Sexual dimorphism of size or shape is widespread in animals and has attracted considerable interest from biologists (Kolata 1977; Hedrick and Temeles 1989; Bonnet et al. 2010). It is assumed that sexual dimorphism results from the interactions between natural selection and sexual selection: natural selection favors morphological traits that maximize survival and juvenile growth rates while sexual selection influences morphological characteristics in ways that directly increase reproductive success (Lande and Arnold 1985; Shine 1990; Rivera 2008). Sexual selection and natural selection can interact in opposition or in synergy, depending upon various factors (Hedrick and Temeles 1989; Shine 1989, 1990; Arnold 1994; Djordjevic et al. 2011). Examining the size and shape of traits together provides a much-more complete quantification of sexual dimorphism, as the 2 components are inherently related to one another (Travis 1994; Willemsen and Hailey 2003; Mann et al. 2006; Kuo et al. 2009; Bonnet et al. 2010).

Turtles are an excellent group in which to test the selective forces of sexual dimorphism. First, they exhibit a diversity of ecologies (strictly terrestrial to highly aquatic), mating strategies (female choice, combat, and/or forced insemination), and types of sexual dimorphism (males larger than females to females larger than males). Second, the absence of parental care in turtles could minimize the overlap between the male and female roles and favor multiple mating systems (Bonnet et al. 2001). Third, their body shape can be assessed via measurements of the shell geometry because feeding and reproductive statuses do not modify shell dimensions (Bonnet et al. 2010). Therefore, extensive and profound research on turtle sexual dimorphism has been conducted worldwide, ranging in scope from one focal species (Gibbons and Lovich 1990; Bonnet et al. 2001) to multiple species (Willemsen and Hailey 2003; Kaddour et al. 2008; Barros et al. 2012) or different geographical populations (Iverson 1985; Stillwell et al. 2007; Lovich et al. 2010; Lefebvre et al. 2011).

Beal's eyed turtle Sacalia bealei is endemic to China and has been listed as a Convention on International Trade in Endangered Species of Wild Fauna and Flora (CITES 2017) Appendix II species. However, data on sexual dimorphism in size and shape of S. bealei are lacking except for a few studies with limited data on size measurements (Chen 1991; Zhang et al. 1998), and no quantitative analysis has been done. We studied the sexual dimorphism of S. bealei by analyzing various morphological characteristics and used these analyses to provide plausible explanations for the adaptive evolution of sexual dimorphism in S. bealei.

METHODS

RESULTS

In this study, the SDI for CL was (139.4/127.8) − 1 = 0.09, indicating that females were slightly larger than males. The comparisons between the sexes of the size-corrected morphological traits (body proportions or body shape) are summarized in Table 1. On average, females attained larger maximal and mean sizes than did males. This translated into greater absolute values for all the traits we measured except for PTL (more distally located cloaca in males), ASJ (more space available to move the tail in males), and TL (longer tail in males).

Table 1. Sexual dimorphism of body size and shape in adult S. bealei from Fujian Province of China. Results for CL and PTL are means, and statistics are from ANOVA by sex, while other variables are adjusted means and statistics are from ANCOVA by sex with CL, PL, or HL used as a covariate (see text).^a

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Females displayed a more voluminous shell than did males. Notably, they exhibited a longer plastron (PL, MPL) and higher carapace (CH, CCW) relative to CL, thereby providing a larger internal volume. Females also exhibited a relatively wider head (HW relative to CL; HW relative to HL). In males, the openings between the plastron and the carapace (BL and ASJ) were more developed. Overall, the spaces available to move the legs, the head, and the tail were relatively larger in males.

DISCUSSION

Turtle species vary greatly in the degree of SDI, with the larger sex ranging from 1% to 158% larger than the smaller sex (Ernst et al. 1994). Our results showed, when compared with other species that have females as the larger sex, that S. bealei displayed relatively small SDI values (0.09 compared with mean SDI = 0.36; median SDI = 0.23; Gibbons and Lovich 1990).

Female-biased SSD is thought to be driven by both sexual selection and natural selection. According to the sexual selection hypothesis, SSD would contribute to copulation success (Lande and Arnold 1985; Hedrick and Temeles 1989). Males are usually larger than females in species with male combat and/or forced insemination and are smaller than females when these behaviors are absent (Berry and Shine 1980; Mann et al. 2006). For species in the latter category, males often show elaborate precoital displays and highly developed nuptial structures (Stephens and Wiens 2009). In addition, SSD correlates with habitat types, which could affect male mating strategy. In truly aquatic species, males utilize elaborate precoital displays instead of combat or forcible insemination and are usually smaller than females (Berry and Shine 1980). Also in aquatic species, larger females could be more aggressive, making forced insemination an unreliable strategy (Plummer 1977; Berry and Shine 1980). The results of our morphological analysis are consistent with the hypothesis for truly aquatic species in that males of S. bealei are smaller than females. In addition, females are more aggressive during intrasexual or intersexual competition while males have much brighter coloration on their neck and limbs in order to attract females and utilize precoital displays during mating season (L. Lin, pers. obs.). Head width is greater in female than in male S. bealei. Greater head size in female turtles may function to increase the size range of food items, perhaps in response to calcium depletion after oviposition (Bonnet et al. 2001; Trembath and Freier 2004).

According to the hypothesis of natural selection for fecundity, larger females have increased reproductive potential, either through greater allocation to individual offspring (i.e., larger eggs), greater numbers of offspring (i.e., more eggs), or the ability to reproduce more frequently (i.e., more clutches per year; Ernst et al. 1998; Zuffi et al. 1999; Djordjevic et al. 2011). Therefore, females in many turtle species have wider and higher shells than do males (Rowe 1997; Brophy 2006; Munoz and Nicolau 2006; Kaddour et al. 2008; Xiao et al. 2014). In S. bealei, females can reproduce only one time every year and lay 2.1 ± 0.8 eggs each time (n = 15; L. Lin, pers. obs.). Female S. bealei, compared with males, have higher shells and larger plastrons. Both of these characteristics could increase the intra-abdominal volume to hold larger or more eggs (egg length: 47.02 ± 3.96 mm, width: 23.09 ± 1.73 mm, n = 23; L. Lin, pers. obs.), which could increase the competitiveness and survival rate of offspring. Males are probably favored if they increase or maximize their searching efforts during courtship, copulation, and male–male combat (Travis 1994; Kaddour et al. 2008; Djordjevic et al. 2011). In the present study, the smaller plastron, shorter bridge, and longer ASJ of male S. bealei results in an increase in the size of openings in the shell. The size of the openings in the shell can limit the movements of the head, tail, and limbs (Bonnet et al. 2001); therefore, larger openings in the shells of males could thus enhance their mobility for moving and copulating with females (Kaddour et al. 2008). In turtles, the precloacal region of the tail accommodates the males' penis (Mosimann and Bider 1960); therefore, having a more posterior vent on the tail combined with greater space to move the tail could contribute to greater copulation success (Bonnet et al. 2001). Overall, the sexual shape dimorphism (SShD) of S. bealei could increase the fecundity of females and facilitate the mobility of searching and copulation for males, respectively.

Sexual dimorphism in size and shape of S. bealei is less noticeable than that of its coloration, especially the ocelli on head. Various morphological measurements and statistical analyses should be conducted to verify the sexual dimorphism of turtles (Lovich and Gibbons 1992; Smith 1999). Furthermore, a dramatic decrease of wild populations makes sample collection difficult for most Chinese turtles. Only 2 other turtle species, the four-eyed spotted turtle Sacalia quadriocellata and the Chinese strip-necked turtle Mauremys sinensis have been studied for their sexual dimorphism in China (Chen and Lue 1998; Xiao et al. 2014). Decline in the wild is the likely reason SSD in S. bealei has not been described previously. Nevertheless, the knowledge of SSD and SShD is important for a better understanding of the adaptive evolution and mating strategy of this species.