Comparisons of SSD in marine with non-marine aquatic turtles
Regression Approach .- Figure 2 illustrates separate regressions of male versus female body size for marine and NMAT with 95% confidence intervals and the 1:1 line (null hypothesis) for comparison. The regression for marine turtles using only the species-mean data (Fig. 2A) was: male CL = -2.4647 + 1.0014 (female CL) adj r2=0.99, p<0.0001). Neither the slope nor the intercept differed significantly from the null expectation (slope: t(4)=-0.001, tcrit=2.267, p=0.99; intercept: t(4)=-1.874, tcrit=2.267, p=1). The 95% confidence intervals of this regression overlap or encompasses the 1:1 line.
By contrast, NMAT exhibit a wide range of departures from equality in size, mostly in the direction of larger female size (Fig. 2A), which is reflected by a slope of 0.76. The 95% confidence intervals overlap the 1:1 line only in the domain of the very smallest species (<~15cm CL). The ANOVA (Table 1a) indicated an overall significant effect of female size on male size, but also a significant interaction between female size and habitat, indicating that this effect differed between marine and non-marine habitats. In other words, in conjunction with the results of the regressions, this means that females are on average larger than males in NMAT, but sexes do not differ in size in marine turtles.
SDILGF Approach .- Figure 2B illustrates SDILGF values for all 94 species of aquatic turtles (87 non-marine, seven marine). The values for marine turtles are very close to or overlapping the null expectation of no sexual size dimorphism (SDILGF = 0). The mean SDILGF for marine turtles was 0.027 ± 0.0103, and ranged from 0.002 to 0.067, whereas the mean SDILGF for NMAT was an order of magnitude higher and biased towards females (0.337 ± 0.0419, range -0.215 to 1.684). ANOVA (Table 1b) indicated that these distributions were significantly different (F1,92=4.339, p=0.04). Furthermore, the range of values was considerably larger in non-marine turtles (1.899) than in marine species (0.066).
DISCUSSION
Our comprehensive review of the literature permitted the first definitive statistical evaluation of the degree of SSD in marine turtles, reflecting information from all seven extant species. Our analysis revealed a striking lack of SSD (Fig. 1), a pattern that is notably distinct from NMAT, which typically exhibit female-biased SSD (Fig. 2). Female-biased SSD is typically interpreted as a response to fecundity selection, in the absence of male combat, which should result in larger male size via sexual selection (Berry & Shine, 1980). Marine turtles do not exhibit male combat and therefore would be expected to exhibit female-biased SSD, with all other conditions remaining the same. Whatever the sources of selection, differences between sexes in body size arise due to differences in growth rates over the same prematuration interval or due to differences in the prematuration duration of growth (Bernardo, 1993; Cox & John-Alder, 2007; J. Stamps & Krishnan, 1997; J. A. Stamps, 2008). A third possibility is differential, size-specific mortality that influences one sex more than the other(DeGregorio, Grosse, & Gibbons, 2012; Roosenburg, 1991). The lack of SSD in marine turtles thus requires an understanding of what kind of selection is prohibiting differentiation in size between sexes. We suggest that this is due to both the high energetic cost of locomotion in the marine environment coupled with frequent long-distance movements by both sexes.
It is well-established that the marine environment imposes strong selection on body form of large, widely-foraging vertebrates (Frank E Fish, 1993, 1998; Frank E. Fish, Howle, & Murray, 2008; Kelley & Pyenson, 2015; Seibel & Drazen, 2007; Webb, 1988; Webb & De Buffrénil, 1990; Williams Terrie, 1999), driven principally by selection for drag reduction and therefore cost-efficient swimming (Frank E Fish, 1993, 1998; Webb, 1988; Williams Terrie, 1999). Saltwater is denser and has both higher dynamic and kinematic viscosities than freshwater (Vogel, 1994). Consequently, we would expect from first principles that the marine environment establishes a different selective milieu on sexual dimorphism.
Marine turtles are morphologically distinctive among all aquatic turtles in several ways. First, marine turtle limbs reflect strong selection for specialised locomotion, both in form and in function. While all limbs are modified into flippers, the forelimbs are hypertrophied and modified into broad, distally tapered, rigid, wing-like flippers (Davenport, Munks, & Oxford, 1984; Renous, de Broin, Depecker, Davenport, & Bels, 2007; Wyneken, 1997). Apart from the external wing-like shape itself, the underlying bony architecture is distinct in marine turtles (Renous et al., 2007). In particular, the humerus is flattened compared to other turtles (Renous et al., 2007; Wyneken, 1997) and biomechanical analyses indicate that this confers great strength and hydrodynamic efficiency (Dickson & Pierce, 2019).The locomotory pattern of marine turtles consists of a synchronous upward/downward sweeping motion of the fore flippers that generates thrust (Davenport et al., 1984; Wyneken, 1997), similar to the pattern in other marine tetrapods that have flippers (Clark & Bemis, 1979; Walker, 2002). That such derived flippers have convergently evolved across multiple lineages of other marine tetrapods, including seals, penguins, and plesiosaurs (Wyneken, 1997), indicates strong selection for efficient long-distance swimming. It is well established from mathematical modelling that flapping appendages in large aquatic animals permit efficient and rapid propulsion (Blake, 1981; Walker, 2002; Walker & Westneat, 2000).
The second morphological specialisation of marine turtles is the extraordinary streamlining of their body form (Davenport et al., 1984; Wyneken, 1997). This stereotypic streamlining is evident throughout their evolutionary history including the oldest known definitive species, Desmatochelys padillai (Cadena & Parham, 2015), and across an order of magnitude range in body size from the smallest living species Lepidochelys kempii (~63 cm carapace length) to the largest known species, the extinctArchelon ischyros (Wieland, 1896), which exceeded 400 cm in carapace length. A further adaptation evident in D. coriacea are the longitudinal dorsal ridges on the carapace that enhance hydrodynamic performance (Bang, Kim, Lee, & Choi, 2016).
Taken together, these specialisations indicate that selection has optimised marine turtle morphology for energetically efficient swimming. Indeed, a key feature of marine turtle biology is their capacity to exploit resources across vast geographic expanses. Both sexes of all seven species of marine turtles undertake long-distance, sometimes trans-oceanic migrations covering many hundreds to thousands of kilometers (Boyle et al., 2009; Graeme C Hays, Houghton, & Myers, 2004; Graeme C. Hays, Mortimer, Ierodiaconou, & Esteban, 2014; Graeme C. Hays & Scott, 2013; Luschi, Hays, & Papi, 2003; Plotkin, 2003, 2010; Shillinger et al., 2008). Two species (D. coriacea and L. olivacea ) are oceanic, pelagic, widely-foraging predators (Graeme C Hays et al., 2004; Plotkin, 2010; Shillinger et al., 2008). Satellite tagging studies show that D. coriacea achieves a mean speed of 33-49 km/d, with a maximum of 62 km/d (Shillinger et al., 2008) andL. olivacea a mean of 28.32 km/d and a maximum of 79.4 km/d (Plotkin, 2010).
Despite their having evolved unique morphology among turtles for efficient swimming, this high vagility lifestyle still entails substantial energetic expenditure. Unfortunately, few quantitative data on the energetic requirements of swimming in adult marine turtles are available. However, Prange (1976) studied the metabolic cost of swimming in juvenile Chelonia mydas . By extrapolating these costs, he estimated that the energetic demand for a long-distance migration of adults between breeding and feeding grounds would require approximately 21% of their body mass in fat stores. Given the common body form and long-distance movement of all marine turtle species, it is not far-fetched that these energy requirements are incurred by all of the species.
Because the high energetic costs of sustained swimming are incurred by both sexes, neither sex can allocate significant energy to continued growth after maturation and therefore neither sex can achieve a larger size than the other (Bernardo, 1993; Cox & John-Alder, 2007; J. Stamps & Krishnan, 1997; J. A. Stamps, 2008). For instance, female-biased SSD is usually attributed to fecundity selection, but the ability for female marine turtles to allocate energy to enhanced post-maturation growth in response to fecundity selection appears to be prohibited by their costly locomotion. An analysis of growth rates in different populations of loggerhead turtles instantiates that the cost of achieving larger size comes at the expense of reproductive frequency (Hatase & Tsukamoto, 2008). Thus, the capacity to continue to grow and produce eggs come into close conflict because of the energetic background costs of locomotion (Hatase & Tsukamoto, 2008). A further indication that marine turtles lack discretionary energy for continued growth that could produce SSD is found in their unusual post-maturation growth patterns. Marine turtles exhibit determinate-like growth (Omeyer, Fuller, Godley, Snape, & Broderick, 2018), a pattern which is unlike other turtles (Congdon, Gibbons, Brooks, Rollinson, & Tsaliagos, 2013; Gibbons, Semlitsch, Greene, & Schubauer, 1981; Lindeman, 1999) and in fact unlike most other ectotherms (Bernardo, 1993; Gotthard, 2001; Sebens, 1987; Tilley, 1980) which exhibit indeterminate growth.
In conclusion, our study demonstrated that, unlike NMAT, marine turtles are not sexually size dimorphic, and we argued that this difference is due to the distinct selective milieu imposed by the oceanic environment. Hence, future studies should acknowledge this distinction and no longer group marine turtles with NMAT as numerous studies have previously done. We also note that, where data are available for multiple populations of the same species (Figure 1A), the magnitude and direction of SSD vary. This indicates that the common practise of basing a species-level trait estimate on a single population likely introduces error variance in comparative datasets. Further, we note that in our comprehensive dataset, the sample size for females was more than 20 times that for males, and in the case of N. depressus , only a single male has been measured. This unbalanced sample size between sexes is likely due to the oversampling of nesting fmales; future studies need to be deliberate about acquiring male data on marine turtle males.
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Table 1. Analyses of Variance (ANOVAs) modelling the degree of difference in body size between males and females in non-marine versus marine turtles. (a) Analysis of mean body size between males and females (b) Analysis of SDILGFvalues.