Patterns of fluctuating asymmetry in the limbs of freshwater turtles: Are more functionally important limbs more symmetrical?

Abstract

Understanding how selective forces influence patterns of symmetry remains an active area of research in evolutionary biology. One hypothesis, which has received relatively little attention, suggests that the functional importance of morphological characters may influence patterns of symmetry. Specifically, it posits that for structures that display bilateral symmetry, those with greater functional importance should display lower levels of asymmetry. The aim of this study was to examine the patterns of fluctuating asymmetry (FA) present in the limb bones of freshwater turtles in the family Emydidae. Aquatic emydid turtles of the subfamily Deirochelyinae employ a hindlimb‐dominant swimming style, suggesting that hindlimbs should display lower levels of FA. Consistent with the morpho‐functional hypothesis of symmetry, we found a strong, clade‐wise pattern of humeral‐biased FA in aquatic Deirochelyinae. In contrast, some emydids of the subfamily Emydinae possess more terrestrial tendencies. As terrestrial locomotion places more equal importance on fore‐ and hindlimbs, we predicted that such behaviors may minimize differences in FA. No clade‐wise pattern was detected in the subfamily Emydinae. We also detected a phylogenetic signal in FA within the femur and discovered that FA has evolved at vastly different rates between the fore‐ and hindlimbs.

Prenatal Developmental Trajectories of Fluctuating Asymmetry in Bat Humeri

“…Asymmetry across multiple traits has shown decoupled patterns, reflecting functional differences and indicating independent developmental mechanisms controlling phenotypic symmetry across different structures of the body of bats ( Gummer and Brigham, 1995 ; Robaina et al, 2017 ), turtles ( Rivera and Neely, 2020 ), and birds ( Aparicio and Bonal, 2002 ). Our results of decoupled patterns of longitudinal and cross-sectional humeral FA point toward independent trajectories of bone elongation (endochondral ossification) and thickening (intramembranous ossification) while also suggesting that it could be applicable within single structures.…”

“…The presence of FA and DA in longitudinal and cross-sectional asymmetry was statistically tested with full-factorial ANOVAs using side (left or right), individual, and duplicate as factors (FA ∼ side + individual + side/individual; see Table 2 ; Monteiro et al, 2019 ; Rivera and Neely, 2020 ). The side factor provides a statistical test for DA, whereas the side–individual interaction provides statistical tests for FA.…”

Fluctuating Asymmetry in the Polymorphic Sand Cricket (Gryllus firmus): Are More Functionally Important Structures Always More Symmetric?

“…This dimensionless index of proportional difference, hereafter referred to as ‘individual measurement’, is the most common transformation used to correct for variation in trait size. To ensure that this transformation did in fact remove the size-dependence of FA data without inducing additional patterns, we conducted regression analyses for unscaled and scaled side-difference magnitudes against the average structure size [ 17 , 26 ].…”

“…To do this, it was important to maintain a high level of variability in our data, but also to set an upper threshold for extreme differences that might be indicative of developmental abnormalities. As such, for each of the 32 datasets (two sexes × two morphs × eight structures), we excluded individual measurements more than three times greater than the interquartile range below or above the first and third quartile, respectively (<Q 1 − 3.0 × IQR or >Q 3 + 3.0 × IQR; see Rivera and Neely [ 26 ]). Once outliers were removed, we tested for differences in size for each measured structure (i.e., the average of the left and right sides), using a two-way ANOVA (sex × morph).…”

“…In both anurans (Bufonidae and Ranidae: [ 17 ]) and turtles (Emydidae: [ 26 ]), hindlimbs play a greater role in locomotion (e.g., greater force production) than forelimbs; concordantly, they exhibit lower levels of FA. In addition to finding that more functionally important structures (i.e., hindlimbs) display lower levels of FA, Rivera and Neely [ 26 ] also showed that low levels of FA have been canalized in the hindlimbs, in contrast to patterns in the forelimbs, where rates of evolutionary change are approximately sixfold greater. Importantly, asymmetry of bilateral structures not only affects trait functionality, but can strongly be related to fitness.…”