Out on a limb: bandicoot limb co‐variation suggests complex impacts of development and adaptation on marsupial forelimb evolution

Garland, Kathleen; Marcy, Ariel E.; Sherratt, Emma; Weisbecker, Vera

doi:10.1111/ede.12220

Cited by 21 publications

(21 citation statements)

References 75 publications

(166 reference statements)

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“…This contrasts with predictions of individual shapes falling along a spectrum of change along a high-eigenvalue PC1, as expected under a scenario of constraint. Rather, it concurs with our expectation that within-species morphospaces can contain too much "noisy" variation to infer a constraint or interpret in a context of macroevolutionary patterns [6,13,27,38]. While individual variability in our sample is high, shape variation within species tends to occur most frequently in areas of high masticatory stress, which also seems to cause the uniform within-species PC1 landmark displacement patterns.…”

Section: Discussionsupporting

confidence: 86%

“…Our results point towards a mostly biomechanically caused, mastication-related driver of wombat skull shape variation, suggesting that important mechanisms of shape macroevolution, such as a possible constraint on marsupial skull shape, may only emerge above the species level in some mammals [6,13,27,38]. This posits an important challenge in testing hypotheses of constraints, and identifying differences between heritable and epigenetic variation, within mammalian skulls [13]; this is already being acknowledged, for example in studies that account for population-level shape "noise" in tree dating [57].…”

Section: Discussionmentioning

confidence: 69%

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Individual variation of the masticatory system dominates 3D skull shape in the herbivory-adapted marsupial wombats

et al. 2019

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Background: Within-species skull shape variation of marsupial mammals is widely considered low and strongly size-dependent (allometric), possibly due to developmental constraints arising from the altricial birth of marsupials. However, species whose skulls are impacted by strong muscular stressesparticularly those produced through mastication of tough food itemsmay not display such intrinsic patterns very clearly because of the known plastic response of bone to muscle activity of the individual. In such cases, allometry may not dominate within-species shape variation, even if it is a driver of evolutionary shape divergence; ordination of shape in a geometric morphometric context through principal component analysis (PCA) should reveal main variation in areas under masticatory stress (incisor region/zygomatic arches/mandibular ramus); but this main variation should emerge from high individual variability and thus have low eigenvalues. Results: We assessed the evidence for high individual variation through 3D geometric morphometric shape analysis of crania and mandibles of three species of grazing-specialized wombats, whose diet of tough grasses puts considerable strain on their masticatory system. As expected, we found little allometry and low Principal Component 1 (PC1) eigenvalues within crania and mandibles of all three species. Also as expected, the main variation was in the muzzle, zygomatic arches, and masticatory muscle attachments of the mandibular ramus. We then implemented a new test to ask if the landmark variation reflected on PC1 was reflected in individuals with opposite PC1 scores and with opposite shapes in Procrustes space. This showed that correspondence between individual and ordinated shape variation was limited, indicating high levels of individual variability in the masticatory apparatus. Discussion: Our results are inconsistent with hypotheses that skull shape variation within marsupial species reflects a constraint pattern. Rather, they support suggestions that individual plasticity can be an important determinant of within-species shape variation in marsupials (and possibly other mammals) with high masticatory stresses, making it difficult to understand the degree to which intrinsic constraints act on shape variation at the within-species level. We conclude that studies that link micro-and macroevolutionary patterns of shape variation might benefit from a focus on species with low-impact mastication, such as carnivorous or frugivorous species.

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Section: Discussionsupporting

confidence: 86%

Section: Discussionmentioning

confidence: 69%

Individual variation of the masticatory system dominates 3D skull shape in the herbivory-adapted marsupial wombats

et al. 2019

Self Cite

View full text Add to dashboard Cite

show abstract

Section: Discussionsupporting

confidence: 85%

“…Our results point towards a mostly biomechanically caused, mastication-related drive of wombat skull shape variation, suggesting that important drivers of shape macroevolution, such as a possible constraint on marsupial skull shape, may only emerge above the species level in some mammals [6,13,27,48]. This posits an important challenge in testing hypotheses of constraints, and identifying differences between heritable and epigenetic variation, within mammalian skulls [13]; this is already being acknowledged, for example in studies that account for population-level shape "noise" in tree dating [65].…”

Section: Discussionmentioning

confidence: 69%

Individual variation of the masticatory system dominates 3D skull shape in the herbivory-adapted marsupial wombats

Weisbecker

Guillerme

Speck

et al. 2019

Preprint

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Background: Within-species skull shape variation of marsupial mammals is widely considered low and strongly size-dependent (allometric), possibly due to developmental constraints arising from the altricial birth of marsupials. However, species whose skulls are impacted by strong muscular stresses -particularly those produced through mastication of tough food items -may not display such intrinsic patterns very clearly because of the known plastic response of bone to muscle activity of the individual. In such cases, shape variation should not be dominated by allometry; ordination of shape in a geometric morphometric context through principal component analysis (PCA) should reveal main variation in areas under masticatory stress (incisor region/zygomatic arches/mandibular ramus); but this main variation should emerge from high individual variability and thus have low eigenvalues. Results:We assessed the evidence for high individual variation through 3D geometric morphometric shape analysis of crania and mandibles of thre species of grazing-specialized wombats, whose diet of tough grasses puts considerable strain on their masticatory system. As expected, we found little allometry and low Principal Component 1 (PC1) eigenvalues within crania and mandibles of all three species. Also as expected, the main variation was in the muzzle, zygomatic arches, and masticatory muscle attachments of the mandibular ramus. We then implemented a new test to ask if the landmark variation reflected on PC1 was reflected in individuals with opposite PC1 scores and with opposite shapes in Procrustes space. This showed that correspondence between individual and ordinated shape variation was limited, indicating high levels of individual variability in the masticatory apparatus. Discussion:Our results are inconsistent with hypotheses that skull shape variation within marsupial species reflects a constraint pattern. Rather, they support suggestions that individual plasticity can be an important determinant of within-species shape variation in marsupials (and possibly other mammals) with high masticatory stresses, making it difficult to understand the degree to which intrinsic constraint act on shape variation at the within-species level. We conclude that studies that link micro-and macroevolutionary patterns of shape variation might benefit from a focus on species with low-impact mastication, such as carnivorous or frugivorous species.3

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“…When viewed across a phylogeny, this pattern is known as evolutionary morphological integration [ 38 ]. Integration is expected to decrease when each trait is under different, possibly antagonistic, selection pressures [ 39 ], such as in the evolutionary decoupling of mammalian fore- and hind-limbs as a result of life history changes [ 40 ] or different locomotory behaviour [ 41 ]. These examples also demonstrate how an animal’s ecology influences evolutionary morphological integration.…”

Section: Introductionmentioning

confidence: 99%

Rates of morphological evolution, asymmetry and morphological integration of shell shape in scallops

2017

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BackgroundRates of morphological evolution vary across different taxonomic groups, and this has been proposed as one of the main drivers for the great diversity of organisms on Earth. Of the extrinsic factors pertaining to this variation, ecological hypotheses feature prominently in observed differences in phenotypic evolutionary rates across lineages. But complex organisms are inherently modular, comprising distinct body parts that can be differentially affected by external selective pressures. Thus, the evolution of trait covariation and integration in modular systems may also play a prominent role in shaping patterns of phenotypic diversity. Here we investigate the role ecological diversity plays in morphological integration, and the tempo of shell shape evolution and of directional asymmetry in bivalved scallops.ResultsOverall, the shape of both valves and the magnitude of asymmetry of the whole shell (difference in shape between valves) are traits that are evolving fast in ecomorphs under strong selective pressures (gliders, recessers and nestling), compared to low rates observed in other ecomorphs (byssal-attaching, free-living and cementing). Given that different parts of an organism can be under different selective pressures from the environment, we also examined the degree of evolutionary integration between the valves as it relates to ecological shifts. We find that evolutionary morphological integration is consistent and surprisingly high across species, indicating that while the left and right valves of a scallop shell are diversifying in accordance with ecomorphology, they are doing so in a concerted fashion.ConclusionsOur study on scallops adds another strong piece of evidence that ecological shifts play an important role in the tempo and mode of morphological evolution. Strong selective pressures from the environment, inferred from the repeated evolution of distinct ecomorphs, have influenced the rate of morphological evolution in valve shape and the magnitude of asymmetry between valves. Our observation that morphological integration of the valves making up the shell is consistently strong suggests tight developmental pathways are responsible for the concerted evolution of these structures while environmental pressures are driving whole shell shape. Finally, our study shows that directional asymmetry in shell shape among species is an important aspect of scallop macroevolution.Electronic supplementary materialThe online version of this article (10.1186/s12862-017-1098-5) contains supplementary material, which is available to authorized users.

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Out on a limb: bandicoot limb co‐variation suggests complex impacts of development and adaptation on marsupial forelimb evolution

Cited by 21 publications

References 75 publications

Individual variation of the masticatory system dominates 3D skull shape in the herbivory-adapted marsupial wombats

Individual variation of the masticatory system dominates 3D skull shape in the herbivory-adapted marsupial wombats

Individual variation of the masticatory system dominates 3D skull shape in the herbivory-adapted marsupial wombats

Rates of morphological evolution, asymmetry and morphological integration of shell shape in scallops

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