Early tetrapod cranial evolution is characterized by increased complexity, constraint, and an offset from fin-limb evolution

Rawson, James R. G.; Esteve‐Altava, Borja; Porro, Laura B.; Dutel, Hugo; Rayfield, Emily J.

doi:10.1126/sciadv.adc8875

Cited by 3 publications

(4 citation statements)

References 75 publications

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“…These modifications to the jaw played a crucial part in the water-to-land radiation, allowing early tetrapods to transition from feeding in the water to feeding on land (49–51). High levels of within-group disparity in the early tetrapod jaw correspond to high disparity previously identified in early tetrapod humerus (52) and cranium (53). Additionally, our disparity analysis shows a rapid peak and trough coincident with the period referred to as Romer’s Gap, a well-known period with few fossils from 360 to 345 Ma (41).…”

Section: Discussionsupporting

confidence: 76%

Neither Williston nor Dollo: mandibular complexity from stem tetrapods to modern amphibians

Watt,

Felice,

Goswami

2023

Preprint

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Directional trends in evolution have long captured the attention of biologists, and are particularly interesting when they reflect fundamental developmental processes that underlie morphological change. Here, we apply deep time data and a phylogenetic comparative framework to assess two fundamental “laws” – Williston’s law of phenotypic simplification and Dollo’s law of irreversibility – in the tetrapod mandible, a structure that has sustained the same primary function of feeding for nearly 400 million years. In spite of this conserved function, the tetrapod mandible has undergone numerous morphological and compositional changes during and since the initial water-to-land transition around 390Ma. To quantify these shifts, we reconstructed the compositional evolution of the mandible with 31 traits scored in 568 species from early tetrapods through to modern amphibians, thereby capturing immense developmental and ecological diversity as well as an excellent fossil record. Mandibular complexity and jaw disparity are highest at the base of the tetrapod tree and generally decrease through time, with stasis dominating over the last ∼160M years. Nonetheless, we find a lack of support for Williston’s and Dollo’s laws, with loss and gain of jaw components equally likely throughout the course of early tetrapod and amphibian evolution. Combined, our results demonstrate that evolutionary patterns of mandibular complexity are more nuanced than either Williston’s or Dollo’s laws allow. Thus, laws of simplification are too crude to capture the evolutionary processes underlying the evolution of even a functionally conserved structure through deep time.Significance StatementThe lower jaw is a key innovation in vertebrate evolution with a unifying primary function: feeding. In spite of this conserved function, the jaw is extremely diverse in shape and composition. In limbed vertebrates (tetrapods), the jaw evolves from a complex structure comprising multiple elements and high numbers of teeth towards a simpler structure comprising few elements and generally fewer teeth. Superficially, this pattern suggests support for both Williston’s and Dollo’s laws of phenotypic simplification and irreversibility, respectively. However, we find a lack of support for either law in the jaw of the earliest tetrapods and amphibians, adding to growing literature refuting overly simplified “laws” governing organismal evolution.

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Section: Discussionsupporting

confidence: 76%

Neither Williston nor Dollo: mandibular complexity from stem tetrapods to modern amphibians

Watt,

Felice,

Goswami

2023

Preprint

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“…In this study, we use a network approach [39] to overcome some of these difficulties. Networks have been used in previous studies of morphological integration [40], morphological complexity [41] and ecological complexity [42,43].…”

Section: Introductionmentioning

confidence: 99%

“…In this study, we use a network approach (39) to overcome some of these difficulties. Networks have been used in previous studies of morphological integration (40), morphological complexity (41), and ecological complexity (42,43). Here they allow us to create a flexible but consistent framework in which to characterize temporal patterns in part interactions and functional integration, regardless of the age, affinities, or specific homologies of the reproductive structures.…”

Section: Introductionmentioning

confidence: 99%

Quantifying the complexity of plant reproductive structures reveals a history of morphological and functional integration

Leslie,

Mander

2023

Proc. R. Soc. B.

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Vascular plant reproductive structures have undoubtedly become more complex through time, evolving highly differentiated parts that interact in specialized ways. But quantifying these patterns at broad scales is challenging because lineages produce disparate reproductive structures that are often difficult to compare and homologize. We develop a novel approach for analysing interactions within reproductive structures using networks, treating component parts as nodes and a suite of physical and functional interactions among parts as edges. We apply this approach to the plant fossil record, showing that interactions have generally increased through time and that the concentration of these interactions has shifted towards differentiated surrounding organs, resulting in more compact, functionally integrated structures. These processes are widespread across plant lineages, but their extent and timing vary with reproductive biology; in particular, seed-producing structures show them more strongly than spore or pollen-producing structures. Our results demonstrate that major reproductive innovations like the origin of seeds and angiospermy were associated with increased integration through greater interactions among parts. But they also reveal that for certain groups, particularly Mesozoic gymnosperms, millions of years elapsed between the origin of reproductive innovations and increased interactions among parts within their reproductive structures.

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“…Assumed to increase cranial integrity and skull strength 4 , simplification has been achieved through solidification, fusion, reduction, and loss of skeletal elements. These simplification events can be found across different tetrapod lineages [5][6][7] and throughout synapsid history, including mammals and their synapsid, pre-mammaliaform cynodont precursors (referred to as cynodonts hereafter) 8 . The evolution of mammals from cynodonts is a key transition in vertebrate history and is further characterised by a number of modifications of the cranial structure 9 , including the evolution of a novel, secondary jaw joint and a reduction of the seven bones in the lower jaw to a single tooth-bearing bone in crown mammals 10,11 .…”

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confidence: 99%

Functional reorganisation of the cranial skeleton during the cynodont–mammaliaform transition

et al. 2023

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Skeletal simplification occurred in multiple vertebrate clades over the last 500 million years, including the evolution from premammalian cynodonts to mammals. This transition is characterised by the loss and reduction of cranial bones, the emergence of a novel jaw joint, and the rearrangement of the jaw musculature. These modifications have long been hypothesised to increase skull strength and efficiency during feeding. Here, we combine digital reconstruction and biomechanical modelling to show that there is no evidence for an increase in cranial strength and biomechanical performance. Our analyses demonstrate the selective functional reorganisation of the cranial skeleton, leading to reduced stresses in the braincase and the skull roof but increased stresses in the zygomatic region through this transition. This cranial functional reorganisation, reduction in mechanical advantage, and overall miniaturisation in body size are linked with a dietary specialisation to insectivory, permitting the subsequent morphological and ecological diversification of the mammalian lineage.

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Early tetrapod cranial evolution is characterized by increased complexity, constraint, and an offset from fin-limb evolution

Cited by 3 publications

References 75 publications

Neither Williston nor Dollo: mandibular complexity from stem tetrapods to modern amphibians

Neither Williston nor Dollo: mandibular complexity from stem tetrapods to modern amphibians

Quantifying the complexity of plant reproductive structures reveals a history of morphological and functional integration

Functional reorganisation of the cranial skeleton during the cynodont–mammaliaform transition

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