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      Morphological and ecological convergence at the lower size limit for vertebrates highlighted by five new miniaturised microhylid frog species from three different Madagascan genera

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          Abstract

          Miniaturised frogs form a fascinating but poorly understood amphibian ecomorph and have been exceptionally prone to taxonomic underestimation. The subfamily Cophylinae (family Microhylidae), endemic to Madagascar, has a particularly large diversity of miniaturised species which have historically been attributed to the single genus Stumpffia largely based on their small size. Recent phylogenetic work has revealed that several independent lineages of cophyline microhylids evolved towards highly miniaturised body sizes, achieving adult snout–vent lengths under 16 mm. Here, we describe five new species belonging to three clades that independently miniaturised and that are all genetically highly divergent from their relatives: (i) a new genus ( Mini gen. nov.) with three new species from southern Madagascar, (ii) one species of Rhombophryne, and (iii) one species of Anodonthyla. Mini mum sp. nov. from Manombo in eastern Madagascar is one of the smallest frogs in the world, reaching an adult body size of 9.7 mm in males and 11.3 mm in females. Mini scule sp. nov. from Sainte Luce in southeastern Madagascar is slightly larger and has maxillary teeth. Mini ature sp. nov. from Andohahela in southeast Madagascar is larger than its congeners but is similar in build. Rhombophryne proportionalis sp. nov. from Tsaratanana in northern Madagascar is unique among Madagascar’s miniaturised frogs in being a proportional dwarf, exhibiting far less advanced signs of paedomorphism than other species of similar size. Anodonthyla eximia sp. nov. from Ranomafana in eastern Madagascar is distinctly smaller than any of its congeners and is secondarily terrestrial, providing evidence that miniaturisation and terrestriality may be evolutionarily linked. The evolution of body size in Madagascar’s microhylids has been more dynamic than previously understood, and future studies will hopefully shed light on the interplay between ecology and evolution of these remarkably diverse frogs.

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          Most cited references 66

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          Size and shape in ontogeny and phylogeny

          We present a quantitative method for describing how heterochronic changes in ontogeny relate to phyletic trends. This is a step towards creating a unified view of developmental biology and evolutionary ecology in the study of morphological evolution. Using this representation, we obtain a greatly simplified and logical scheme of classification. We believe that this scheme will be particularly useful in studying the data of paleontology and comparative morphology and in the analysis of processes leading to adaptive radiation. We illustrate this scheme by examples drawn from the literature and our own work.
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            Vast underestimation of Madagascar's biodiversity evidenced by an integrative amphibian inventory.

            Amphibians are in decline worldwide. However, their patterns of diversity, especially in the tropics, are not well understood, mainly because of incomplete information on taxonomy and distribution. We assess morphological, bioacoustic, and genetic variation of Madagascar's amphibians, one of the first near-complete taxon samplings from a biodiversity hotspot. Based on DNA sequences of 2,850 specimens sampled from over 170 localities, our analyses reveal an extreme proportion of amphibian diversity, projecting an almost 2-fold increase in species numbers from the currently described 244 species to a minimum of 373 and up to 465. This diversity is widespread geographically and across most major phylogenetic lineages except in a few previously well-studied genera, and is not restricted to morphologically cryptic clades. We classify the genealogical lineages in confirmed and unconfirmed candidate species or deeply divergent conspecific lineages based on concordance of genetic divergences with other characters. This integrative approach may be widely applicable to improve estimates of organismal diversity. Our results suggest that in Madagascar the spatial pattern of amphibian richness and endemism must be revisited, and current habitat destruction may be affecting more species than previously thought, in amphibians as well as in other animal groups. This case study suggests that worldwide tropical amphibian diversity is probably underestimated at an unprecedented level and stresses the need for integrated taxonomic surveys as a basis for prioritizing conservation efforts within biodiversity hotspots.
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              Heterochrony and allometry: the analysis of evolutionary change in ontogeny.

              The connection between development and evolution has become the focus of an increasing amount of research in recent years, and heterochrony has long been a key concept in this relation. Heterochrony is defined as evolutionary change in rates and timing of developmental processes; the dimension of time is therefore an essential part in studies of heterochrony. Over the past two decades, evolutionary biologists have used several methodological frameworks to analyse heterochrony, which differ substantially in the way they characterize evolutionary changes in ontogenies and in the resulting classification, although they mostly use the same terms. This review examines how these methods compare ancestral and descendant ontogenies, emphasizing their differences and the potential for contradictory results from analyses using different frameworks. One of the two principal methods uses a clock as a graphical display for comparisons of size, shape and age at a particular ontogenic stage, whereas the other characterizes a developmental process by its time of onset, rate, and time of cessation. The literature on human heterochrony provides particularly clear examples of how these differences produce apparent contradictions when applied to the same problem. Developmental biologists recently have extended the concept of heterochrony to the earliest stages of development and have applied it at the cellular and molecular scale. This extension brought considerations of developmental mechanisms and genetics into the study of heterochrony, which previously was based primarily on phenomenological characterizations of morphological change in ontogeny. Allometry is the pattern of covariation among several morphological traits or between measures of size and shape; unlike heterochrony, allometry does not deal with time explicitly. Two main approaches to the study of allometry are distinguished, which differ in the way they characterize organismal form. One approach defines shape as proportions among measurements, based on considerations of geometric similarity, whereas the other focuses on the covariation among measurements in ontogeny and evolution. Both are related conceptually and through the use of similar algebra. In addition, there are close connections between heterochrony and changes in allometric growth trajectories, although there is no one-to-one correspondence. These relationships and outline links between different analytical frameworks are discussed.
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                Author and article information

                Contributors
                Role: ConceptualizationRole: Data curationRole: Formal analysisRole: InvestigationRole: MethodologyRole: Project administrationRole: ResourcesRole: Writing – original draftRole: Writing – review & editing
                Role: InvestigationRole: ResourcesRole: Writing – review & editing
                Role: InvestigationRole: ResourcesRole: Writing – review & editing
                Role: InvestigationRole: ResourcesRole: Writing – review & editing
                Role: InvestigationRole: ResourcesRole: Writing – review & editing
                Role: InvestigationRole: ResourcesRole: Writing – review & editing
                Role: InvestigationRole: ResourcesRole: Writing – review & editing
                Role: InvestigationRole: ResourcesRole: Writing – review & editing
                Role: InvestigationRole: ResourcesRole: Writing – review & editing
                Role: ConceptualizationRole: InvestigationRole: ResourcesRole: SupervisionRole: Writing – review & editing
                Role: ConceptualizationRole: InvestigationRole: ResourcesRole: SupervisionRole: Writing – review & editing
                Role: Editor
                Journal
                PLoS One
                PLoS ONE
                plos
                plosone
                PLoS ONE
                Public Library of Science (San Francisco, CA USA )
                1932-6203
                27 March 2019
                2019
                : 14
                : 3
                Affiliations
                [1 ] Sektion Herpetologie, Zoologische Staatssammlung München (ZSM-SNSB), München, Germany
                [2 ] Division of Evolutionary Biology, Zoologisches Institut, Technische Universität Braunschweig, Braunschweig, Germany
                [3 ] Systematische Zoologie, Department Biologie II, Biozentrum, Ludwig-Maximilians-Universität München, Planegg-Martinsried, Germany
                [4 ] Biodiversity Institute and Department of Ecology and Evolutionary Biology, University of Kansas, Lawrence, KS, United States of America
                [5 ] Mention Zoologie et Biodiversité Animale, Université d’Antananarivo, Antananarivo, Madagascar
                [6 ] Institute of Zoology, Universität Hamburg, Hamburg, Germany
                [7 ] Museum für Naturkunde–Leibniz Institute for Evolution and Biodiversity Science, Berlin, Germany
                [8 ] SEED Madagascar, London, United Kingdom
                [9 ] Oxford Brookes University, Oxford, United Kingdom
                [10 ] CIBIO, Research Centre in Biodiversity and Genetic Resources, InBIO, Campus Agrário de Vairão, Universidade do Porto, Vairão, Portugal
                University of Sydney, AUSTRALIA
                Author notes

                Competing Interests: The authors have declared that no competing interests exist.

                Article
                PONE-D-18-35188
                10.1371/journal.pone.0213314
                6436692
                30917162
                © 2019 Scherz et al

                This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.

                Page count
                Figures: 13, Tables: 2, Pages: 45
                Product
                Funding
                AC is supported by an Investigador FCT grant from the Portuguese National Funds through FCT (Foundation for Science and Technology) grant IF/00209/2014. JCR, JG, M-OR and SHN were supported by the Deutsche Forschungsgemeinschaft (grant GL 665/1-1 and RO 3064/2-1). Fieldwork of FG and MV was supported by the Volkswagen foundation. MDS and MV were supported by the Deutsche Forschungsgemeinschaft (grant VE 247/13-1). No funders played any role in study design, data collection, analysis, or decision to publish.
                Categories
                Research Article
                Biology and Life Sciences
                Anatomy
                Musculoskeletal System
                Body Limbs
                Legs
                Feet
                Toes
                Medicine and Health Sciences
                Anatomy
                Musculoskeletal System
                Body Limbs
                Legs
                Feet
                Toes
                Biology and Life Sciences
                Organisms
                Eukaryota
                Animals
                Vertebrates
                Amphibians
                Frogs
                Biology and Life Sciences
                Anatomy
                Digestive System
                Teeth
                Medicine and Health Sciences
                Anatomy
                Digestive System
                Teeth
                Biology and Life Sciences
                Anatomy
                Head
                Jaw
                Teeth
                Medicine and Health Sciences
                Anatomy
                Head
                Jaw
                Teeth
                Biology and Life Sciences
                Anatomy
                Musculoskeletal System
                Body Limbs
                Arms
                Hands
                Fingers
                Medicine and Health Sciences
                Anatomy
                Musculoskeletal System
                Body Limbs
                Arms
                Hands
                Fingers
                Biology and Life Sciences
                Anatomy
                Musculoskeletal System
                Skeleton
                Maxilla
                Medicine and Health Sciences
                Anatomy
                Musculoskeletal System
                Skeleton
                Maxilla
                Biology and Life Sciences
                Anatomy
                Osteology
                Medicine and Health Sciences
                Anatomy
                Osteology
                Biology and Life Sciences
                Taxonomy
                New Species Reports
                Computer and Information Sciences
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                Biology and life sciences
                Biochemistry
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                Non-coding RNA
                Ribosomal RNA
                Biology and life sciences
                Biochemistry
                Ribosomes
                Ribosomal RNA
                Biology and life sciences
                Cell biology
                Cellular structures and organelles
                Ribosomes
                Ribosomal RNA
                Custom metadata
                Osteological data are deposited in MorphoSource.org: http://morphosource.org/Detail/ProjectDetail/Show/project_id/464. Sequence data are deposited in GenBank (see S1 Table for a full list of those used herein). All measurement data are contained within the manuscript.

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