Evidence for the Morphological Constraint Hypothesis and Optimal Offspring Size Theory in the Mexican Mud Turtle (Kinosternon integrum) Author(s): Rodrigo Macip-Ríos, Pablo Brauer-Robleda, Gustavo Casas-Andreu, María de Lourdes Arias-Cisneros and Víctor Hugo Sustaita-Rodríguez Source: Zoological Science, 29(1):60-65. 2012. Published By: Zoological Society of Japan DOI: http://dx.doi.org/10.2108/zsj.29.60 URL: http://www.bioone.org/doi/full/10.2108/zsj.29.60 BioOne (www.bioone.org) is a nonprofit, online aggregation of core research in the biological, ecological, and environmental sciences. BioOne provides a sustainable online platform for over 170 journals and books published by nonprofit societies, associations, museums, institutions, and presses. Your use of this PDF, the BioOne Web site, and all posted and associated content indicates your acceptance of BioOne’s Terms of Use, available at www.bioone.org/page/terms_of_use. 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ZOOLOGICAL SCIENCE 29: 60–65 (2012) ¤ 2012 Zoological Society of Japan Evidence for the Morphological Constraint Hypothesis and Optimal Offspring Size Theory in the Mexican Mud Turtle (Kinosternon integrum) Rodrigo Macip-Ríos1*, Pablo Brauer-Robleda2, Gustavo Casas-Andreu3, María de Lourdes Arias-Cisneros4, and Víctor Hugo Sustaita-Rodríguez3 1Instituto de Ciencias de Gobierno y Desarrollo Estratégico, Benemérita Universidad Autonoma de Puebla. 4 Sur 104, Edificio Carolino, Tercer Patio, Centro Histórico CP 72000, México 2Dirección de Delegaciones y Subdelegaciones, Secretaria del Medio Ambiente y Recursos Naturales. Carretera Picacho-Ajusco S/N. Tlapan, Ciudad de México CP 14210, México 3Departamento de Zoología, Instituto de Biología, Universidad Nacional Autónoma de México. Circuito Exterior S/N, Ciudad Universitaria, Coyoacán, México, Ciudad de México CP 04510, México 4Departamento de Pequeñas Especies, Facultad de Medicina Veterinaria y Zootécnia, Universidad Nacional Autónoma de México. Circuito Exterior, S/N, Ciudad Universitaria, Coyoacán, Ciudad de México CP 04510, México Optimal offspring size theory states that natural selection should balance reproductive output by optimizing between offspring size and offspring number. If a species has evolved an optimal off- spring size, the fitness of larger females should be increased by simply producing more offspring of an optimum size. In contrast, when offspring size is not optimized, the morphological constraint hypothesis may apply, and in this case, maternal fitness is increased by producing the greatest number of the largest offspring that mothers are physically capable of producing. We used a log- log allometric regression approach on clutch size, egg size, and body size data to test the appli- cation of optimal offspring size theory and the morphological constraint hypothesis in the Mexican mud turtle (Kinosternon integrum) in southern Mexico. Our results indicate that this turtle seems to follow the morphological constraint hypothesis when all data are analyzed together, but when data are divided between small (< 140 mm plastron length) and large females (> 140 mm plastron length), optimal offspring (egg) size theory was supported only in large females, while the morpho- logical constraint hypothesis was supported in small females. Our results thus indicate that K. integrum females may increase their fitness in two different, size-dependent ways as they grow from size at sexual maturity to maximum body size. Key words: optimal offspring size theory, morphological constraints, hypoallometry, clutch size-body size correlation 1998; Roff, 2002; Gluckman et al., 2007). INTRODUCTION Optimal offspring size theory states that natural selec- An organism’s energy that is available to reproduction is tion should balance the reproductive output between devoted to many different compartments. A fraction of an offspring size and offspring number in order to maximize fit- organism’s energy is invested in courtship, mating, and ness (Smith and Fretwell, 1974; Congdon and Gibbons, nesting behavior (Williams, 2005); meanwhile, other frac- 1987). If a species has evolved an optimum offspring size, tions are invested in carrying, transport, physiology, and larger females may increase their fitness by simply produc- developmental expenses of offspring during gestation ing more offspring (i.e. eggs) of an optimum size (Ryan and (Rollison and Brooks, 2007); another fraction is invested in Lindeman, 2007). On the other hand, the morphological con- the size and number of offspring (Stearns, 1977, 1992; Roff, straint hypothesis suggests that anatomical or physiological 2002). Females should optimize their offspring fitness in factors, such as the mother’s pelvic aperture (Tucker et al., order to match egg size and number to the prevailing envi- 1978; Congdon and Gibbons, 1987; Wilkinson et al., 2005), ronmental conditions and selection pressures (Stearns, caudal gap (Clark et al., 2001), or endocrine-regulated egg 1992; McNamara and Houston, 1996; Mousseau and Fox, size (Bowden et al., 2004), may constrain the balance between offspring size and offspring number. In this case, * Corresponding author. Tel. : +52(55)-56-22-82-22, Ext. 47859; small mothers produce smaller eggs than expected by their Fax : +52(55)-55-50-01-64; body size, and to increase their fitness, they should produce E-mail: [email protected] the greatest number of the largest eggs that they are physi- doi:10.2108/zsj.29.60 cally capable of laying (Ryan and Lindeman, 2007). Evidence Morphological Constraint Hypothesis 61 for optimal offspring size comes from a large number of non- metric relationships of egg size, clutch size, and maternal avian reptilian species (Blueweiss et al., 1978; Congdon and body size to test for support of optimal offspring size theory, Gibbons, 1987; Rohr, 1997; Radder and Shanbhag, 2004), or the morphological constraint hypothesis in Kinosternon whereas evidence for the morphological constraint hypothe- integrum in southern Mexico. We expected to find 1) no cor- sis has been documented in long-lived reptiles (Ballinger, relation between egg size and maternal body size, and a 1983; Bronikowski and Arnold, 1999; Congdon and Gibbons, log-log isometric correlation for clutch size to maternal body 1985, 1987; Wilbur and Morin, 1988; Vogt, 1990; Clark et size if egg size is optimized, or 2) a hypoallometric correla- al., 2001; Wilkinson et al., 2005; Ryan and Lindeman, 2007; tion to egg size and clutch size on maternal body size if egg Platt et al., 2008; Casas-Andreu et al., 2011). size is constrained by female morphology. We also expected As Ryan and Lindeman (2007) have pointed out, the that 3) if egg size is optimized, it will show little, or no variation only logical way to test if turtle populations follow the optimal across the range of body size; but, 4) if egg size is con- offspring size or the morphological constraint hypothesis is strained, this constraint should cease when turtles attain by using King’s (2000) methodology. Optimal offspring (egg) larger sizes, when optimum egg size could be reached. size would be supported if clutch size is directly related to body size in an isometric function, and egg size shows no cor- relation with body size; whereas the morphological constraint hypothesis would be supported if clutch size and egg size are both related to female body size in a hypoallometric function. Ryan and Lindeman (2007) demonstrated support for the mor- phological constraint hypothesis in a population of Graptemys geographica, and also noted this pattern in the emydid turtles G. versa, Chrysemys picta, and Trachemys scripta. Evidence (using non-allometric approaches) from kinos- ternids indicates morphological constraint on egg size in some species, due to the small size of the pelvic opening or the caudal gap (Congdon and Gibbons, 1985; Iverson, 1991, 2002; Clark et al., 2001; Wilkinson et al., 2005). How- ever, evidence from other kinosternids indicates that egg size is not constrained by the pelvis (van Loben-Sels et al., 1997; Wilkinson et al., 2005; Macip-Ríos et al., 2009). To our knowledge no study has tested optimal egg size theory or the morphological constraint hypothesis in kinosternid tur- Fig. 1. Study area and the localities where Kinosternon integrum tles using King’s (2000) allometric approach. were captured along the Balsas River Basin and adjacent basins in The purpose of the present study was to analyze the allo- southern Mexico. Table 1. Reproductive characteristics of the six populations of Kinosternon integrum surveyed across the Balsas River Basin. PL = Plastron length, CS = Clutch size, CM = Clutch mass, MeanEL = Mean egg length, MeanEW = Mean egg width, EM = Mean egg mass, MaxEL = Max- imum egg length, MaxEW = Maximum egg width, MaxEM = Maximum egg mass. Tonatico 1 = data collected from October 2003 to November 2004, Tonatico 2 = data collected from June 2007 to October 2008. Mean, SD in parenthesis, and range. MeanEL MeanEW MaxEL MaxEW MaxEM Population n PL (mm) Body Mass (g) CS CM (g) EM (g) (mm) (mm) (mm) (mm) (g) Nanchititla 2 132.5 397.6 4.0 23.1 31.7 17.3