Classification and Evolution of the Burrowing Sea Anemones
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ZOOSYSTEMATICA ROSSICA ISSN 2410-0226 Zoological Institute, Russian Academy of Sciences, St Petersburg ▪ https://www.zin.ru/journals/zsr/ [ onl ine] 0320-9180 Vol. 29(2): 213–237 ▪ Published online 20 October 2020 ▪ DOI 10.31610/zsr/2020.29.2.213 [ print] RESEARCH ARTICLE Classification and evolution of the burrowing sea anemones (Anthozoa: Actiniaria: Athenaria): a review of the past and current views Классификация и эволюция закапывающихся актиний (Anthozoa: Actiniaria: Athenaria): обзор прежних и современных представлений N.Yu. Ivanova Н.Ю. Иванова Natalia Yu. Ivanova, Zoological Institute, Russian Academy of Sciences, 1 Universitetskaya Emb., St Petersburg 199034, Russia. E-mail: [email protected] Abstract. The opinions of systematists about the classification and evolution of burrowing sea anemones have repeatedly changed over the long-term study of Actiniaria. Four stages can be distinguished over the course of the classification history. Each system was characterised by the use of mainly one particular fea- ture. These features were: (1) characters of the external morphology, (2) arrangement of the mesenteries, (3) presence or absence of the basilar muscles and (4) molecular markers. The views on the origin and the evolution of the burrowing sea anemones were also altered more than once, that led to the emergence of several hypotheses. The burrowing sea anemones were considered as a primitive group or, on the contrary, as more advanced descendants of large hexamerous actinians. Резюме. Представления исследователей о классификации и эволюции закапывающихся актиний неоднократно менялись в течение длительного времени изучения Actiniaria. В процессе формирования классификации можно выделить четыре этапа. Каждый из них характеризовался использованием в основном одного признака, на который опирались авторы при построении своей системы. К этим признакам следует отнести: (1) черты внешнего строения, (2) распо- ложение мезентериев, (3) наличие или отсутствие базилярных мускулов и (4) молекуляр- ные маркеры. Представления о происхождении и эволюции закапывающихся актиний также неоднократно изменялись, что привело к появлению нескольких гипотез. Закапывающиеся морские анемоны рассматривались в качестве примитивной группы или, наоборот, как более продвинутые потомки крупных гексамерных актиний. Key words: burrowing anemones, comparative morpho-anatomical analysis, taxonomic characters, clas- sification, evolution, Athenaria Ключевые слова: закапывающиеся актинии, сравнительный морфо-анатомический анализ, таксономические признаки, классификация, эволюция, Athenaria ZooBank Article LSID: urn:lsid:zoobank.org:pub:2B001412-4B70-4E12-BB97-54D620F6D12F Introduction huge amount of work in an attempt to build a nat- ural classification that reflected the evolution of The classification of the burrowing sea anemo- this group. The first researchers (Milne-Edwards nes has a long history dating back more than 150 & Haime, 1857; Gosse, 1858, 1860) relied main- years. During this time, researchers conducted a ly on the external features of the burrowing sea © 2020 Zoological Institute RAS and the Author(s) N.Yu. Ivanova. Classification and evolution of the burrowing sea anemones anemones to arrive at a classification. Later it be- to represent a polyphyletic group (Hand, 1966; came clear that anatomical characters were more Schmidt, 1972, 1974). stable and reliable characters (Hertwig, 1882; Following the contemporary trend in the nat- McMurrich, 1893). ural sciences, many specialists had high hopes of The transition to a classification based on in- solving the difficult problems of phylogeny and sys- ternal features was associated with a detailed tematics based on molecular genetic studies. Un- study of the successive development of the mes- fortunately, as evident from the new higher-level enteries by Hertwig & Hertwig (1879). It became classification for Actiniaria proposed by Rodríguez soon clear, however, that relying solely on the ar- et al. (2014), these issues are still far from being rangement of the mesenteries led to the union of resolved. Firstly, that classification yields a com- unrelated polyps and to the separation of close- bination of completely dissimilar forms. For exam- ly related forms (Beneden, 1897). According to ple, the edwardsians and the endocoelantheans are Carlgren (1898, 1900, 1905), the most important placed in one order: apart from sequence similarity, feature in classifying the burrowing sea anemones however, these sea anemones have no other common is the absence of the basilar muscles. Over time, his features in either structure or biology. Secondly, system was improved, developed, and published in placing some burrowing sea anemones, which lack the monograph “A survey of the Ptychodactiaria, acontia, together with the thenarian polyps that Corallimorpharia and Actiniaria” (1949). Carl- possess them, in the superfamily Metridioidea, was gren’s (1949) classification was universally accept- explained by loss of the acontia. Thirdly, when us- ed and was used by all researchers until recently. ing one set of markers, the position of many genera In the second half of the 20th century, however, in the scheme reflected a particular phylogenetic Carlgren’s system was increasingly though not to relationship, whereas using other markers yielded reflect the phylogeny of Actiniaria, and the bur- a quite different result. That cast doubt on the ap- rowing sea anemones were ultimately considered plicability of the method itself. Fig 1. Early sea anemone division based on characters of their external morphology. a, burrowing sea anemones, elongated forms with a rounded aboral end or physa; b, large attached sea anemones with a well-developed, flat, adhesive and muscular pedal disc. After Gosse (1860). 214 ( Zoosystematica Rossica, Vol. 29, No. 2, pp. 213–237 N.Yu. Ivanova. Classification and evolution of the burrowing sea anemones 1. Development of classification of 1.2. Transition to the classification based the burrowing sea anemones on internal features: the succession of arising mesenteries 1.1. Classification based on external morphological features The system of all Anthozoa, including the sea anemones, was later based on features of the inter- The taxonomists of the mid-19th century re- nal organization of the polyp (McMurrich, 1893). lied on external features to construct the classi- fication of sea anemones. They separated the bur- Haime (1854) was the first to point out the impor- rowing forms from the remaining representatives tance of anatomical features, but only Hertwig & based on their elongated body shape and absence Hertwig (1879) began to use them in constructing of a pedal disc (Fig. 1a, b). Milne-Edwards & their classification. Having traced the formation Haime (1857) placed these anemones inside of the of mesenteries in the sea anemones, the zoanthids, subfamily Actininae in section “Actinines pivo- and the octocorals, Hertwig & Hertwig (1879) tantes”, defining them as “species whose base is considered that the arrangement of mesenteries very small and body is very elongated” (Fig. 2). In and the development of their muscles (but not constructing his system, Gosse (1860) also relied their number as Ehrenberg (1834) and Haeckel on the presence or absence of a sticky pedal disc. (1866) believed) should be regarded as the most Accordingly, he isolated the worm-like anemones important taxonomic characters. along with the cerianthids from other anemones Hertwig & Hertwig (1879) and many subse- in the family Ilyanthidae (Gosse, 1858). Verrill quent researchers demonstrated that, in the early (1864) was among the first zoologists to draw at- stages of development, sea anemones are bilateral- tention to internal features of the polyp, indicating ly symmetrical animals. This is underlined by the the number of mesenteries (“internal lamellae”) in presence of eight primary mesenteries, which are a description of the species. Nonetheless, as diag- symmetrical with respect to the plane of a flat- nostic features for distinguishing genera and fami- tened pharynx. First, in anemone larvae, two lies, Verrill mainly used external features: body ventro-lateral mesenteries are formed to the right shape, surface structure, tentacles number, etc. and left of the flattened pharynx, making up the Klunzinger (1877) also used the elongated body bilateral pair (“couple”) (Fig. 3a). They divide the and rounded or pointed proximal end of the body body cavity into a smaller part located on the con- without a well-differentiated pedal disc as diag- ventionally ventral side, and a large portion on the nostic characteristics. conventionally dorsal side. The next mesenteries Fig 2. The position of burrowing sea anemones (in bold) in Milne-Edwards & Haime’s (1857) classification of coral polyps. ( Zoosystematica Rossica, Vol. 29, No. 2, pp. 213–237 215 N.Yu. Ivanova. Classification and evolution of the burrowing sea anemones Figs 3–6. The succession of arising mesenteries, schematic transversal section. 3, the first type;a , the first cou- ple (ventro-lateral mesenteries); b, the second couple (dorsal directive mesenteries); c, the third couple (ventral directive mesenteries); d, the fourth couple (dorso-lateral mesenteries); 4, the second type; a, the first couple (ven- tro-lateral mesenteries); b, the second couple (dorso-lateral mesenteries); c, the third couple (ventral directive mesenteries); d, the fourth couple (dorsal directive mesenteries); 5, Edwardsia stage; 6, arising of the fifth and sixth couples of lateral mesenteries.