rensch’s rule, its converse, or complete isometry (Blanckenhorn et al., 2006, 2007). These species-specific responses would be completely independent of the mode of scaling (if any) of SSD and body size at higher taxonomic levels. Despite the obvious conclusion that the Ctenomyidae do not follow Rensch’s rule as many other mammalian higher taxa, the present results add up to the growing idea that Rensch’s rule is hardly a rule at all (in the sense of Bergmann’s, Allen’s, or Gloger’s rule) but a pattern that may be present occasionally and perhaps, mainly at the intraspecific level. Of course, when it undoubtedly occurs, as in Catarrhyni Primates, it must be explained and since it is directly related to SSD, explanations based on sexual selection could apply. We suggest that further studies of Rensch’s rule must be performed at the intraspecific level especially in species of large geographic distributions (e.g. canids and felids within the Carnivora) to assess the importance of Bergmannian or counterBergmannian patterns on the shaping of SSD. Ethical standards The present work complies with the laws of the countries (Argentina and Brazil) in which it was developed. Conflict of interest The authors declare that they do not have conflict of interest. Acknowledgements We are extremely grateful to our colleagues Enrique Lessa (Montevideo) and Thales R.O. de Freitas (Porto Alegre) for invaluable body size data of Uruguayan and Brazilian Ctenomys species, respectively. Thanks are also due to two anonymous reviewers whose suggestions improved the manuscript. Pablo A. Martinez would like to thank the National Council of Technological and Scientific Development–CNPq for their financial support. References Abouheif, E., Fairbairn, D.J., 1997. A comparative analysis of allometry for sexual size dimorphism: assessing Rensch’s rule. Am. Nat. 149, 540–562. Anderson, S., 1997. Mammals of Bolivia: taxonomy and distribution. Bull. Am. Mus. Nat. Hist. 234, 1–652. Andersson, M., 1994. Sexual Selection. Princeton University Press, Princeton.
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Please cite this article in press as: Martínez, P.A., Bidau, C.J., A re-assessment of Rensch’s rule in tuco-tucos (Rodentia: Ctenomyidae: Ctenomys) using a phylogenetic approach. Mammal. Biol. (2014), http://dx.doi.org/10.1016/j.mambio.2014.11.008