Background
Sexual size dimorphism (SSD) is a phenomenon that has received a great deal of theoretical and empirical attention, as it is thought to reflect variation in sex-specific selection due to ecological performance, and fitness effects arising from fecundity selection and mating systems (D J Fairbairn, 1997; Daphne J Fairbairn, Blanckenhorn, & Székely, 2007; Shine, 1989, 1990). Turtles (Order Testudines) have been prominent model systems for comparative analyses aimed at understanding the causes of SSD, owing to the diversity of their mating systems, habitats (freshwater, terrestrial, marine) they occupy, and the wide availability of data on body size of many species (Agha et al., 2018; Berry & Shine, 1980; Ceballos, Adams, Iverson, & Valenzuela, 2013; Gibbons & Lovich, 1990; Gosnell, Rivera, & Blob, 2009; Halámková, Schulte, & Langen, 2013; Regis & Meik, 2017). All of these analyses assign turtle species to different habitat types (aquatic, semi-aquatic, terrestrial, etc.), but with varying degrees of detail. In all cases, marine turtles, the subject of this paper, are lumped with non-marine aquatic turtles (NMAT).
The seven species of marine turtles comprise a monophyletic lineage (superfamily Chelonioidea) containing two families (Cheloniidae, Dermochelyidae) (reviewed in Figgener, Bernardo, and Plotkin (2019)). Both extant and extinct marine turtles are well-known to exhibit striking adaptations to the marine environment including forelimbs highly modified into flippers with concomitant neuromuscular repatterning, and streamlining of body form as is seen in other highly vagile marine vertebrates (Frank E Fish, 1993; Kelley & Pyenson, 2015; Pyenson, Kelley, & Parham, 2014). Three issues pertaining to the marine turtle data that have been used in prior analyses of testudine SSD prompted this study. The first issue is that most reviews do not include data for all seven species, (two to five species have been included) although data exist for all seven species in the literature. Second, most studies include species’ mean values that are often based on a single population ignoring a large amount of literature data on body sizes in different populations. Further, some studies report values whose origin in the primary literature is unclear (Supplementary Table 1). Because most marine turtles occupy far more expansive geographic ranges (Figgener et al., 2019) than any other turtle species including both temperate and tropical regions, intraspecific diversity in body size may influence overall conclusions about SSD in marine turtles. The third and possibly most concerning issue is that all the prior analyses cited above are consistent in grouping marine turtles with other aquatic turtles despite their well-known distinct morphology and ecology, which includes long-distance, often trans-oceanic migrations (Godley et al., 2008; Graeme C. Hays & Hawkes, 2018; Plotkin, 2003, 2010).
In this paper, we critically examine these issues. First, we address the lack of SSD data for marine turtles in previous studies by assembling the most comprehensive dataset to date on body size of all seven marine turtle species, including estimates from multiple populations. We then analysed these data to describe quantitatively intraspecific and interspecific patterns in marine turtle SSD. Finally, we compared these new estimates of marine turtle SSD to data from other fully aquatic turtles to test the hypothesis that the previous grouping of marine turtles with other aquatic turtles in comparative analyses of sexual size dimorphism is justified.
Methods
We carefully reviewed all data on marine turtle body size reported and used in prior analyses of testudine SSD to validate their accuracy and to gauge any omissions. As part of this process, we re-examined all the primary sources reported in these studies. This exercise revealed many omissions and errors (summarised in Supplementary Table 1). Therefore, we generated a novel, comprehensive dataset (Supplementary Table 2) of sex-specific body sizes (carapace length, CL) of adult marine turtles in which data for both sexes were reported from the same population using data from primary sources. The detailed methodology and the resultant dataset for this synthesis are detailed in the Electronic Supplementary Material.
We analysed this new dataset to test the hypothesis that marine turtles exhibit significant sexual size dimorphism. First, to gain an overview of species differences as well as intraspecific variation, we computed sex-specific mean values for each population and species. Then we plotted male vs female size for each population and computed a regression of males versus females (Ranta, Laurila, & Elmberg, 1994). The null hypothesis, in this case, is that males and females for a given species do not differ in size, which implies a slope of one and an intercept of zero. This null hypothesis thus differs from the standard null in regressions that both the slope and intercept are zero. Because the data were unbalanced with respect to the number of populations per species (Fig. 1A), we repeated the analysis using only mean values for each species. In both models, each component of the null hypothesis (slope, intercept) was evaluated using a one sample, two-tailed t-test.