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In Search of Phylogenetic Congruence Between Molecular and Morphological Data in Bryozoans with Extreme Adult Skeletal Heteromorphy

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In Search of Phylogenetic Congruence Between Molecular and Morphological Data in Bryozoans with Extreme Adult Skeletal Heteromorphy Title In search of phylogenetic congruence between molecular and morphological data in bryozoans with extreme adult skeletal heteromorphy Authors Taylor, PD; Waeschenbach, A; Smith, AM; Gordon, DP Description peerreview_statement: The publishing and review policy for this title is described in its Aims & Scope. aims_and_scope_url: http://www.tandfonline.com/action/journalInformation? show=aimsScope&journalCode=tsab20 Date Submitted 2016-03-24 Systematics and Biodiversity In search of phylogenetic congruence between molecular and morphological data in bryozoans with extreme adult skeletal heteromorphy Journal: Systematics and Biodiversity Manuscript ID: TSAB-2015-0002.R1 Manuscript Type: Original Research Article Bryozoa, Cyclostomata, early astogeny, molecular phylogeny, morphology, Keywords: New Zealand, taxonomy URL: http://mc.manuscriptcentral.com/tsab Page 1 of 48 Systematics and Biodiversity 1 2 3 4 5 6 In search of phylogenetic congruence between molecular and 7 8 morphological data in bryozoans with extreme adult skeletal 9 10 heteromorphy 11 12 1 2 3 13 PAUL D. TAYLOR , ANDREA WAESCHENBACH , ABIGAIL M. SMITH & 14 DENNIS P. GORDON4 15 16 17 1Department of Earth Sciences, Natural History Museum, London SW7 5BD 18 2 19 Department of Life Sciences, Natural History Museum, London SW7 5BD 20 3Department of Marine Science, University of Otago, Dunedin 9054, New Zealand 21 4 22 NIWA, Greta Point, P.O. Box 14-901, Wellington, New Zealand 23 24 25 The taxonomy of cyclostome bryozoans, both Recent and fossil, is founded almost 26 entirely on characters of the mineralized skeleton. However, the adequacy of these 27 28 characters is now being questioned by molecular sequence data. In this study we 29 construct a molecular tree using ssrDNA and lsrDNA sequences and identify a clade 30 of New Zealand cyclostomes containing species exhibiting widely different 31 32 morphologies. In particular, Diaperoecia purpurascens (Hutton), a species assigned 33 to the suborder Tubuliporina on the basis of adult skeletal morphology, is shown to be 34 35 closely related to New Zealand species assigned to Heteropora, including H. 36 neozelanica Busk, which has a very different adult skeleton and is traditionally placed 37 38 in the suborder Cerioporina. A new species resembling the Antarctic genus 39 Hastingsia, ‘H’. whitteni sp. nov., from North Island, New Zealand, is found to 40 41 belong to the same clade, despite being placed conventionally in a different family 42 (Hastingsiidae) from both Diaperoecia (Diaperoeciidae) and Heteropora 43 44 (Cerioporidae). These results challenge the utility of adult skeletal morphology in 45 cyclostome taxonomy. In contrast to the striking dissimilarity between the adult 46 47 skeletons of D. purpurascens and ‘Hastingsia’ whitteni compared to New Zealand 48 species of Heteropora, morphological similarities in early colony development, as 49 50 well possibly as the presence of a gizzard, corroborate the molecular interpretation of 51 their close relationships. Greater attention should be paid in the future to early 52 53 astogenetic characters in cyclostome taxonomy. 54 55 56 57 58 1 59 60 URL: http://mc.manuscriptcentral.com/tsab Systematics and Biodiversity Page 2 of 48 1 2 3 4 5 6 Key words: Bryozoa, Cyclostomata, early astogeny, molecular phylogeny, 7 morphology, New Zealand, taxonomy 8 9 10 11 Introduction 12 A recurrent topic of discussion in taxonomy is the reliability of morphology in 13 14 interpreting phylogenetic relationships and hence in devising ‘natural’ classifications. 15 Molecular sequence data provide a powerful means of accessing the efficacy of 16 17 morphology for this purpose. In the ideal scenario there is a high degree of 18 congruence between molecules and morphology, corroborating the taxonomic value 19 20 of morphology. However, there are numerous instances where molecular sequence 21 data have undermined the taxonomic value of traditional morphological characters by 22 23 revealing close genetic relationships between morphologically distinct taxa (e.g. 24 Blackwell et al., 2003; Sotiaux et al., 2009; Pérez, 2011; Bourret et al., 2012). 25 26 Bryozoa is a phylum of lophotrochozoan invertebrates, distributed globally 27 across many aquatic habitats, and moderately diverse, comprising some 5689 living 28 29 species (Bock & Gordon, 2013). The two dominant orders of modern bryozoans – 30 Cheilostomata and Cyclostomata – are both marine and have calcareous skeletons that 31 furnish nearly all of the characters used in their taxonomy. Not only are these skeletal 32 33 characters immediately obvious in preserved material, but exactly the same characters 34 are available to palaeontologists studying fossil cheilostomes and cyclostomes. 35 36 Indeed, a common procedure in taxonomic studies of cheilostomes and cyclostomes is 37 to soak specimens in dilute bleach to remove all soft tissues, leaving only the 38 39 calcareous skeleton for identification. 40 A reasonably large number of skeletal morphological characters are available 41 42 for cheilostome taxonomy and molecular studies at low taxonomic levels generally 43 show good congruence with morphology (e.g., Hughes et al., 2008; Herrera-Cubilla 44 45 & Jackson, 2014), even though morphological convergence is evident between some 46 higher taxonomic groups (Waeschenbach et al., 2012). Cyclostomes, however, have a 47 48 simpler skeletal morphology and there can be significant incongruence between 49 molecules and morphology, as is apparent from mismatches when traditional 50 51 suborders founded on skeletal morphology are mapped onto molecular trees 52 (Waeschenbach et al., 2009; Taylor et al., 2011). 53 54 55 56 57 58 2 59 60 URL: http://mc.manuscriptcentral.com/tsab Page 3 of 48 Systematics and Biodiversity 1 2 3 4 5 6 The purpose of this study is to use molecular sequence data to construct a 7 phylogenetic tree for cyclostome bryozoans and to focus particularly on the 8 9 unexpected relationships found between some species from New Zealand. These 10 species are revised taxonomically, based on traditional skeletal characters, and 11 12 morphological apomorphies supporting the molecular phylogeny are sought. One of 13 the commonest cyclostome bryozoans found in New Zealand waters is Diaperoecia 14 15 purpurascens (Hutton, 1877) (Fig. 1). Although the generic attribution of this species 16 has varied through time, with others placing it in Entalophora or Pustulopora, it has 17 18 always been considered as belonging to suborder Tubuliporina based on skeletal 19 morphology. We here generate ssrDNA and lsrDNA sequences for Diaperoecia 20 21 purpurascens for the first time, showing that the species groups within a clade 22 containing New Zealand material attributed to Heteropora (Fig. 2). Traditional 23 24 cyclostome taxonomy places Heteropora in a different suborder – Cerioporina – 25 reflecting the striking differences in the morphology of the zooidal skeletons of 26 27 Diaperoecia and Heteropora. However, our molecular findings are corroborated by a 28 study of skeletal characters from early colony development, notably the shape and 29 30 pattern of the pseudopores on the protoecium, which support a close relationship 31 among D. purpurascens, the New Zealand species of Heteropora and a previously un- 32 33 named New Zealand species of ‘Hastingsia’ which molecular sequence data group 34 with these other two cyclostomes. Our findings point to the potential taxonomic value 35 36 of morphological characters seen in the early colony development of cyclostome 37 bryozoans. 38 39 40 Material and methods 41 42 43 Morphology 44 45 The material used for this study comprises historical specimens preserved in the 46 collections of the Natural History Museum, London (NHMUK), as well as some more 47 48 recently collected material from New Zealand which is now divided between the 49 collections of the NHMUK and the National Institute for Water and Atmospheric 50 51 Research (NIWA) in Wellington, New Zealand. 52 SEM of skeletal morphology was undertaken using LEO 1455VP and FEI 53 54 Quanta 650 ESEM scanning electron microscopes at the NHMUK. These instruments 55 56 57 58 3 59 60 URL: http://mc.manuscriptcentral.com/tsab Systematics and Biodiversity Page 4 of 48 1 2 3 4 5 6 allowed the study of uncoated, dried and bleached specimens imaged with back- 7 scattered electrons. 8 9 10 Molecular study 11 12 Total genomic DNA was extracted from ethanol-preserved specimens using the 13 DNeasy tissue kit (QIAGEN) following the manufacturer’s instructions. lsrDNA was 14 15 amplified in two fragments using Steno250F + Steno1800R and Steno1800F + 16 Steno3490R (Waeschenbach et al., 2009). ssrDNA was amplified in two fragments 17 18 using 18e (Hillis & Dixon, 1991) + Stenolae600R (Waeschenbach et al. 2009) and 19 Stenolae600F (Waeschenbach et al., 2009) + 18p (Hillis & Dixon, 1991) (for PCR 20 21 cycling conditions, primer sequences and additional sequencing primer details, see 22 Waeschenbach et al., 2009). PCR products were purified using QIAquick PCR 23 24 purification Kit (QIAGEN). Sequencing was carried out on an Applied Biosystems 25 3730 DNA Analyser, using Big Dye version 1.1. Sequence identity was checked 26 27 using the Basic Local Alignment Search Tool (BLAST) (www.ncbi.nih.gov/BLAST/). 28 Contigs were assembled using SEQUENCHER 4.8 (GeneCodes Corporation). 29 30 Newly generated lsrDNA and ssrDNA sequences were aligned by eye to an 31 existing alignment, as published in the supplementary data for Waeschenbach et al. 32 33 (2009; see this reference for
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