Sexual dimorphisms in body proportions of Masai giraffe

doi:10.21203/rs.3.rs-2985975/v1

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Sexual dimorphisms in body proportions of Masai giraffe

https://doi.org/10.21203/rs.3.rs-2985975/v1

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Giraffes exhibit a large sexual dimorphism in stature and body mass. Whether sexual dimorphisms also exist in relative body proportions of the axial and appendicular skeleton has been debated, particularly regarding the evolution of the giraffe’s iconic long neck. We measured and analyzed the relative anatomical proportions of the neck, legs, and body trunk of the Masai giraffe (G.c. tippelskirchi) in captive and wild populations. We found that female Masai giraffes have proportionally longer necks relative to their forelegs than males. Moreover, the female body trunk is proportionally longer whereas male foreleg length and neck width are proportionally greater. The sexual dimorphisms in body proportions were found in both captive and wild Masai giraffes suggesting that these differences are genetically determined. We speculate that the proportionally longer female neck is to compensate for females’ overall shorter stature to expand access to forage and their longer trunk is to accommodate fetal growth. Males’ longer forelegs, which contribute to the overall anterior body stature, likely provides some advantage in physical intrasexual competitions. Differences in the proportions of major body components define sex phenotypes, but several male and female giraffes display opposite-sex phenotypes with a significantly higher level of discordancy seen in captive males. We speculate that body proportion sexual dimorphisms are maintained in the wild by natural and/or sexual selection, but in captivity selection is relaxed because of human-altered mating and feeding behavior resulting in a higher proportion of sexual dimorphism discordances.

sexual dimorphism

body proportions

allometric growth

giraffe neck

axial skeleton

appendicular skeleton

Body size sexual dimorphism (SSD) exists in most mammalian groups with adult males generally larger than adult females (Reiss, 1989; Abouheif and Fairbairn, 1997; Weckerly, 1998). Evolutionary hypotheses for the development of SSD include natural selection based on the two sexes competing for resources or occupying different ecological niches (Slatkin, 1984) or SSD may be a non-adaptive byproduct of natural selection for larger size in both sexes (Leutenegger and Cheverud, 1982). SSD could also result from or be increased by sexual selection based on male-male competition for mates (Darwin, 1871; Clutton-Brock, 1989), male-female coercion (Clutton-Brock and Parker, 1995), or female choice (Eberhard, 1996). SSD might also be the result of some combination of the above natural and sexual selection processes. The degree of SSD differs among mammalian groups, and Darwin (Darwin, 1871) was the first to point out that polygyny was associated with the largest differences (Ralls, 1977; Weckerly, 1998; Cassini, 2020). Moreover, the magnitude of SSD in mammals is typically greater in species with high body mass, which is known as Rensch’s rule (Rensch, 1959; Abouheif and Fairbairn, 1997). For example, giraffes (Giraffa camelopardalis), a polygynous megaherbivore, exhibit extreme SSD with adult males 30–40% larger mass than adult females (Hall-Martin, 1977; Mitchell, 2021; Roylance-Casson, 2021).

Less common than comparisons of absolute size as in SSD, are body proportion sexual dimorphisms (BpSD), also known as body shape dimorphisms, that are due to allometric growth and developmental differences between sexes with different overall adult sizes (Badyaev, Hill and Whittingham, 2001). Examining BpSDs illuminates the different selective pressures acting on the 2 sexes in dimorphic species (Tarnawski, Cassini and Flores, 2014) such as when comparing the shapes of male and female skeletal components. The absolute neck length of giraffes is longer in adult males than adult females (Mitchell et al., 2013). Based on the observation that male giraffes frequently engage in neck fighting as a means to establish dominance, Simmons and Scheepers (Simmons and Scheepers, 1996a) proposed that longer necks gave males a competitive advantage. The different neck lengths and overall size of male and female giraffes reduce foraging competition between the sexes, and with other browsers as was proposed by Lamarck (Lamarck, 1809) and Darwin (Darwin, 1872) as the driver of the evolution of the giraffe’s long neck (Cameron and du Toit, 2007; Mitchell, Van Sittert and Skinner, 2009; Wilkinson and Ruxton, 2012; Mitchell, 2021). It is also possible that sexual selection involving neck fighting may have subsequently enhanced preexisting sexual dimorphisms in neck size and morphology. Mature adult males do indeed have longer necks than females, as every part of the adult male giraffe is much larger than the female. Our question is: Do male giraffes have proportionally longer necks than females when accounting for allometric differences between male and female skeletons? Moreover, do other aspects of the giraffe skeleton exhibit BpSDs? The answers to these questions will identify skeletal components likely undergoing selection and inform future work using genetic pedigrees to determine the mating system of giraffes and the sex-specific body morphology traits that have higher survival and/or reproduction.

Critically assessing body proportion sexual dimorphisms in giraffes requires the comparison of the core components of the appendicular and axial skeleton including the fore and hind legs and vertebral segments that contribute to the length of the neck and trunk. Given that the birthdates of wild giraffes are rarely known, previous studies by Simmons (Simmons and Scheepers, 1996b), Mitchell (Mitchell, Van Sittert and Skinner, 2009; van Sittert, Skinner and Mitchell, 2010; Mitchell, 2021) and others have used body mass and size as proxies for age. However, age is a confounding factor in assessing relative body proportions in giraffes because (a) their necks are known to grow at a more rapid rate than their legs during neonatal and juvenile development, (b) the body size sexual dimorphism, which is readily apparent in mature adults, develops over an unknown period of time, and (c) growth rates and terminal size are highly variable among individuals.

Using photographic images of known-age captive Masai giraffe (G.c. tippelskirchi) from North American zoos and safari parks, we calculated the relative body proportions of the neck and trunk, comprising the axial skeleton, and the forelegs and hindlegs, comprising the appendicular skeleton. Because the identity, pedigree, and birthdates of these animals were known, we were also able to quantify the postnatal developmental changes in body proportions over a wide span of ages. By utilizing photographs, we were able to obtain a much larger sample size than what was possible in previous studies that utilized postmortem samples. To determine if any observed sex differences in captive giraffe body proportions also existed in wild populations, we used the same methods to estimate body proportions from photographic images of adult wild Masai giraffes located in the Tarangire Ecosystem in Tanzania.

Photographic images. We obtained photographic images of captive Masai giraffes in North American zoos and safari parks (list of institutions in supplementary data) from three sources: images taken by the authors, images obtained from zoos and safari parks, and images from online public domains including Flicker (https://www.flickr.com) and Smugmug (https://www.smugmug.com). The American Zoo and Aquarium (AZA) association provided pedigree and vital statistical data of nearly 500 Masai giraffes that have existed in North American zoos and safari parks since the importation of the original founders from 1940–1982 (Cantwell, 2018). To reduce inbreeding, captive giraffe have been translocated among member AZA institutions under the guidance of the AZA and the Masai giraffe survival species plan (AZA, 2023). Although some of the participating AZA institutions have other giraffe subspecies, cross breeding of Masai with other subspecies is generally not done. Moreover, the pedigree of all captive Masai giraffe in this study is known with certainty and no subspecies hybrids were included in this study. The founders of the captive Masai giraffe in North American zoos and safari parks originated from southeastern Kenya and northeastern Tanzania(Cantwell, 2018) from populations that are located east of the steep escarpments of the Gregory Rift Valley. The wild Masai giraffe used in this study (described below) are located in the same general region east of the Gregory Rift Valley escarpments. Genetic distance measured by whole genome sequence analysis of nuclear and mitochondrial DNA sequence of several captive and wild giraffe indicate that they are closely related as compared to wild Masai giraffe west of Gregory Rift Valley escarpments in the Serengeti ecosystem (unpublished results). The identity of the captive giraffe in images obtained from online photo galleries is typically not indicated. To determine the identity of giraffes in such images, we searched online for named images often associated with news announcements of newborn calves. Because the spot pattern of Masai giraffes is individually distinctive and does not change in character over their lifespan(Foster, 1966) it is relatively easy to match newborn calf images with adult images. Finally, we conferred with zoo staff to verify the identity of several of the giraffes in our study. We have been unable to determine the identity of only one giraffe among the ~ 250 giraffe for which we have photographs. Images of wild Masai giraffes from the Tarangire Ecosystem were obtained by two of us (D.E.L. and M.L.B.) during triannual surveys conducted between 2011–2020 (Lee et al., 2016; Bond et al., 2021). For nearly all of the wild giraffes that were used in the current study, estimates of height (cm) were determined using photogrammetry (Lee et al., 2016). Wild males that were > 442 cm and wild females that were > 381cm and also with mature adult body characteristics were used in this study.

Measuring body proportions. We used the GNU Image Manipulation Program (GIMP) (https://www.gimp.org/) to measure the length of the neck, trunk, foreleg, and hindleg facing the camera in units of pixels (px). Our interest was in proportional body measurements and all proportion metrics are ratios of two lengths. We considered each image of a known-age giraffe with a known-date of creation as an independent sampling unit in our data, thus our image-specific calculations in pixel units accounted for variation in resolution among images.

To accurately quantify body dimensions from photographic images, the giraffe body must be perpendicular to the camera and the anatomical landmarks we used for length measurements need to be visible or able to be accurately estimated (See Figure S1 for measurement landmarks and definitions). Because of these stringent criteria, only a very small fraction (< 1%) of the thousands of images that we obtained could be used for measurement. Body measurements (in units px) in each image were performed by three individuals, and the mean measurements for each image were validated by the corresponding author for precision and repeatability.

Neck length was measured from the neck-chest indentation (Figure S1) to the occipital ridge near the junction of the C1 cervical vertebra and the skull. The neck length measurements for giraffes whose neck angle deviated substantially from 43^o, the normal resting position, were adjusted by moving the occipital ridge landmark to 43^o. We chose to use the neck-chest indentation, which is readily identifiable, as our primary landmark for neck and foreleg measurements. Foreleg length was measured as the number of pixels between the neck indentation and the bottom of the proximate foreleg hoof. Hindleg length was measured between the sacral pin and the bottom of the proximate hindleg hoof. In cases where the forelegs and hindlegs deviated substantially from perpendicular, the bottom of the hoof landmark was moved horizontally to a position that was nearly perpendicular. Neck width was measured between the neck-chest indentation to the withers neck-bending inflection point. The girth of the neck (neck thickness) was not measured in this study but is known to be proportionally greater in adult males, in part due to the lateral increase of muscle mass. By contrast, neck width is largely determined by the length of the scapula and dorsal spines of the anterior thoracic vertebrae (Mitchell, 2021).

Other giraffe studies which have compared relative neck to foreleg length using postmortem measurements (e.g., van Sittert, Skinner and Mitchell, 2010; Mitchell, 2021) used the distance between the withers peak to the occipital ridge as the estimate of neck length, and the distance between the withers peak to the bottom of the foreleg hoof as the estimate of foreleg length. We also estimated the relative neck and foreleg lengths by this alternative method.

We calculated sex-specific body proportions (defined in Fig. 1) of 179 captive Masai giraffes from North American zoo and safari parks and determined significance of mean differences according to sex using t-tests with alpha corrected for multiple tests using the Benjamini-Hochberg method (Benjamini and Hochberg, 1995). To determine if the sex-dependent body proportion differences observed in adult giraffes in zoos were present in a free ranging wild population, we calculated the body proportions of 98 mature adult Masai giraffes in the Tarangire ecosystem. The ages and dates of birth are unknown for these animals; therefore, we used conservative estimates of height and body characteristics to identify giraffes that were highly likely to be older than 8 years of age.

Data analysis. Relative body proportions of each image were calculated either as a ratio of two body measurements or calculated as a proportional fraction of potential vertical height (PVH) composed of the sum of the neck and foreleg lengths (Fig. 1). In addition, we summed the lengths of each of the components of the axial and appendicular skeleton as the total axial-appendicular length. The fractions of neck, trunk, foreleg, and hindleg of the total axial-appendicular length were calculated. The relative body proportions of the neck and trunk, comprising the axial skeleton, and the foreleg and hindleg, comprising the appendicular skeleton were estimated for males and females across ages from neonatal calves (0 year. old) through mature adults (16 year. old). We used GraphPad Prism 9.4.1 for macOS (www.graphpad.com) to generate plots of longitudinal body proportion data by age for the 179 individual captive giraffes from 357 images with 1–5 images per individual taken at different ages with curve fitting by non-linear regression. To correct for multiple regression tests the p values were alpha-corrected using the Bonferroni method (‘Etymologia: Bonferroni Correction’, 2015).

Because the axial:appendicular ratio is somewhat confounded by the large growth rate differences of the fore and hindlegs, we also compared growth of various skeletal components to the hindleg only, which shows the least variation between males and females. To ascertain when BpSD first becomes statistically significant, we examined the relative body proportions of the 0–0.1 year., 0.1–1 year., 1–3 year., 3–6 year., and 6–16 year. age classes. We used discriminant analysis of principal components (DAPC)(Jombart, Devillard and Balloux, 2010) to evaluate proportional neck, trunk, foreleg, and hindleg lengths to total axial-appendicular length; neck width to neck length ratio; and hindleg length to axial skeleton length (neck + trunk length) ratio for adult captive and wild Masai giraffes to define sex-specific morphology phenotypes. The two sexes, female and male, were used as the a priori groups. From the DAPC analysis the first discriminant function was plotted, and each individual’s sex membership probability was determined according to their morphology.

We found that the axial:appendicular ratio steadily increased in both sexes during the first 8 years indicating a faster growth rate of the axial skeleton (Tables 1 and 2, Fig. 2b). No significant sex differences were observed in the axial:appendicular ratio during the first year (Table 2 and Fig. 2b), but between 0.5–10 years a small difference in growth rates yielded a highly significant difference in the elevation of the growth curve (Table 1) and the axial:appendicular ratio (Tables 2 and 3). Within the axial skeleton, the neck grows at a somewhat faster rate than the trunk (Table 1), but no sexual dimorphisms were seen in either the relative growth rates or the neck to trunk ratio in mature adults (Tables 1 and 2). We observed larger growth rate differences in the appendicular skeleton with the foreleg growing at a faster pace than the hindleg (Fig. 2c and Table 1) in both sexes. Foreleg growth was particularly high in males (Fig. 2c and Table 1) which yielded a relatively large sexual dimorphism in foreleg: hindleg ratio in mature adults (Tables 2 and 3). The axial: hindleg, neck: hindleg, and trunk: hindleg ratios all exhibited positive allometric growth (Table 1), higher female growth rates, and yielded BpSD in mature adults (Tables 2 and 3) confirming the female-biased axial growth rates.

The potential vertical height (PVH) of giraffes is determined by the length of the forelegs, neck, and head. We found that neck length in adult females comprised a larger fraction of PVH than males (Table 2 Fig. 2a). The proportionally longer forelegs compared to hindlegs in adult males (Tables 2 and 3) partly contributes to this finding. However, adult female neck length is also proportionally longer than adult males when compared to the hindleg length (Table 2). We further measured the relative neck and foreleg lengths (wNeck/wForeleg) using the withers peak as the central landmark as is typically measured postmortem samples (Mitchell, 2021). We also found that adult females have proportionally longer necks than adult males using this method (Tables 2 and 3).

Body height in all other ungulates besides the giraffe is considered to be the height of the withers lying at the base of the neck above the shoulders (Thomas, 2005). We measured the withers height proportional to the rump (croup) height and found that adult male giraffes have proportionally greater withers height than adult females (Tables 2 and 3) consistent with the foreleg to hindleg BpSD which contribute to the largest fraction of withers and rump height, respectively.

We measured proximal neck width, the distance between the neck indentation and the withers peak, compared to neck length to determine if a BpSD exists for this trait. The neck width: length ratio was not significantly different between the sexes in newborn calves (Table 2), but proportional neck thickness grows at a much faster rate in males than females during the first 10 years of life (Table 1 and Fig. 1d) yielding a large difference BpSD in mature adults (Table 2). It should be noted that the neck width: length ratio is highest in newborn calves and then decreases as neck length rapidly grows (Table 2). The decrease in male neck width: length ratio ceases by the end of the second year but continues to decline in females until approximately the tenth year (Fig. 2d).

Regarding age of significant differences in BpSD, none of the BpSD seen in adult animals are statistically significant at birth or during the first year, but all of the adult BpSDs are statistically significant or near statistical significance in the 3–6 year age class (Table 2). For all BpSD, however, the effect differences and statistical significance are much higher in the 6–16 year age class.

Mean proportional neck lengths of wild adult Masai giraffe were nearly identical to captive Masai giraffe and showed a highly significant longer neck proportion in females than males (Table 1). Wild Masai giraffe also displayed the same pattern of sex-specific differences for the other traits including proportionally longer trunks, necks, and axial skeletons in females and proportionally longer forelegs and wider necks in males (Table 3).

The estimated mean lengths of the neck, trunk, and legs define adult female body phenotypes (FBP) and adult male body phenotypes (MBP) (e.g., Fig. 3a-b). However, some giraffes of both sexes, and particularly males, exhibited opposite-sex phenotypes (e.g., Fig. 3c-d). To quantify sex-specific phenotypes, we performed a discriminate analysis of principal components (DAPC) (Jombart, Devillard and Balloux, 2010) of neck, foreleg, hindleg, and trunk lengths as fractions of the total axial-appendicular length, neck width to neck length ratio, and and the axial to hindleg length ratio using female and male sex as the prior groups for both captive and wild giraffes. The initial principal component analysis (PCA) showed the expected closer correlation of the neck and trunk of the axial skeleton and the forelegs and hindlegs of the appendicular skeleton (Fig. S1). The DAPC analysis of the membership probability of each sex showed that the average probability of females for FBP was 93.1% and 92.9% for captive and wild giraffes, respectively, and the average probability of males for MBP was 79.1% and 92.1% for captive and wild giraffes, respectively (Fig. 4 and Table S2). Only one captive female (1.9%) and one wild female (2.5%) exhibited greater than 50% MBP phenotype membership, whereas four captive males (15%) and three wild males (5.2%) exhibited greater than 50% FBP phenotype membership. The relative differences in sex phenotypes between captive and wild giraffes were also readily seen in the linear discriminant analysis (Fig. S2), which showed a broader range and greater overlap in captive giraffes FBP and MBP phenotypes. Consistent with the DAPC analysis, the coefficient of variation (CV) of the major body components was higher in males than females. It is important to note that the fertility of captive giraffes exhibiting the most discordant body proportion phenotypes appeared to be normal. For example, only two captive males exhibited > 90% FBP membership probability, but they have both sired several offspring. However, these captive males had no competition for mating. By contrast, we do not know the relative mating success of wild males according to phenotype.

During postnatal development the various components of the core axial and appendicular skeleton generally show positive allometry with body size in giraffes (Mitchell 2021). The components of the axial and appendicular skeleton exhibit a high degree of morphological integration as determined by shared developmental origins and functional integration (Randau and Goswami, no date; Hanot et al., 2017; Arlegi, Veschambre-Couture and Gómez-Olivencia, 2020; Mallo, Buffetaut and Diaz, 2021). Within those constraints specific components can be modified for specialized functions such as the change in forelimb function of hominids from locomotion to grasping (Pouydebat et al., 2008; Stamos and Alemseged, 2023) and the extension of the neck in giraffes. However, the length of the neck, particularly compared to the forelegs, grows proportionally faster (Mitchell, 2021). These specialized adaptations of core skeletal components require compensatory changes in other skeletal components to maintain overall functional integration. For example, to maintain balance and locomotion the evolutionary extension of the giraffe’s neck required shortening the trunk and shifting the neck to be more posteriorly positioned above the forelegs. Giraffes’ lofty stature is not only contributed by their long neck but also by extending the legs and lengthening the scapula and thoracic dorsal spines compared to other artiodactyls. The morphological integration of these changes places considerable allometric constraints on individual variation. Nonetheless, we found significant sexual dimorphisms in core axial and appendicular skeletal components in Masai giraffes. Specifically, adult females have proportionally longer necks and trunks, whereas males have proportionally longer forelegs and wider necks. These BpSD are seen in captive and wild adult Masai giraffes and their magnitudes are virtually identical. This finding supports the hypothesis that the BpSDs are largely, if not entirely, genetically determined and justifies the use of captive giraffes to interrogate postnatal development of these traits.

At birth we found no differences in core body proportions between captive female and male calves. The growth rate of male calves is faster than females during the first year, but BpSDs do not become statistically significant until sometime after the third year when giraffes are beginning to reach sexual maturity. These BpSDs are therefore likely to be determined by hormonal differences between the sexes that arise during puberty in a similar manner for sexual dimorphisms in other species (Cox, Stenquist and Calsbeek, 2009).

We speculate that the adaptive function of the body proportion dimorphisms in Masai giraffes are twofold: (1) The extension of the axial skeleton in female giraffes serves to expand the browsing lateral range by lengthening the neck and to provide sufficient space for prenatal development by lengthening the body trunk. Observation of feeding behavior of female giraffes indicates that their long necks are advantageous in reaching deep into acacia thickets horizontally(Mitchell, 2021) rather than reaching at the tops of trees. Thus, female giraffes, through the proportional extension of the axial skeleton, have increased the horizontal dimension to effect higher reproductive capacity. (2) The proportional extension of the forelegs and increased withers height serves to enhance male mating competitiveness by increasing the vertical height of the anterior body trunk. As a result, the proximal base of the neck is elevated, and the forelegs are longer potentially providing increased leverage during body-pushing competitions. Additionally, the slope of the back increases which accentuates the appearance of size and dominance. The shortening of the body trunk in males compared to females also further enhances this appearance. These BpSDs combined with the large body size sexual dimorphism results in an overall imposing stature of a mature adult male.

Male giraffes establish a dominance hierarchy by dominance display behavior and through physical contact with each other. Male-male physical contact includes body-pushing (e.g., shoulder-shoulder engagement) and neck sparring behavior (Coe, 1967; Pratt and Anderson, 1985). Dominant males are usually but not always larger (Dagg and Foster, 1976; Pratt and Anderson, 1985), and we speculate that withers height is likely to be more advantageous than longer necks. Once dominance relationships have been established, male giraffes remember and recognize males of higher rank by sight (Pratt and Anderson, 1985). Most male-male interactions are low intensity involving behavioral displays, body pushing, and neck sparring behavior (Coe, 1967; Pratt and Anderson, 1985). High intensity neck-fighting is rare, and usually involves individuals that are unknown to each other (Pratt and Anderson, 1985). Whether females choose mates based upon size and appearance is unknown because copulation in the wild is rarely observed and paternity is never known.

We propose that the male-biased BpSD are evolutionarily tied to the large male-biased body size sexual dimorphism (SSD) seen in giraffes. Male biased SSD evolved primarily in ungulate species with comparatively large body size and that are polygynous, social, and occur in open habitats (McPherson and Chenoweth, 2012, Pérez-Barbería, et al, 2002, Polák and Frynta, 2009; Roylance-Casson, 2021; Cameron and du Toit, 2007). The presence of male-biased SSD in giraffes but not in Okapia johnstoni, the giraffe’s closest existing relative, is largely consistent with these trends. Giraffes are larger, more social, and occur in open habitats, whereas okapis are exclusively found in closed canopy forests (Stanton et al., 2014). Male biased SSD is argued to be the product of sexual selection particularly in polygynous species where all females will be reproductively successful but not all males will be (McPherson and Chenoweth, 2012). Female giraffes begin reproduction as early as the third year and may continue to produce offspring throughout their lives. By contrast male giraffes have a much shorter window for reproduction because males are not successful in mating until they become large enough to outcompete other males, and their lifespan is approximately 25% shorter than females in captivity and in the wild (Lacky and LaRue, 1997; Berry and Bercovitch, 2012; Bercovitch and Berry, 2017). The much shorter lifespan of male giraffes is almost certainly due to the considerable cost to their skeletal health of having 30–40% higher body mass (Hall-Martin, 1977; Mitchell, 2021; Roylance-Casson, 2021). The increase in body mass, with the largest fraction compressed on top of the forelegs, results in foreleg joint and hoof dysfunction as male giraffes reach 15 years of age. In addition to poorer skeletal health, adult males are less likely than females to survive severe droughts because they require proportionally more nutrition to survive (Mitchell, van Sittert and Skinner, 2010). Mitchell (Mitchell, 2021) has persuasively argued that giraffes, and particularly male giraffes, have pushed the limits of the skeletal system to withstand the gravitation force exerted by the mass of the anterior trunk, neck, and head stacked on top of their long, spindly forelegs. The elevation of the forelegs and wither height and trunk shortening in adult males as reported herein exacerbates this physical challenge by shifting additional body mass over the forelegs. Differential niche occupation has been proposed as a potential explanation for SSD in giraffes and other large herbivores (Ruckstuhl and Neuhaus, 2002). Male and female giraffes do tend to browse at different levels and may select different types of browse (Ginnett and Demment, 1999; Cameron and du Toit, 2007; Mramba et al., 2017). However, the substantial cost of male giraffe stature to longevity and resilience argues against this hypothesis as the primary selective pressure that resulted in SSD. We assert that dominance competitions and access to mating are the major drivers of sexual selection for male-biased SSD and BpSD. For male giraffes, having an elevated anterior body trunk and appearing to be bigger is believed to determine the degree of reproductive success (Pratt and Anderson, 1985), but has yet to be proved with genetic evidence of reproductive success differences among male phenotypes.

While we favor sexual selection as the explanation for the size and body proportion sexual dimorphisms in giraffes, the overwhelming evidence supports the hypothesis that the giraffe’s long neck and tall stature evolved through natural selection by foraging competition with other ungulate browsers (Cameron and du Toit, 2007; Wilkinson and Ruxton, 2012) and not by sexual selection. While the necks for sex hypothesis has been refuted (Mitchell, Van Sittert and Skinner, 2009; van Sittert, Skinner and Mitchell, 2010; Mitchell, 2021) and amended by authors (Simmons and Altwegg, 2010), it remains a more appealing explanation to the public and popular science (Luntz, 2022; Wang et al., 2022). The cornerstone of the necks for sex hypothesis is the prediction that male giraffes should have proportionally longer necks (Simmons and Scheepers, 1996). However, Mitchell and coworkers (Mitchell, Van Sittert and Skinner, 2009; Mitchell et al., 2013; Mitchell, 2021) have shown that for the South African giraffes (G.c. giraffa) females have proportionally longer necks than males. Our study on Masai giraffes (G.c. tippelskirchi) confirm their finding that adult females have proportionally longer necks than adult males. But in contrast to South African giraffes where males apparently have longer trunks (Mitchell et al., 2013; Mitchell, 2021), we found that body trunks are proportionally longer in female Masai giraffes than males. In addition, we found that mature adult male giraffes have proportionally longer forelegs, consistent with the findings for South African giraffes as well as and Angolan giraffes, G.c. angolensis (Silberbauer, Strydom and Hoffman, 2021). It is important to note that in addition to these body proportion sex differences, mature adult male giraffes have greatly thickened secondary ossicones, and the primary ossicones are enlarged and more extensively ossified (Pratt and Anderson, 1985) than in females. In addition, the male neck is thicker laterally due to increased muscle mass. While we observed some variation in these secondary sex characteristics in males, we did not observe any females that displayed these male-specific secondary sex characteristics.

Although our studies on Masai giraffes and previously published studies on South African giraffes refute the major claims and predictions of the necks for sex hypothesis for the evolution of the giraffe’s long neck, male neck fighting almost certainly has an important function, and this form of male combat requires an extraordinarily long neck. Evidence from the fossil record of ancestral species to giraffes indicate that long legs evolved first followed by elongation of the neck (Mitchell, 2021). Mitchell has proposed that long legs evolved to compete for browse at higher levels but were allometrically constrained to extend their legs further and then evolutionary pressures elongated the neck (Mitchell, 2021).

The mean body proportion sex differences define stereotypical male and female giraffe phenotypes: females with long necks and trunks and males with long forelegs and wide necks. However, we discovered some individuals of both sexes that displayed opposite-sex body proportion phenotypes in captive and wild giraffes. Captive males exhibited the largest fraction of discordant phenotypes. In the majority of these exceptional cases, a departure from expected sex phenotype was due to a difference in the axial to appendicular ratio, and not to just one part of the skeleton. Differential growth regulation of the giraffe’s axial and appendicular skeleton is suggested by the discovery and characterization of two wild giraffes that displayed disproportionate dwarfism characterized by shortened legs but normal neck and trunk (Brown and Wells, 2020). Under this model, downstream axial and appendicular specific growth factors would need to regulate the additional expansion of neck in females and forelegs in males. That captive male giraffes exhibit a much higher sex phenotype discordancy suggests that the underlying selective forces may be relaxed in captivity. We postulate that sexual selection is the most obvious candidate for maintaining these BpSDs in the wild, whereas males mating in captivity is entirely arranged. Individuals exhibiting opposite-sex body proportion phenotypes may be indicative of an underlying parental competition for growth control. Several growth control genes in humans and other mammals have been discovered to be genomically imprinted such that either the maternal or paternal allele is repressed (Bartolomei and Tilghman, 1997; Wu et al., 2004; Ishida and Moore, 2013). The balance in parental competition for growth control can also be impacted by nutrition through epigenetic mechanisms.

Acknowledgements

Rebecca Bourne, Penn State University; James Madeli and Emmanuel Kimaro, Wild Nature Institute; Petra Campbell; Andrea Putnam, AZA and San Diego Zoo Global; Sheri Horiszyny AZA and Oregon Zoo; Heather Robertson, Nashville Zoo; Zoli Gyimesi, Louisville Zoo; Terri Roth, Cincinnati Zoo; Noah Dunham, Cleveland Zoo; Adam Felts, Columbus Zoo; Chris McKinney and Louis DiVincenti, Seneca Park Zoo; Louis Perrotti, Roger Williams Park Zoo; Lauren Hinton, Brevard Zoo; Chris Hamlin, San Diego Zoo; Judi Barnes and Cressa Nursement, Santa Barbara Zoo; Michele Green and Vernon Presley, Fresno Chaffe Zoo; Melissa McCartney, Sacramento Zoo. Wild giraffe photographic data collection in Tanzania supported by the Living Desert Zoo and Gardens, Sacramento Zoo, Tierpark Berlin, Tulsa Zoo, Columbus Zoo, Zoo Miami, Cincinnati Zoo, Toronto Zoo, Roger Williams Park Zoo, and Save the Giraffes.

Author contributions

Douglas Cavener: Conceptualization; data curation; data analysis; methodology; writing – original draft and editing. Monica Bond: data curation (supporting); writing – review and editing; George Lohay: data curation (supporting); writing – review and editing; Lan Wu-Cavener: data curation (supporting); writing – review and editing; David Pearce: data analysis (supporting); writing – review and editing; Rebecca Bourne: data analysis (supporting); writing – review and editing; Xiaoyi Hou: data curation (supporting); writing – review and editing. Derek Lee: data curation (supporting); methodology (supporting); writing – review and editing.

Conflict of interests:

The authors declare no conflict of interest.

Data accessibility statement:

Data used in this manuscript are deposited in Dryad:

Cavener, Douglas, et al. (2022), Necks for sex or food: Giraffes stand to gain, Dryad, Dataset, https://doi.org/10.5061/dryad.hhmgqnkkw

Temporary link: https://datadryad.org/stash/share/QmeLnYllPqVdtuCU1bFIk53F6zgeWKqDNtLeK-ECXeg

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Sexual dimorphisms in body proportions of Masai giraffe

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