The New Systematics of Scleractinia: 2 Integrating Molecular 4 3 and Morphological Evidence
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1 The New Systematics of Scleractinia: 2 Integrating Molecular 4 3 and Morphological Evidence 4 Marcelo V. Kitahara, Hironobu Fukami, 5 Francesca Benzoni, and Danwei Huang 6 Abstract 7 The taxonomy of scleractinian corals has traditionally been established based on morphol- 8 ogy at the “macro” scale since the time of Carl Linnaeus. Taxa described using macromor- 9 phology are useful for classifying the myriad of growth forms, yet new molecular and 10 small-scale morphological data have challenged the natural historicity of many familiar 11 groups, motivating multiple revisions at every taxonomic level. In this synthesis of sclerac- 12 tinian phylogenetics and systematics, we present the most current state of affairs in the field 13 covering both zooxanthellate and azooxanthellate taxa, focusing on the progress of our 14 phylogenetic understanding of this ecologically-significant clade, which today is supported 15 by rich sets of molecular and morphological data. It is worth noting that when DNA 16 sequence data was first used to investigate coral evolution in the 1990s, there was no con- 17 certed effort to use phylogenetic information to delineate problematic taxa. In the last 18 decade, however, the incompatibility of coral taxonomy with their evolutionary history has 19 become much clearer, as molecular analyses for corals have been improved upon techni- 20 cally and expanded to all major scleractinian clades, shallow and deep. We describe these 21 methodological developments and summarise new taxonomic revisions based on robust 22 inferences of the coral tree of life. Despite these efforts, there are still unresolved sections 23 of the scleractinian phylogeny, resulting in uncertain taxonomy for several taxa. We high- 24 light these and propose a way forward for the taxonomy of corals. 25 Keywords 26 Azooxanthellate • Cnidaria • Coral • Integrative taxonomy • Phylogenetics • Reef • Species 27 boundaries • Zooxanthellae M.V. Kitahara Departamento de Ciências do Mar, Universidade Federal de São Paulo, Campus Baixada Santista, Av. Alm. Saldanha da Gama, 89, Ponta da Praia, 11030-400 Santos, SP, Brazil Centro de Biologia Marinha, Universidade de São Paulo, F. Benzoni Rod. Manoel Hyppólito do Rego km 131,5, Praia do Cabelo Department of Biotechnology and Biosciences, University of Gordo, São Sebastião/SP 11600-000, Brazil Milano-Bicocca, Piazza della Scienza 2, 20126 Milan, Italy e-mail: [email protected] e-mail: [email protected] H. Fukami D. Huang (*) Department of Marine Biology and Environmental Science, Department of Biological Sciences and Tropical Marine Science Faculty of Agriculture, University of Miyazaki, Institute, National University of Singapore, 1-1 Gakuen-kibanadai Nishi, Miyazaki 889-2192, Japan 14 Science Drive 4, Singapore 117543, Singapore e-mail: [email protected] e-mail: [email protected] © Springer International Publishing Switzerland 2016 41 S. Goffredo, Z. Dubinsky (eds.), The Cnidaria, Past, Present and Future, DOI 10.1007/978-3-319-31305-4_4 42 M.V. Kitahara et al. 28 4.1 Introduction describe recent taxonomic research at family, genus and spe- 79 cies levels. Finally we conclude by highlighting taxonomic 80 29 Stony corals belonging to the order Scleractinia (Anthozoa: issues that remain unresolved in the hope that research efforts 81 30 Hexacorallia) are a clade of cnidarians that build a calcium will be refocused to stabilise all of the problematic taxa. 82 31 carbonate skeleton in the form of aragonite, and are sister 32 group to the non-stony corallimorpharians (Daly et al. 2003; 33 Fukami et al. 2008; Kitahara et al. 2014; Lin et al. 2014). At 4.2 The Rise of Molecular Phylogenetic 83 34 present, Scleractinia contains 31 families, about 240 genera, Methods 84 35 and over 1,500 species (Cairns 1999, 2009; Appeltans et al. 36 2012; Huang and Roy 2015), including both zooxanthel- Genetic data have been collected from scleractinian corals 85 37 late—hosting the symbiotic dinoflagallate Symbiodinium— since the early 1980s, but these were first based on allozyme 86 38 and azooxanthellate corals. Zooxanthellate species typically allelic frequencies obtained using gel electrophoresis 87 39 inhabit shallow waters surrounding warm-subtropical and (Ridgway 2005). Stoddart (1983, 1984) examined the genetic 88 40 tropical seas and comprise the main coral reef framework diversity of Pocillopora damicornis using up to ten enzymes, 89 41 builders with about 800 valid species. Azooxanthellate spe- and found that populations from Western Australia and 90 42 cies are widely distributed in the world’s oceans from shal- Hawaii were maintained predominantly via asexual repro- 91 43 low to deep waters and consist of about 700 valid species. duction. Willis and Ayre (1985) analysed eight enzyme loci 92 44 Neither zooxanthellate and azooxanthellate nor shallow and from Great Barrier Reef Pavona cactus to show that geneti- 93 45 deep species are distinguished phylogenetically and only par- cally similar colonies tended to show the same growth form, 94 46 tially separated at the family level taxonomically. Due to the and overall the species comprised highly clonal populations 95 47 ecological and economic importance of tropical coral reefs— (Ayre and Willis 1988). Allozyme electrophoresis was also 96 48 e.g., high species diversity and mass fisheries production— employed to clarify genetic boundaries of closely-related 97 49 zooxanthellate taxa have been the subject of a greater volume morphotypes, such as between Montipora species (Heyward 98 50 of research relative to azooxanthellate species. However, and Stoddart 1985), M. digitata populations (Stobart and 99 51 both groups have comparable richness, having diversified Benzie 1994), within the Orbicella (previously 100 52 successfully over hundreds of millions of years. Therefore in “Montastraea”) annularis species complex (Knowlton et al. 101 53 this chapter on coral systematics, they deserve equal atten- 1992; van Veghel and Bak 1993), and among Platygyra mor- 102 54 tion, limited only by the amount of published data available. phospecies (Miller and Benzie 1997). 103 55 The coral skeleton has been and continues to be the main Another early genotyping method was restriction frag- 104 56 source of morphological characters used in scleractinian ment length polymorphism (RFLP), which hybridised 105 57 classification. Most coral species are colonial, but solitary digested DNA fragments to probes for determining their 106 58 corals have evolved in at least six lineages independently lengths, or to genomic DNA of known species to establish 107 59 (Barbeitos et al. 2010). Among colonial species, each coral- identity. McMillan and Miller (1988) used RFLP to distin- 108 60 lite (skeletal unit formed by an individual polyp) within a guish the morphologically confusing corals, Acropora 109 61 colony or species may have varying characteristics depend- formosa (= A. muricata) and A. “nobilis” (= A. intermedia; 110 62 ing on growth rate, position in the colony and other see Veron and Wallace 1984). 111 63 environmentally-influenced traits. Consequently, morpho- The first set of scleractinian DNA sequence data to be 112 64 logical boundaries between species are generally obscure, published comprised highly repetitive sequences of 118 bp 113 65 and the task of identifying corals falling within and outside each, otherwise known as minisatellites, cloned from 114 66 the limited pool of systematists has remained challenging at Acropora muricata and A. latistella (McMillan and Miller 115 67 every taxonomic level since Linnaeus (1758) established 1989). Five more species were sequenced for these repeats in 116 68 Madrepora. a follow-up study, in which a maximum parsimony analysis 117 69 Fortunately, molecular phylogenetic analyses in the last did not support most of the morphological subgroups 118 70 two decades have undoubtedly advanced coral taxonomy by (McMillan et al. 1991). 119 71 making large amounts of data available and inspiring the The use of polymerase chain reaction (PCR), an essential 120 72 next generation of systematists. Understandably, the numer- technique of today, began for corals with the amplification of 121 73 ous name changes across the entire coral phylogeny that nuclear 28S ribosomal DNA (rDNA) that was then sequenced 122 74 have ensued can cause considerable confusion for coral for reconstructing the phylogeny of Anthozoa (Chen et al. 123 75 researchers outside the limited circle of systematists. To 1995). This analysis included nine species of scleractinian 124 76 address this apparent disarray, we track the history of molec- corals, and two families tested with more than one species 125 77 ular data used for phylogenetic reconstruction, summarise each were recovered as clades. In a subsequent analysis that 126 78 the most recent phylogenetic understanding of corals, and focused on Scleractinia, Veron et al. (1996) added six species 127 4 The New Systematics of Scleractinia: Integrating Molecular and Morphological Evidence 43 128 with improved representation from Fungiidae and Poritidae, their utility for inferring phylogenies, but they continue to be 180 129 which were found to be monophyletic. the main workhorse for population genetic studies. 181 130 At about the same time, the mitochondrial 16S rDNA was The first multi-species evolutionary trees of Scleractinia 182 131 sequenced from 34 species to reconstruct a larger scleractin- were reconstructed on the basis of the mitochondrial 16S 183 132 ian phylogeny (Romano