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      Wing Musculature Reconstruction in Extinct Flightless Auks ( Pinguinus and Mancalla) Reveals Incomplete Convergence with Penguins (Spheniscidae) Due to Differing Ancestral States

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          Synopsis

          Despite longstanding interest in convergent evolution, factors that result in deviations from fully convergent phenotypes remain poorly understood. In birds, the evolution of flightless wing-propelled diving has emerged as a classic example of convergence, having arisen in disparate lineages including penguins (Sphenisciformes) and auks (Pan-Alcidae, Charadriiformes). Nevertheless, little is known about the functional anatomy of the wings of flightless auks because all such taxa are extinct, and their morphology is almost exclusively represented by skeletal remains. Here, in order to re-evaluate the extent of evolutionary convergence among flightless wing-propelled divers, wing muscles and ligaments were reconstructed in two extinct flightless auks, representing independent transitions to flightlessness: Pinguinus impennis (a crown-group alcid), and Mancalla (a stem-group alcid). Extensive anatomical data were gathered from dissections of 12 species of extant charadriiforms and 4 aequornithine waterbirds including a penguin. The results suggest that the wings of both flightless auk taxa were characterized by an increased mechanical advantage of wing elevator/retractor muscles, and decreased mobility of distal wing joints, both of which are likely advantageous for wing-propelled diving and parallel similar functional specializations in penguins. However, the conformations of individual muscles and ligaments underlying these specializations differ markedly between penguins and flightless auks, instead resembling those in each respective group’s close relatives. Thus, the wings of these flightless wing-propelled divers can be described as convergent as overall functional units, but are incompletely convergent at lower levels of anatomical organization—a result of retaining differing conditions from each group’s respective volant ancestors. Detailed investigations such as this one may indicate that, even in the face of similar functional demands, courses of phenotypic evolution are dictated to an important degree by ancestral starting points.

          French

          La reconstruction de la musculature des ailes d’espèces éteintes de pingouins non-volants ( Pinguinus et Mancalla) révèle une convergence incomplète avec les manchots (Spheniscidae) expliquée par des états ancestraux différentsMalgré un intérêt de longue date pour l'évolution convergente, les facteurs limitant l’evolution de phénotypes entièrement convergents restent mal compris. Chez les oiseaux, l'évolution de la plongée propulsée par les ailes, associée à une perte de la capacité de vol, est devenue un exemple classique de convergence, apparue dans des lignées disparates telles que les manchots (Sphenisciformes) et les pingouins (Pan-Alcidae, Charadriiformes). On sait cependant peu de choses sur l'anatomie fonctionnelle des ailes des pingouins non-volants, car tous sont éteints et leur morphologie est presque exclusivement représentée par des restes squelettiques. Ici, afin de réévaluer l'étendue de la convergence évolutive chez les espèces non-volantes d’oiseaux plongeurs propulsés par leurs ailes, les muscles des ailes et les ligaments ont été reconstruits chez deux espèces éteintes de pingouins non-volants. Ces espèces représentent des transitions indépendantes vers l'inaptitude à voler : Pinguinus impennis (un alcidé du groupe-couronne) et Mancalla (un alcidé du groupe-tronc). Des données anatomiques approfondies ont été recueillies à partir des dissections de 12 espèces actuelles de Charadriiformes et de 4 espèces d’oiseaux d’eau Aequornithes, dont un manchot. Les résultats suggèrent que les ailes des deux taxons de pingouins non-volants étaient caractérisées par un avantage mécanique accru des muscles alaires élévateurs / rétracteurs, et par une mobilité réduite des articulations distales de l'aile. Ces deux éléments sont probablement avantageux pour la plongée propulsée par les ailes, et représentent des spécialisations fonctionnelles similaires à celles des manchots. Cependant, les conformations des muscles et des ligaments individuels sous-jacents à ces spécialisations diffèrent nettement entre les manchots et les pingouins non-volants. Ces conformations ressemblent ainsi plutôt à celles des taxons proches de chaque groupe respectif. Chez ces oiseaux plongeurs non-volants propulsés par les ailes, les ailes peuvent être décrites comme convergentes en tant qu’unités fonctionnelles globales, mais sont incomplètement convergentes à des niveaux inférieurs d’organisation anatomique. C’est le résultat du maintien de conditions différentes héritées des ancêtres volants respectifs de chaque groupe. Des recherches détaillées comme celle-ci peuvent indiquer que, même face à des exigences fonctionnelles similaires, le cours de l'évolution phénotypique est dicté, de manière importante, par le point de départ ancestral.(Translated by Simon L. Ducatez)

          Spanish

          La reconstrucción de la musculatura del ala en álcidos extintos no voladores ( Pinguinus y Mancalla) revela una convergencia incompleta con los pingüinos (Spheniscidae) debido a sus distintos estados ancestralesA pesar del gran interés que tradicionalmente ha despertado la evolución convergente, los factores que limitan la evolución de fenotipos completamente convergentes siguen siendo poco conocidos. En las aves, la evolución del buceo mediante propulsión alar asociado a una pérdida de la capacidad de vuelo ha emergido como un ejemplo clásico de convergencia evolutiva, habiendo aparecido en linajes dispares que incluyen los pingüinos (Sphenisciformes) y los álcidos (Pan-Alcidae, Charadriiformes). Sin embargo, el conocimiento sobre la anatomía funcional de los álcidos no voladores es limitado, dado que dichos taxones están completamente extintos y su morfología está representada de modo prácticamente exclusivo por restos esqueléticos. En este trabajo, reconstruimos los ligamentos y los músculos del ala de dos álcidos extintos no voladores que representan dos transiciones independientes hacia la condición no voladora: Pinguinus impennis (un álcido del grupo corona) y Mancalla (un álcido del grupo troncal), con el objetivo de reevaluar el alcance de la convergencia evolutiva entre los distintos grupos de aves no voladoras que bucean mediante propulsión alar. A tal efecto, recolectamos información anatómica exhaustiva a partir de la disección de 12 especies existentes de caradriformes y 4 aequornitinas acuáticas, incluyendo un pingüino. Los resultados sugieren que las alas de ambos álcidos no voladores estaban caracterizadas por una mayor ventaja mecánica de los músculos elevadores/retractores del ala, y por una disminución de la movilidad de las articulaciones distales del ala. Ambas características son probablemente ventajosas para el buceo mediante propulsión alar y representan especializaciones funcionales similares a las de los pingüinos. Sin embargo, la configuración de los ligamentos y músculos individuales ligados a dichas especializaciones difiere marcadamente entre pingüinos y álcidos no voladores, siendo similar a la configuración en los respectivos parientes cercanos de cada grupo. En consecuencia, las alas de estas aves no voladoras que bucean mediante propulsión alar pueden ser descritas como convergentes si son consideradas como unidades funcionales generales, pero esta convergencia es incompleta en niveles inferiores de su organización anatómica. Esto es el resultado de la retención de las distintas condiciones presentes en los antepasados voladores de ambos grupos. Investigaciones detalladas como la presente pueden indicar que, incluso frente a requerimientos funcionales similares, el curso de la evolución fenotípica está fuertemente dictado por el punto de partida ancestral.(Translated by Juan Benito Moreno)

          Japanese

          絶滅無飛翔性ウミスズメ類( Pinguinus および Mancalla)における翼筋群の復元, およびそのペンギン類との「不完全な」収斂に見る祖先状態の重要性収斂進化に関する研究の歴史は古いが, 一見して収斂していると見られる系統間での表現型の違い(「不完全な」収斂)が生じる要因はよく理解されていない. 翼潜水性鳥類における無飛翔化は, ペンギン類(ペンギン目)やウミスズメ類(チドリ目汎ウミスズメ科)などの異なる系統で独立に生じており, 収斂の典型的な例とされてきた. しかし, 無飛翔性のウミスズメ類はすべてが現在では絶滅しており骨格以外の部分が知られていないため, その翼の機能形態に関する知見は皆無である. 本研究では, 無飛翔性の翼潜水鳥類における収斂の程度を再評価するため, 独立に無飛翔化を遂げた系統である Pinguinus impennis(ウミスズメ類頂冠群)および Mancalla(ウミスズメ類基幹群)の翼の筋および靭帯の復元を行った. この目的のため, 現生のチドリ目鳥類 12 種およびペンギンを含むアエクオルニテス類の水鳥 4 種の解剖を行った. 結果として, これらの無飛翔性ウミスズメ類の翼においては, 挙上・尾方屈曲にかかわる筋群の力学的有効性が大きいこと, 遠位の関節群の可動域が小さいことが示唆された. これらの特徴は翼潜水において機能的に有利であると考えられ, ペンギン類における特徴とも共通点が見られる. しかし, 個々の筋や靭帯の配置はペンギン類と無飛翔性ウミスズメ類との間で顕著に異なっており, むしろそれぞれの近縁群のものに近い. つまり, これらの鳥類の翼は機能的なレベルでは収斂しているものの, より下位の解剖学的なレベルでの収斂は不完全であり, これはそれぞれの飛翔性の祖先における形質状態が保持された結果であると解釈される. このような例は, 類似した機能的要求の下でも, 表現型進化の経路は祖先状態によって大きく左右されうることを示している.(Translated by JW)

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          Most cited references152

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          Convergent evolution of similar phenotypic features in similar environmental contexts has long been taken as evidence of adaptation. Nonetheless, recent conceptual and empirical developments in many fields have led to a proliferation of ideas about the relationship between convergence and adaptation. Despite criticism from some systematically minded biologists, I reaffirm that convergence in taxa occupying similar selective environments often is the result of natural selection. However, convergent evolution of a trait in a particular environment can occur for reasons other than selection on that trait in that environment, and species can respond to similar selective pressures by evolving nonconvergent adaptations. For these reasons, studies of convergence should be coupled with other methods-such as direct measurements of selection or investigations of the functional correlates of trait evolution-to test hypotheses of adaptation. The independent acquisition of similar phenotypes by the same genetic or developmental pathway has been suggested as evidence of constraints on adaptation, a view widely repeated as genomic studies have documented phenotypic convergence resulting from change in the same genes, sometimes even by the same mutation. Contrary to some claims, convergence by changes in the same genes is not necessarily evidence of constraint, but rather suggests hypotheses that can test the relative roles of constraint and selection in directing phenotypic evolution. © 2011 The Author(s). Evolution© 2011 The Society for the Study of Evolution.
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            Adaptive radiation, ecological opportunity, and evolutionary determinism. American Society of Naturalists E. O. Wilson award address.

            Adaptive radiation refers to diversification from an ancestral species that produces descendants adapted to use a great variety of distinct ecological niches. In this review, I examine two aspects of adaptive radiation: first, that it results from ecological opportunity and, second, that it is deterministic in terms of its outcome and evolutionary trajectory. Ecological opportunity is usually a prerequisite for adaptive radiation, although in some cases, radiation can occur in the absence of preexisting opportunity. Nonetheless, many clades fail to radiate although seemingly in the presence of ecological opportunity; until methods are developed to identify and quantify ecological opportunity, the concept will have little predictive utility in understanding a priori when a clade might be expected to radiate. Although predicted by theory, replicated adaptive radiations occur only rarely, usually in closely related and poorly dispersing taxa found in the same region on islands or in lakes. Contingencies of a variety of types may usually preclude close similarity in the outcome of evolutionary diversification in other situations. Whether radiations usually unfold in the same general sequence is unclear because of the unreliability of methods requiring phylogenetic reconstruction of ancestral events. The synthesis of ecological, phylogenetic, experimental, and genomic advances promises to make the coming years a golden age for the study of adaptive radiation; natural history data, however, will always be crucial to understanding the forces shaping adaptation and evolutionary diversification.
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              To better determine the history of modern birds, we performed a genome-scale phylogenetic analysis of 48 species representing all orders of Neoaves using phylogenomic methods created to handle genome-scale data. We recovered a highly resolved tree that confirms previously controversial sister or close relationships. We identified the first divergence in Neoaves, two groups we named Passerea and Columbea, representing independent lineages of diverse and convergently evolved land and water bird species. Among Passerea, we infer the common ancestor of core landbirds to have been an apex predator and confirm independent gains of vocal learning. Among Columbea, we identify pigeons and flamingoes as belonging to sister clades. Even with whole genomes, some of the earliest branches in Neoaves proved challenging to resolve, which was best explained by massive protein-coding sequence convergence and high levels of incomplete lineage sorting that occurred during a rapid radiation after the Cretaceous-Paleogene mass extinction event about 66 million years ago. Copyright © 2014, American Association for the Advancement of Science.
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                Author and article information

                Journal
                Integr Org Biol
                Integr Org Biol
                iob
                Integrative Organismal Biology
                Oxford University Press
                2517-4843
                2021
                11 November 2020
                11 November 2020
                : 3
                : 1
                Affiliations
                [1 ] Department of Earth Sciences, University of Cambridge , Downing Street, Cambridge, CB2 3EQ, UK
                [2 ] Department of Geology and Mineralogy, Kyoto University, Sakyoku Kitashirakawa Oiwakecho , Kyoto, 606-8502, Japan
                Author notes
                Article
                obaa040
                10.1093/iob/obaa040
                8271220
                34258512
                f2b10bbd-17d2-4642-aef0-32a82be4d6a3
                © The Author(s) 2020. Published by Oxford University Press on behalf of the Society for Integrative and Comparative Biology.

                This is an Open Access article distributed under the terms of the Creative Commons Attribution License ( http://creativecommons.org/licenses/by/4.0/), which permits unrestricted reuse, distribution, and reproduction in any medium, provided the original work is properly cited.

                Page count
                Pages: 65
                Product
                Funding
                Funded by: Royal Society;
                Categories
                Research Article

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