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A single origin of extreme matrotrophy in African mabuyine skinks.

ABSTRACT: Most mammals and approximately 20% of squamates (lizards and snakes) are viviparous, whereas all crocodilians, birds and turtles are oviparous. Viviparity evolved greater than 100 times in squamates, including multiple times in Mabuyinae (Reptilia: Scincidae), making this group ideal for studying the evolution of nutritional patterns associated with viviparity. Previous studies suggest that extreme matrotrophy, the support of virtually all of embryonic development by maternal nutrients, evolved as many as three times in Mabuyinae: in Neotropical Mabuyinae (63 species), Eumecia (2 species; Africa) and Trachylepis ivensii (Africa). However, no explicit phylogenetic hypotheses exist for understanding the evolution of extreme matrotrophy. Using multilocus DNA data, we inferred a species tree for Mabuyinae that implies that T. ivensii (here assigned to the resurrected genus Lubuya) is sister to Eumecia, suggesting that extreme matrotrophy evolved only once in African mabuyine skinks.

SUBMITTER: Metallinou M

PROVIDER: S-EPMC5014036 | biostudies-literature | 2016 Aug

REPOSITORIES: biostudies-literature

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A single origin of extreme matrotrophy in African mabuyine skinks.

Metallinou Margarita M Weinell Jeffrey L JL Karin Benjamin R BR Conradie Werner W Wagner Philipp P Schmitz Andreas A Jackman Todd R TR Bauer Aaron M AM

Biology letters 20160801 8

Most mammals and approximately 20% of squamates (lizards and snakes) are viviparous, whereas all crocodilians, birds and turtles are oviparous. Viviparity evolved greater than 100 times in squamates, including multiple times in Mabuyinae (Reptilia: Scincidae), making this group ideal for studying the evolution of nutritional patterns associated with viviparity. Previous studies suggest that extreme matrotrophy, the support of virtually all of embryonic development by maternal nutrients, evolved ...[more]

PMID: 27555650

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Project description:BackgroundSkulls serve many functions and as a result, are subject to many different evolutionary pressures. In squamates, many fossorial species occupy a unique region of skull morphospace, showing convergence across families, due to modifications related to head-first burrowing. As different substrates have variable physical properties, particular skull shapes may offer selective advantages in certain substrates. Despite this, studies of variation within burrowers have been limited and are typically focused on a single origin of fossoriality. We focused on seven skink genera (Acontias, Typhlosaurus, Scelotes, Sepsina, Feylinia, Typhlacontias, and Mochlus; 39 sp.) from southern Africa, encompassing at least three independent evolutions of semi-fossoriality/fossoriality. We used microCT scans and geometric morphometrics to test how cranial and mandibular shape were influenced by phylogenetic history, size, and ecology. We also qualitatively described the skulls of four species to look at variation across phylogenetic and functional levels, and assess the degree of convergence.ResultsWe found a strong effect of phylogenetic history on cranial and mandibular shape, with size and substrate playing secondary roles. There was a clear gradient in morphospace from less specialized to more specialized burrowers and burrowers in sand were significantly different from those in other substrates. We also created an anatomical atlas for four species with each element described in isolation. Every bone showed some variation in shape and relative scaling of features, with the skull roofing bones, septomaxilla, vomer, and palatine showing the most variation. We showed how broad-scale convergence in traits related to fossoriality can be the result of different anatomical changes.ConclusionsOur study used geometric morphometrics and comparative anatomy to examine how skull morphology changes for a highly specialized and demanding lifestyle. Although there was broad convergence in both shape and qualitative traits, phylogenetic history played a large role and much of this convergence was produced by different anatomical changes, implying different developmental pathways or lineage-specific constraints. Even within a single family, adaptation for a specialized ecology does not follow a singular deterministic path.

Project description:Matrotrophy, the continuous extra-vitelline supply of nutrients from the parent to the progeny during gestation, is one of the masterpieces of nature, contributing to offspring fitness and often correlated with evolutionary diversification. The most elaborate form of matrotrophy-placentotrophy-is well known for its broad occurrence among vertebrates, but the comparative distribution and structural diversity of matrotrophic expression among invertebrates is wanting. In the first comprehensive analysis of matrotrophy across the animal kingdom, we report that regardless of the degree of expression, it is established or inferred in at least 21 of 34 animal phyla, significantly exceeding previous accounts and changing the old paradigm that these phenomena are infrequent among invertebrates. In 10 phyla, matrotrophy is represented by only one or a few species, whereas in 11 it is either not uncommon or widespread and even pervasive. Among invertebrate phyla, Platyhelminthes, Arthropoda and Bryozoa dominate, with 162, 83 and 53 partly or wholly matrotrophic families, respectively. In comparison, Chordata has more than 220 families that include or consist entirely of matrotrophic species. We analysed the distribution of reproductive patterns among and within invertebrate phyla using recently published molecular phylogenies: matrotrophy has seemingly evolved at least 140 times in all major superclades: Parazoa and Eumetazoa, Radiata and Bilateria, Protostomia and Deuterostomia, Lophotrochozoa and Ecdysozoa. In Cycliophora and some Digenea, it may have evolved twice in the same life cycle. The provisioning of developing young is associated with almost all known types of incubation chambers, with matrotrophic viviparity more widespread (20 phyla) than brooding (10 phyla). In nine phyla, both matrotrophic incubation types are present. Matrotrophy is expressed in five nutritive modes, of which histotrophy and placentotrophy are most prevalent. Oophagy, embryophagy and histophagy are rarer, plausibly evolving through heterochronous development of the embryonic mouthparts and digestive system. During gestation, matrotrophic modes can shift, intergrade, and be performed simultaneously. Invertebrate matrotrophic adaptations are less complex structurally than in chordates, but they are more diverse, being formed either by a parent, embryo, or both. In a broad and still preliminary sense, there are indications of trends or grades of evolutionarily increasing complexity of nutritive structures: formation of (i) local zones of enhanced nutritional transport (placental analogues), including specialized parent-offspring cell complexes and various appendages increasing the entire secreting and absorbing surfaces as well as the contact surface between embryo and parent, (ii) compartmentalization of the common incubatory space into more compact and 'isolated' chambers with presumably more effective nutritional relationships, and (iii) internal secretory ('milk') glands. Some placental analogues in onychophorans and arthropods mimic the simplest placental variants in vertebrates, comprising striking examples of convergent evolution acting at all levels-positional, structural and physiological.

Dataset Information

A single origin of extreme matrotrophy in African mabuyine skinks.

Publications

A single origin of extreme matrotrophy in African mabuyine skinks.

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