Skip to main content
NCBI home page
Zoological Studies logoLink to Zoological Studies
. 2017 May 4;56:e9. doi: 10.6620/ZS.2017.56-09

Loss and Gain of Group I Introns in the Mitochondrial Cox1 Gene of the Scleractinia (Cnidaria; Anthozoa)

Yaoyang Chuang 1,2, Marcelo Kitahara 3,4, Hironobu Fukami 5, Dianne Tracey 6, David J Miller 3,7,*, Chaolun Allen Chen 1,2,8,*
PMCID: PMC6517707  PMID: 31966208

Abstract

Yaoyang Chuang, Marcelo Kitahara, Hironobu Fukami, Dianne Tracey, David J. Miller, and Chaolun Allen Chen (2017) Group I introns encoding a homing endonuclease gene (HEG) that is potentially capable of sponsoring mobility are present in the cytochrome oxidase subunit 1 (cox1) gene of some Hexacorallia, including a number of scleractinians assigned to the “robust” coral clade. In an e ort to infer the evolutionary history of this cox1 group I intron, DNA sequences were determined for 12 representative “basal” and “complex” corals and for 11 members of the Corallimorpharia, a sister order of the Scleractinia. Comparisons of insertion sites, secondary structures, and amino acid sequences of the HEG implied a common origin for cox1 introns of corallimorpharians, and basal and complex corals, but cox1 introns of robust corals were highly divergent, most likely reflecting independent acquisition. Phylogenetic analyses with a calibrated molecular clock suggested that cox1 introns of scleractinians and corallimorpharians have persisted at the same insertion site as that in the common ancestor 552 million years ago (mya). This ancestral intron was probably lost in complex corals around 213 to 190 mya at the junction between the Trassic and Jurassic. The coral cox1 gene remained intronless until new introns, probably from sponges or fungi, reinvaded different positions of the cox1 gene in robust corals around 135 mya in the Cretaceous, and then it subsequently began to lose them around 65.5 mya in some robust coral lineages coincident with the later Maastrichtian extinction at the Cretaceous-Tertiary boundary.

Keywords: Group I intron, Cytochrome oxidase I, Scleractinian, Corallimorpharian, Mass extinction

BACKGROUND

While mitochondrial genomes of anthozoan cnidarians resemble those of other animals in a number of respects, they are unique among metazoans in typically containing one or more self-splicing group I introns (Beagley et al. 1996). NADH dehydrogenase subunit 5 (nad5) genes of all anthozoans so far examined contain a large group I intron that may be the result of a single transfer event (Beagley et al. 1998; Boore 1999; Fukami and Knowlton 2005; Lavrov and Lang 2005; Medina et al. 2006; Tseng et al. 2005; van Oppen et al. 2002). However, in some but not all anthozoans, a second group I intron is present in the cytochrome c oxidase subunit 1 (cox1) gene (Lin et al. 2011; Medina et al. 2006). The cox1 intron differs from that in the nad5 gene in that the former encodes an LAGLI-DADG family homing endonuclease (HE) that is potentially capable of mobilizing the intron (Beagley et al. 1996; Fukami et al. 2007), whereas the latter does not. Group I introns containing an HE gene (HEG) can create a double-strand break at specific nucleotide sequences and invade themselves or with introns, invade other genes (Belfort 1990; Dujon 1989; Perlman and Butow 1989). A homing cyclical model of parasitic genetic elements describes the life cycle of these elements and their strategies to avoid purifying selection (Goddard and Burt 1999; Gogarten and Hilario 2006). The distribution of introns in the mitochondrial cox1 genes of anthozoans is extremely patchy -- for example, introns are present in 13 of 41 genera (20 of 73 species) of “robust” corals, conventionally assigned to the suborder Faviina. With one exception, phylogenies of the robust coral cox1 gene and its intron are concordant, suggesting at most 2 insertions and many subsequent losses (Beagley et al. 1996; Fukami et al. 2007).

The source(s)/donor(s) of introns in anthozoan cox1 genes are unclear. Beagley et al. (1996) suggested a common origin from a symbiotic dinoflagellate (genus Symbiodinium) or endolithic fungus living in close association with corals (Bentis et al. 2000; Raghukumar and Raghukumar 1991). In contrast, a separate origin (from a sponge or fungal donor) was proposed for cox1 group I introns in the suborder Faviina, the major group of “robust” corals (Fukami et al. 2007). While the hypothesis of 2 insertions and many subsequent losses accounts for the limited available data on anthozoan cox1 introns, the extent to which it is more generally applicable remains to be tested, as data are available for few members of the “basal” and “complex” lineages of scleractinians or their sister group, the corallimorpharians (Fukami et al. 2008; Kitahara et al. 2010; Lin et al. 2014; Medina et al. 2006). Corallimorpharians, a small order of Anthozoa composed of 40-45 species, are morphologically similar to scleractinians but lack a calcareous skeleton, and understanding their evolutionary relationship with corals has been a challenging endeavor for decades (Fukami et al. 2008; Kitahara et al. 2010; Kitahara et al. 2014; Lin et al. 2014; Medina et al. 2006). However, recent study based on 291 orthologous single copy protein-coding nuclear genes reveals a topology consistent with scleractinian monophyly and corallimorpharians as the sister clade of scleractinians (Lin et al. 2016)

To better understand the evolutionary history of group I introns, cox1 intron data were obtained for 12 species of Scleractinia, from 7 genera representing 6 families in the “complex” and “basal” clades (Fukami et al. 2008; Kitahara et al. 2010), and from 11 species of Corallimorpharia, including 8 genera representing 3 families. Analyses of insertion sites, primary DNA sequences, and secondary structures, together with comparisons of inferred phylogenies for introns and their host cox1 genes, were consistent with a common origin for cox1 introns of corallimorpharians, actiniarians, anthipatharians, and some basal and complex scleractinians, but also the loss of this intron and subsequent reinvasion of the cox1 locus by distinct group I introns in robust corals.

MATERIALS AND METHODS

Cox1 exon and group I intron sequences

Samples and sources of cox1 sequences used in this study are summarized in table 1. Samples were assigned to groups of corallimorpharians, and “basal”, “complex”, and “robust” scleractinian corals based on Fukami et al. (2008) and Kitahara et al. (Fukami et al. 2008; Kitahara et al. 2010). In addition, cox1 genes belonging to sponges (Porifera) and other anthozoans were included in the molecular evolution analyses. Total genomic DNA was extracted using the CHAOS buffer method (Fukami et al. 2004). A primer set (COX1COMF: 5’-GGT ACG TTA TAT TTA GTA TTT GGG ATT GG-3’ and COX1COMR: 5’-GGA GGA GAA ACA TGA ACC CAT TCT AAG-3’) was designed to amplify complete cox1 exon fragments. A polymerase chain reaction (PCR) was performed with the following thermal cycle: 5 min at 95°C, followed by 5 cycles of 30 s at 94°C, 30 s at 50°C, and 90 s at 72°C, and then by 30 cycles as just described but with an annealing temperature of 55°C instead of 50°C, with a final extension at 72°C for 10 min. An internal primer set (CO1in-F: 5’-CCA TGC TTT TAA CGG ATA GAA ATT-3’ and CO1in-R: 5’-GCA CAT AAT GAA AAT GGG CTA CAA-3’) was designed to assist DNA sequencing if an intron existed.

Table 1. Sequence information in this study. Information includes the name, location, whether or not it contains an intron, the NCBI accession number, and the referenceDistribution of valid species of Microphysogobio from China.

Species Location cox1 intron NCBI Accession
Porifera Cinachyrella levantinensis Israel + AM076987
Plakortis angulospiculatus Florida + EU237487
Octocorallia Acanella eburnea New England - NC_011016
Briareum asbestinum Florida - DQ640649
Dendronephthya gigantea Korea - NC_013573
Keratoisidinae sp. New England - NC_010764
Pseudopterogorgia bipinnata Florida - DQ640646
Zoanthidea Palythoa sp. Florida + DQ640650
Savalia savaglia France + NC_008827
Ceriantharia Ceriantheopsis americana Florida - DQ662399
Antipatharia Chrysopathes formosa California - NC_008411
Leiopathes glaberrima Greece + FJ597644
Actiniaria Metridium senile California + NC_000933
Nematostella sp. Florida - NC_008164
Corallimorpharia Amplexidiscus fenestrafer Taiwan + KP938435
Corallimorphus profundus Taiwan + KP938440
Corynactis califirnica Hawaii + KP938436
Discosoma nummiformis Taiwan + KP938434
Discosoma sp. Bali + NC_008072
Pseudocorynactis sp. Hawaii + KP938437
Rhodactis indosinesis Taiwan + KP938438
Rhodactis mussoides Taiwan + KP938439
Rhodactis sp. Bali + DQ640647
Ricordea florida Florida + NC_008159
Ricordea yuma Taiwan + KP938441
Scleractinia Basal Gardineria hawaiiensis New Caledonia + GQ868677
Complex Acropora tenuis Australia - NC_003522
Agaricia humilis Florida - NC_008160
Alveopora sp. Taiwan - KJ634271
Anacropora matthai Indonesia - NC_006898
Astreopora explanata Taiwan - NC_024090
Astreopora myriophthalma Taiwan - NC_024092
Dendrophyllia sp. Japan + KY887482
Euphyllia sp. Taiwan - KY887483
Fungiacyathus stephanus Taiwan + JF825138
Galaxea sp. Taiwan - KY887484
Goniopora columna Taiwan + JF825141
Goniopora sp. Taiwan + KY887485
Isopora palifera Indonesia - KJ634270
Isopora togianensis Indonesia - NC_024089
Leptoseris cucullata Panama - AB441221
Montipora cactus Taiwan - NC_006902
Pachyseris sp. Taiwan - KY888878
Pavona clavus Panama - NC_008165
Porites compressa Taiwan + KY888879
Porites okinawanesis Japan + JF825142
Porites porites Florida + NC_008166
Siderastrea radians Florida + NC_008167
Pseudosiderastrea formosa Taiwan + NC_026530
Stephanocoenia michelinii Panama + AB441228
Tubastrea sp. Taiwan + AB441238
Robust Acanthastrea echinata Taiwan - AB117250
Anthemiphyllia patera New Caledonia HM018604
Astrangia sp. Florida DQ643832
Blastomussa wellsi Palau + AB289563
Caulastraea furcata Japan + AB289579
Cynarina lacrymalis Pacific + AB289568
Cyphastrea serailia Japan - AB117257
Deltocyathus suluensis Australia HM018631
Diploastrea heliopora Japan + AB289567
Diploria clivosa Panama - AB117226
Echinophyllia aspera Japan + AB289572
Echinophyllia echinoporoides Palau + AB289573
Echinopora pacificus Japan - AB117261
Favia fragum Brazil - AB117223
Favia stelligera Japan - AB117264
Hydnophora grandis Palau - AB117286
Lobophyllia corymbosa Japan + AB117241
Madracis mirabilis Panama - EU400212
Madrepora oculata Taiwan - JX236041
Meandrina braziliensis Brazil - AB117297
Montastraea annularis Panama - AB117260
Montastraea cavernosa Panama - AB117288
Montastraea magnistellata Japan - AB117279
Mussismilia harttii Brazil - AB117232
Mycedium elephantotus Palau + AB289582
Mycetophyllia aliciae Panama - AB117235
Oulastrea crispata Taiwan - AB441197
Oulophyllia bennettae Palau + AB289581
Oxypora lacera Palau + AB289571
Paulastrea sp. Taiwan - KY887486
Pectinia paeonia Palau + AB289584
Physogyra lichtensteini Palau + AB289562
Platygyra lamellina Japan - AB117282
Pocillopora eydouxi Taiwan - KY887487
Polycyathus chaishanensis Taiwan - NC_015642
Scolymia cubensis Brazil - AB117237
Scolymia sp. Palau + AB289570
Scolymia vitiensis Palau + AB289569
Seriatopora caliendrum Taiwan - NC_010245
Seriatopora hystrix Taiwan - NC_010244
Solenastrea bournoni Panama - AB117291
Stylocoeniella sp. Japan - AB441225
Stylophora pistillata Taiwan - NC_011162
Symphyllia radians Japan + AB289578
Trachyphyllia geoffroyi Florida - AB117287
Open in a new tab

Sequence analysis, open reading frame (ORF), and secondary structure prediction of cox1 group I introns

In order to examine the characteristics and origins of group I introns in scleractinians and corallimorpharians, cox1 exons and introns of other anthozoan orders (including the Zoantharia, Actiniaria, and Antipatharia) and Porifera, and of Cinachyrella levantinensis and Plakortis angulospiculatus, were retrieved from GenBank. In total, 94 cox1 sequences with 42 containing group I introns were used for the following analyses. Sequence alignment of cox1 exons and putative ORFs were performed using MEGA 5.05 and Gblocks (Talavera and Castresana 2007; Tamura et al. 2007). ORFs were translated in Vector NTI using the Acropora tenuis genetic code to detect ORFs of longer than 100 amino acids in the intron (van Oppen et al. 1999). Secondary structures of group I introns were estimated using the DNA Mfold server (http://mfold.bioinfo.rpi.edu/; (Zuker 2003) and our current understanding of the group I intron recognition process (Lisacek et al. 1994). Numbers of nonsynonymous substitutions (Ka) and synonymous substitutions (Ks) were calculated using DnaSP vers. 5 software to estimate the selection forces on exon and intron sequences (Librado and Rozas 2009).

Phylogeny construction and comparisons

All cox1 exon sequences used to reconstruct the phylogenetic relationship of scleractinian corals and the relative anthozoan taxa were listed in table 1. The best-fitting models in the maximum- likelihood (ML) analyses were evaluated using ModelTest vers. 3.7 (Posada and Crandall 1998). A general time-reversible substitution model with a proportion of invariance and gamma distribution model (GTR+I+G) of a DNA evolution model were determined using the Akaike Information Criterion (AIC) test for the ML analysis. The ML analysis with Shimodaira and Hasegawa (SH)- like branch support (Guindon et al. 2010) was conducted using the PhyML 3.0 online server. The Bayesian (BA) phylogeny was constructed using Mrbayes (Ronquist and Huelsenbeck 2003) with a substitution model evaluated with Mrmodeltest ver. 3.7 (Nylander 2004). The Bayesian tree was constructed with 6 simultaneous Markov chains for 107 generations with trees sampled every 1000 generations and 2500 initial trees discarded as burn-in.

In order to test the consistency of cox1 exon and intron evolution, phylogenetic analyses of co- speciation comparisons between exons and introns were reconstructed with the ML and BA algorithms. Phylogenetic relationships of corallimorpharians, and the basal, complex, and robust clades of scleractinians were separately estimated because of the di culty of aligning HEG sequences among basal, complex, and robust corals. The GTR+G model was determined using the AIC test for the cox1 exon and the HEG of corallimorpharians and the basal and complex corals, while the Hasegawa, Kishino, and Yano and gamma distribution (HKY+G) model and GTR+I were determined for the cox1 exon and HEG of robust corals.
Patristic distance correlations between exon and intron phylogenies were estimated using Mesquite vers. 2.75 to compare the similarity of tree topologies of exons and HEGs (Maddison 2011). The Kishino-Hasegawa (KH) test, Shimodaira-Hasegawa (SH) test, and Approximately Unbiased (AU) test were conducted in the Consel program to estimate the con dence level of topological differences (Shimodaira and Hasegawa 2001).

Molecular dating of the cox1 exon tree

The divergence time of every clade was calculated using Beast vers. 1.6.1 which allows a relaxed molecular clock among different lineages (Drummond and Rambaut 2007). The Yule birthrate process was chosen as prior, and the distribution of the divergence on each node was set to a normal distribution with a 5% standard error. The GTR+I+G model was selected as the most appropriate evolutionary model to evaluate likelihood ratio tests for molecular clock estimates. In total, 5 × 108 generations were performed and saved every 5 × 104 generations to calculate their phylogenetic relationships. The first 2500 of 104 topologies were discarded as burnin, while the remainder was saved to calculate posterior probabilities. Four reference points were chosen to evaluate the divergence time of each clade. Time of reference points were as follow: Dendrophylliidae (127 million years ago, mya), Acropora (59 mya), Stylophora (68 mya; (Baron- Szabo 2006), and Astrangia/Solenastrea (70 mya). In order to avoid over-evaluation of time, we constrained the origin of scleractinians to 460 mya (Stolarski et al. 2011).

RESULTS

Molecular characteristics of group I introns in cox1 loci

Lengths of introns, putative open reading frames (ORFs), noncoding regions, locations and start/stop codons of ORFs in scleractinians, corallimorpharians, and other members of the Anthozoa and Porifera are summarized in table 2. Eleven species, representing 8 genera in 3 families of corallimorpharians all contained the cox1 intron. Among scleractinian corals, the “basal” coral, Garderneria hawawiiensis, and 11 “complex” coral species, representing 7 genera of 6 families, had introns inserted at the same nucleotide position (nt) 893 in cox1 (herein called I893) as those of corallimorpharians, actinarians, and antipatharians (Table 3). In “robust” corals, 15 species, representing 13 genera of 4 families, had introns inserted at nt position 729 in cox1 (herein called I729), which is identical to the insertion position of sponges (Table 3). In zoanthids, cox1 introns were inserted at nt position 876 (herein called I876).

Lengths of introns and ORFs ranged from 853/672 bp in the actiniarian, Metridinum senile, to 1503/1039 bp in the sponge, Plakortis angulospiculatus (Table 2). Intron and ORF lengths of “complex” corals were signi cantly shorter than those of “robust” corals (Mann-Whitney U-test p < 0.01) but no significantly different between complex corals and corallimorpharians (Mann- Whitney U-test, p = 0.09). Start and stop codons of the cox1 intron ORF were ATA and TAA, respectively, for most corallimorpharians and scleractinians, except those of Ricordea yuma (start codon = GTG) and Stephenoconia sp. (stop codon = TAG). An ORF composed of a specific domain of the LAGLI-DADG HE was identified, although nucleotide sequence alignments among different anthozoans were low. As observed by Fukami et al. (2007), amino acid sequences of the HE in robust corals were highly similar to those of sponges (mean p-distance = 22.2%, Table 4) (Fukami et al. 2007). However, they were highly divergent compared to those of basal, complex, and corallimorpharians (mean p-distance = 83.8%), whereas the latter three possessed relatively similar HEs (mean p-distance = 43.2%).

Secondary structures of the cox1 intron for sponges and 7 anthozoans were predicted to confirm its identification in group I based on the consensus primary structure (Fig. 1). All cox1 introns contained 4 consensus primary structures (P, Q, R, and S) in core structures of group I intron and 9 or 10 paired regions of helices. Paired regions of the secondary structure also reflected the relationship based on primary sequences of introns. For example, I729 of both robust corals and the sponge had lost the P2 helix (Figs. 1A, B). Structures and positions of P1 to P9 were highly similar among I893s of basal and complex corals and corallimorpharians except for the P5 region (Figs. 1C, D). I893s of antipatharians and actiniarians possessed similar secondary structures to corallimorpharians (Fig. 1E), whereas I876 of zoanthiarians had a branched form of the P9.1 paired region representing a unique type of cox1 intron compared to other anthozoans (Fig. 1F).

Table 2. Molecular characteristics of cox1 introns and their open reading frames (ORFs), including the length of the intron, length of the ORF, length of the non-coding region, location of the ORF in the cox1 intron, and its start/stop codon according to predictions from Kitahara et al. (2014) and Lin et al. (2014) .

Taxon Length of Intron Length of ORF Length of Noncoding Location of ORF Start/Stop Codon
Porifera
Cinachyrella levantinensis 1143 1029 114 1-1029 TTA/TAA
Plakortis angulospiculatus 1503 1038 195 359-1396 TTT/TAA
Zoanthidea
Palythoa sp. 1308 747 561 391-1137 ATG/TAA
Savalia savaglia 1250 723 527 441-1163 ATG/TAG
Actiniaria
Metridium senile 853 672 181 155-826 ATG/TAA
Corallimorpharia
Amplexidiscus fenestrafer 1206 1005 201 71-1075 ATA/TAA
Corallimorphus profundus 1182 786 396 47-832 ATA/TAG
Corynactis califirnica 1265 1008 257 71-1078 ATA/TAG
Discosoma nummiformis 1208 711 497 71-781 ATA/TAA
Discosoma sp. 1206 1005 201 71-1075 ATA/TAA
Pseudocorynactis sp. 1177 993 184 71-1063 ATA/TAA
Rhodactis indosinesis 1204 726 478 71-796 ATA/TAA
Rhodactis mussoides 1206 1005 201 71-1075 ATA/TAA
Rhodactis sp. 1206 1029 177 71-1075 ATA/TAA
Ricordea florida 1215 1017 198 90-1106 ATA/TAA
Ricordea yuma 1198 975 223 110-1084 GTG/TAA
Scleractinia (Basal complex group)
Gardineria hawaiiensis 1140 981 159 48-1028 ATA/TAA
Scleractinia (Complex group)
Dendrophyllia sp. 972 831 141 49-879 ATA/TAA
Fungiacyathus stephanus 970 828 142 48-875 ATA/TAA
Goniopora sp. 970 831 139 48-878 ATA/TAA
Porites porites 971 831 140 48-878 ATA/TAA
Porites compressa 970 831 139 48-878 ATA/TAA
Siderastrea radians 994 855 139 48-902 ATA/TAA
Pseudosiderastrea formosa 970 855 115 48-902 ATA/TAA
Stephanocoenia michelinii 940 792 148 47-838 ATA/TAG
Tubastrea sp. 970 831 139 48-878 ATA/TAA
Scleractinia (robust group)
Blastomussa wellsi 1107 933 174 49-981 ATA/TAA
Caulastraea furcata 1128 1005 123 27-1031 ATA/TAA
Cynarina lacrymalis 1078 933 145 49-981 ATA/TAA
Diploastrea heliopora 1076 933 143 49-981 ATA/TAA
Echinophyllia aspera 1077 954 123 27-980 ATA/TAA
Echinophyllia echinoporoides 1077 954 123 27-980 ATA/TAA
Lobophyllia corymbosa 1077 954 123 27-980 ATA/TAA
Mycedium elephantotus 1128 1005 123 27-1031 ATA/TAA
Oulophyllia bennettae 1128 1005 123 27-1031 ATA/TAA
Oxypora lacera 1078 933 145 49-981 ATA/TAA
Pectinia paeonia 1128 1005 123 27-1031 ATA/TAA
Physogyra lichtensteini 1077 933 144 49-981 ATA/TAA
Scolymia sp. 1120 996 124 27-1022 ATA/TAA
Scolymia vitiensis 1078 933 145 49-981 ATA/TAA
Symphyllia radians 1077 954 123 27-980 ATA/TAA
Open in a new tab

Table 3. Insertion sites of the cox1 intron in different groups of anthozoans and a sponge. Double arrows indicate insertion sites of the intron indicate insertion sites of the intron.

Taxa Sequence type
Location  729            876    893
Zoanthidea
Palythoa sp. GCCAT CCGGAGGTTT [149 nt] I876
TGTGTGGGCT→←CACCACATGTTTACAGT - AGGGA
Savalia savaglia GCCAT CCGGAGGTTT [149 nt] I876
TGTGTGGGCT→←CACCACATGTTTACAGT - AGGGA
Actiniaria
Metridium senile GGCAT CCGGAAGTTT [149 nt] I893
TGTGTGGGCA CATCACATGTTTACGGT→←TGGAA
Antipatharia
Leiopathes glaberrima GCCAC CCAGAGGTTT [149 nt] I893
TGTGTGGGCT CATCACATGTTCACGGT→←TGGAA
Corallimorpharia
Ricordea florida GACAT CCAGAGGTAT [149 nt] I893
TGTGTGGGCA CACCATATGTTTACGGT→←TGGAA
Scleractinia
Gardineria hawaiiensis GGCAT CCCGAAGTTT [149 nt] I893
TGGGTGGGCC CATCATATGTTTACGGT→←TGGAA
Siderastrea radians GGCAT CCAGAAGTTT [149 nt] I893
TGTGTGGGCC CACCATATGTTTACGGT→←TGGGA
Diploastrea heliopora GGCAT→←CCTGAAGTTT ~ I729
Sponge
Cinachyrella levantinensis GGCAT→←CCAGAAGTTT [149 nt] I792
AGTTTGAGCC CATCACATGTTTACAGT TGGAA
Open in a new tab

Table 4. Genetic distances of the homing endonuclease gene (HEG) among different organisms. P-distance comparisons of HEG amino acid sequences among different groups of organisms. Distances are listed as percentages (%). nc, not comparedDistribution of valid species of Microphysogobio from China.

Group Basal and complex corals Robust corals Corallimorpharians Actiniarians Sponges
Basal and complex corals 20.6
Robust corals 82.6 6.9
Corallimorpharians 43.2 81.5 2.1
Actiniarians 66.0 82.4 65.1 nc
Sponges 83.8 22.2 81.2 83.3 19.2
Open in a new tab

Fig. 1.

Fig. 1.

Open in a new tab

Fig. 1. Secondary structures of representative cox1 introns in anthozoans. A: Corallimorpharian (Rhodactis howesii); B: basal and complex corals (Gardeneris hawaiinesis); C: robust corals (Diploastrea heliopora); D: actiniarian (Metridinium senile); E: poriferian (Plakortis angulospiculatus); F: zoantharian (Savalia savaglia). Features of the secondary structure indicate the characteristics of group I introns: 10 helical elements P1~P10; consensus primary structures P, Q, R, and S in hollow letters; internal guide sequence, IGS. Initial and terminal sites of the predicted open reading frame are labeled “ORF start” and “ORF stop”, respectively.

Evolutionary rates of the exon and HEG

To evaluate selection forces on the exon and HEG of the intron, we estimated the rate of nonsynonymous substitutions (Ka) versus synonymous substitutions (Ks) in exons and HEGs of corallimorpharians, complex corals, and robust corals. Similar small ratios were observed among cox1 exons of corallimorpharians and scleractinians, while larger differences were found in comparisons of HEGs among corallimorpharians and scleratinians (Fig. 2, Ka/Ks = 0.03-0.045 on average for cox1 exons; Ka/Ks = 0.254-0.489 on average for HEGs). Both the cox1 exon and HEG deviated from neutral variations (Ka/Ks = 1). A lower nonsynonymous ratio of substitutions for the cox1 exon suggested that more-puri ed selection of the cox1 exon was stronger than that of the HEG.

Fig. 2.

Fig. 2.

Open in a new tab

Fig. 2. Ka/Ks comparisons in cox1 exons and introns among corallimorpharians, complex corals, and robust corals. Values behind the each line show average values in each group, indicating the level of selective forces on each group.

Co-evolution of the cox1 exon and intron in scleractinians and corallimorpharians

Results of the phylogenetic analyses are summarized in figure 3. Octocorals were used as outgroups for the phylogenetic analyses because of the sister group relationship between hexacorallians and octocorallians. Both the ML and BA analyses strongly supported the monophyly of the Scleractinia composed of “basal”, “complex”, and “robust” clades as proposed by Kitahara et al. (2010) and Stolarski et al. (2011) Corallimorpharian genera were grouped into a monophyletic clade, except for Corallimorphus profundus which formed a basal clade next to the Scleractinia, although statistical supports of the MA and BA to this node were not relatively high (86/61).

Mapping the occurrence of cox1 introns onto the phylogenetic tree showed that I893 appeared in all genera of the order Corallimorpharia, the basal scleractinian, Gardineria hawaiinensis, and Fungiacyanthus, Porites, Goniopora, Turbinaria, Dendrophyllia, Siderastrea, Pseudosiderastrea and Stephanocoenia of the complex clade of the Order Scleractinia (herein called complex I) (Fig. 3). I893 was absent from the other lineage, complex II, which contained genera of the families Euphyllidae, Acroporidae, and Agaricidae. I729, in contrast to the distributional pattern of I893 in corallimorpharians, and basal and complex coral clades, had a sporadic but restricted distribution in the robust clade of Paci c scleractinian corals (Fig. 3).

Co-evolution tests of cox1 exons and introns were separately conducted for corallimorpharians, basal and complex corals (Fig. 4A), and robust corals (Fig. 4B) due to the high divergence of primary DNA sequences between I893 and I729. cox1 exon and I893 phylogenies were largely congruent in corallimorpharians, and basal and complex corals (Patristic distance correlation = 0.96). The difference was in positions of Corallimorphus profundus and Porites compressa between these 2 trees (Fig. 4A). In contrast, in the case of robust corals, exon and intron phylogenies substantially di ered (Patristic distance correlation = 0.67), suggesting significantly different evolutionary histories for I729 and the cox1 exons in the robust clade (Fig. 4B, Table 5). To test the co-evolution of the exon and intron, the AU, KH, and SH tests were conducted to examine the congruence of the exon and intron phylogenetic trees. Statistical results of the AU, KH and SH tests indicated that tree topologies of the exon and intron signi cantly di ered in robust corals but were consistent in corallimorpharians and complex corals (Table 5).

Table 5. Comparisons of cox1 exon-intron phylogenies. Patristic distance correlations (PDCs) between exon and intron trees were calculated, and the Kishino-Hasegawa (KH), Shimodaira-Hasegawa (SH), and Approximately Unbiased (AU) tests were conducted to estimate the confidence level of topological di erences in Mesquite vers. 2.75. ** p < 0.001 .

Similarity Statistical test between exon and intron phylogenetic trees
PDC AU KH SH
Complex corals and corallimorpharians 0.96 0.243 0.258 0.258
Robust corals 0.67 0.00004** 0.0001** 0.0001**
Open in a new tab

Fig. 3.

Fig. 3.

Open in a new tab

Fig. 3. Phylogeny and characteristics of cox1 intron traits in hexacorals. The tree topology was constructed with Mrbayes. Numbers labeled on branches are Shimodaira-Hasegawa-like support/posterior probabilities. Species with di erent types of introns are labeled with symbols: ●, Intron-729 (I729); ▲, Intron-893 (I893); ■, Intron-876 (I876).

Fig. 4.

Fig. 4.

Open in a new tab

Fig. 4. Comparison of phylogenetic trees between the cox1 exon (left side) and intron (right side) in complex corals and corallimorpharians (A) and in sponges and robust corals (B). Tree topologies presenting the phylogenetic relationships of exons and introns were consensus trees between the maximum-likelihood analysis and Bayesian algorism. Numbers on branches are Shimedaira- Hasegawa-like/posterior probabilities. Dashed lines are potential changes in phylogenetic positions between the exon and intron trees.

Molecular clock estimates for intron loss and gain events

Molecular dating based on the cox1 phylogeny is summarized in figure 5 and table 6. The Corallimorpharia was derived about 552 mya at the end of the Precamrian. The first scleractinian, represented by the “basal” coral, Gar. howaiinesis, was derived from a common ancestor of corallimorpharians around 460 mya. “Complex” and “robust” corals were derived from a common ancestor of basal corals around 423 mya during the end of Silurian, whereas robust corals split from complex corals around 358 mya towards the end of the Devonian and beginning of the Carboniferous. Our results clearly showed that corallimor- pharians and scleractinians shared a single origin for the cox1 intron and subsequently lost and then regained it during evolution by mapping the possession of group I introns onto the Bayesian phylogeny (Fig. 5) and similarities among group I introns (Table 4). I893 already existed in the common ancestor of the corallimorpharian- scleractinian lineage back to 552 mya. All 11 corallimorpharians, ancestors of scleractinians, including both zooxanthellate and azooxanthellate lineages, possess I893. I893 was also observed in the basal coral, Garderneria howawiinensis, and complex I corals. Around 213 to 190 mya at the junction between the Triassic and Jurassic, I893 was lost from complex II corals and most robust corals. I729 independently re-invaded several robust corals later at around 130 mya towards the end of the Cretaceous. The inconsistence between exon and intron phylogenies in Robust corals supported the possibility of multiple insertions of I729 (Fig. 4).

Table 6. Results of divergence time estimates. Information includes the mean, 95% highest posterior density interval (HPD lower-upper), effective sample sizes (ESSs), and the posterior probability of each major clade.

MRCA Event Mean 95% HPD lower-upper ESS Posterior probability
A Origin of corallimorpharians and scleractinians 552.28 473.01-666.97 629 69.24
B Origin of the Gardineria group 460.12 456.14-464.05 4124 98.33
C Origin of scleractinians 423.04 309.73-463.97 281 1
D Origin of robust corals 358.31 378.14-461.46 482.53 1
Intron Loss I893 intron loss 213.02 129.97-290.02 483.26 0.55
Intron Insertion 1stI729 intron insertion 135.38 90.39-186.34 890.99 0.95
Open in a new tab

Fig. 5.

Fig. 5.

Open in a new tab

Fig. 5. Bayesian estimates of divergence times in scleractinians. The basal axis is a geologic time scale in units of million years ago (mya). Different time intervals are labeled with abbreviations (Cam, Cambrian; Ord, Ordovician; Sil, Silurian; Dev, Devonian; Car, Carboniferous; Per, Permian; Tri, Triassic; Jur, Jurassic; Cre, Cretaceous; Pal, Paleogene; Neo, Neogene). The chart below the phylogenetic tree gives the extinction rate (solid line) and origination rate (dashed line) in different geological periods, which were modified from Kiessling (2004) with major extinction events labeled with abbreviations (Rhae, Rhaetian; Plie, Pliensbachian; Kimm, Kimmeridgian; Ceno, Cenomanian; Maa, Maastrichtian, KT-extinction). Species with different types of intron are labeled with symbols: ●, Intron-729 (I729); ▲, Intron-893 (I893); ■, Intron-876 (I876).

DISCUSSION

In this study, cox1 introns were observed in 12 of 23 species belonging to “basal” and “complex” corals, and 11 species of corallimorpharians. Compared to published cox1 introns in “robust” corals, these new cox1 introns suggest that a single origin occurred in the common ancestor of scleractinians and corallimorpharians, and was subsequently lost in complex II corals and most robust corals before re-invasion by new introns from other donor sources, such as sponges or fungi (Fukami et al. 2007).

Evolutionary history of group I introns in scleractinian corals

The “single-origin” scenario of cox1 introns in scleractinians was supported by several aspects: (i) the insertion site in actiniarians, corallimorpharians, and basal and complex corals was the same, but differed from those of robust corals, which have the same insertion site as sponges (Fukami et al. 2007); (ii) amino acid sequence dissimilarities of HEGs among actiniarians, corallimorpharians, and basal and complex corals were significantly lower (0.43-0.66) than those compared to robust corals and sponges (0.812-0.838), whereas the latter two were highly similar (0.222); (iii) secondary structures of cox1 introns were similar among actiniarians, corallimorpharians, and basal and complex corals, but differed from those of robust corals and sponges; and (iv) I893 had an ancestral status in the cox1 gene of all 8 existing corallimorpharian genera and 12 of 14 genera surveyed in actiniarians for over 500 my (Goddard et al. 2006) (Fig. 5). Fukami et al. hypothesized, based on comparisons of intron sequences between the suborder Faviina of robust corals and actiniarians, that both scleractinians and actiniarians independently acquired cox1 group I introns. However, this hypothesis was not supported because key taxa, such as corallimorpharians and basal and complex corals, were not examined by Fukami et al. (Fukami et al. 2007).

Regardless of the details of the history of introns in cox1 genes of corals, the sources of coral introns, and anthozoan introns in general, continue to be debated. Sponge (e.g., Tetilla sp.) or fungal (e.g., Smittium culisetae and Schizosaccharomyces octosporus) cox1 introns were proposed as potential donors to I729 of robust corals based on DNA similarities (Fukami et al. 2007). Whether I729 of robust corals directly invaded from sponges or fungi or indirectly via fungi from sponges or vice versa remains unsettled. In contrast, I893 of actiniarians has the highest similarity compared to the fungus, Neurospora crassa (Dalgaard et al. 1997; Goddard et al. 2006), suggesting that I893 might have come directly from fungi via homing and horizontal transfer events (Goddard et al. 2006). However, the possibility of other donors (e.g., dino agellates) still cannot be excluded because of the complicated symbiotic system in corals (Amend et al. 2012; Baker 2003; Schonberg and Wilkinson 2001).

Our Ka/Ks evolutionary analysis revealed that purifying selection was the predominant force shaping the evolution of cox1 and HEG of introns (Fig. 2). This observation is consistent with previous observations in the Anthozoa (Emblem et al. 2014) of central roles of most mitochondrial (mt)DNA protein products in the fundamental biological process of the mitochondrial electron transport chain function. However, our analysis also demonstrated that the HEG experienced faster rates of molecular evolution as expressed by Ka/Ks ratios and accelerated raw Ka values. Although in ated relative to other genes (such as cox1), calculated HEG Ka/Ks ratios were all < 1, suggesting relaxation of purifying selection rather than positive selection acting on these sequences. Similar findings were also documented in an analysis of actinarian mitochondrial genomes (Emblem et al. 2014).

Results of co-evolutionary comparisons imply that the cox1 intron was stably persistent in the ancestor of corallimorpharians and basal and complex corals, but not that of robust corals. Previous studies also suggested that group I introns had a low rate of lateral invasion in cnidarians (Fukami et al. 2007; Huchon et al. 2010). It was suggested that HEGs were only able to invade actiniarians because of the slow evolutionary rate of mtDNA, and HEGs did not invade other metazoans possibly either due to a lack of opportunity or because metazoans have faster substitution rates, which means that HEGs degenerate more rapidly (Lin et al. 2011; Medina et al. 2006; Shearer et al. 2002). A similar scenario could be used to explain why HEGs could survive in cox1 genes of corallimorpharians and basal and complex corals, but were subsequently lost from robust corals. Although global evolutionary rates of mitochondrial genomes in scleractinians and corallimorpharians are slow compared to those of other metazoans (Shearer et al. 2002), the relative evolutionary rate of the mitochondrial genome in robust corals is higher than those of complex corals and corallimorpharians (Chen et al. 2002; Medina et al. 2006), suggesting that HEGs in the cox1 gene of robust corals will degenerate more rapidly and subsequently be lost compared to those of corallimorpharians and basal and complex corals. Robust corals regained cox1 introns from other source donors which occurred independently in some of their lineages.

Our analysis implies that there should have been another lateral invasion providing an opportunity for I729 to insert itself into the cox1 gene of robust corals. Insertion and loss events seem to have occurred more frequently in robust corals than in corallimorpharians and complex corals. It is obvious that insertion sites of I729 in robust corals all lay between the third base of one codon and the first base of the subsequent codon (phase zero, site 729), while I893 lies on the second and third bases of one codon in basal and complex corals and corallimorpharians (phase two, site 893). Roy and Gilbert (Roy and Gilbert 2005) suggested that phase 0 introns were more likely to be lost than other introns, i.e., introns that do not interrupt a codon would have lower selection risks. This suggests that I729 has been inserted and lost more frequently than I893.

Hypothesis: intron loss and gain might be corroborated with major extinction events

Mapping the occurrence of introns on the cox1 phylogeny of anthozoans suggested that loss and gain of introns in corallimorpharians and scleractinians were corroborated with major extinction events (Fig. 5). I893 was inserted in the common ancestor of hexacorallians some 552 mya, and was maintained in anthipatharians, actiniarians, corallmorpharians, and complex I scleractinians. I893 was lost about 213 mya during the Rhaetian extinction, when about 40% of benthic taxa disappeared towards the end of the Triassic, although the cause of the Rhaetian mass extinction remains controversial (Galli et al. 2005; Marzoli et al. 2004; Olsen et al. 2002). Kiessling et al. suggested that volcanism causing climate changes led to disturbances in the carbon cycle which could have been the reason for this extinction (Kiessling et al. 2007; Kiessling and Baron-Szabo 2004), including inducing high extinction rates among taxa of inshore habitats and reefs (Kiessling and Baron-Szabo 2004). Although re-invasion of I729 into the cox1 gene of robust corals occurred around 135 mya, the later Maastrichtian extinction (K-T extinction) which occurred at 65.5 mya might have triggered loss of I729 from some lineages of robust corals. Interestingly, major loss and invasion events of introns also occurred contemporarily with 2 major mass extinction events in the evolutionary history of scleractinians (Kiessling and Baron- Szabo 2004). These correlations indicate that mass extinctions might have provided cox1 intronless species with a selective advantage of respiration efficiency allowing them to increase their distribution in harsh environments compared to their counterparts with the cox1 intron. A previous study indicated that mobile elements would have led hosts to experience greater selective forces unless they were harmless to their host genes (Domart-Coulon et al. 2001). Although the homing process might have provided a successful way to increase the preservation of invaded elements (Edgell et al. 2011; Gagan et al. 2000), it is believed that introns might decrease the efficiency of gene expression because of the prolonged lengths of their transcripts (Chen et al. 2005; Jeffares et al. 2008). The concentration of atmospheric oxygen rapidly declined from approximately 30% to 13% during the beginning of the Triassic to the Rhaetian extinction (Berner 2001, 2009; Berner et al. 2003; Glasspool and Scott 2010). It is believed that non-essential introns would have imposed costs to a gene by prolonging transcription (Lynch 2002). Cox1 is the catalytic center for reducing oxygen to water in the oxidative phosphorylation of aerobic respiration (Pierron et al. 2012). We speculated that faster transcription e ciency might have provided cox1- intronless corals with a selective advantage under a scenario of declining oxygen concentrations.

Acknowledgments

Acknowledgments: Many thanks go to the New Zealand Institute of Water and Atmosphere Research for providing samples and hosting CAC’s visit. We also thank members of the Coral Reef Evolutionary Ecology and Genetics Group (CREEG), Biodiversity Research Center, Academia Sinica (BRCAS) and anonymous referees for their constructive comments. This study was supported by an Academia Sinica Thematic Grant (2005- 2010) and a National Science Council, Taiwan grant (2006-2011) awarded to CAC. All coral samples were collected with proper permits.

References

  1. Amend A S, Barshis D J, Oliver T A. Coral-associated marine fungi form novel lineages and heterogeneous assemblages. ISME J. 6:1291–1301. doi: 10.1038/ismej.2011.193. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Baker A C. K / T-b o u n dary:Scleractinian corals of the suborders astrocoeniina, faviina, rhipidogyrina and amphiastraeina. Annu Rev Ecol Evol Syst. 34:1–108. [Google Scholar]
  3. Beagley C T, Okada N A, Wolstenholme D R. Two mitochondrial group I introns in a metazoan, the sea anemone Metridium senile: One intron contains genes for subunits 1 and 3 of nadh dehydrogenase. P Natl Acad Sci. 93:5619–5623. doi: 10.1073/pnas.93.11.5619. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Beagley C T, Okimoto R, Wolstenholme D R. The mitochondrial genome of the sea anemone Metridium senile (cnidaria): Introns, a paucity of trna genes, and a near-standard genetic code. Genetics. 148:1091–1108. doi: 10.1093/genetics/148.3.1091. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Belfort M. Phage-t4 introns-self-splicing and mobility. Annu Rev Genet. 24:363–385. doi: 10.1146/annurev.ge.24.120190.002051. [DOI] [PubMed] [Google Scholar]
  6. Bentis C J, Kaufman L, Golubic S. Endolithic fungi in reef-building corals (order: Scleractinia) are common, cosmopolitan, and potentially pathogenic. Biol Bull. 198:254–260. doi: 10.2307/1542528. [DOI] [PubMed] [Google Scholar]
  7. Berner R A. Modeling atmospheric O2 over phanerozoic time. Geochim Cosmochim Acta. 65:685–694. [Google Scholar]
  8. Berner R A. Phanerozoic atmospheric oxygen: New results using the geocarbsulf model. Am J Sci. 309:603–606. [Google Scholar]
  9. Berner R A, Beerling D J, Dudley R, Robinson J M, Wildman R A. Phanerozoic atmospheric oxygen. Annu Rev Earth Planet Sci. 31:105–134. [Google Scholar]
  10. Boore J L. Animal mitochondrial genomes. Nucleic Acids Res. 27:1767–1780. doi: 10.1093/nar/27.8.1767. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Chen C A, Wallace C C, Wolstenholme J. Analysis of the mitochondrial 12s rrna gene supports a two-clade hypothesis of the evolutionary history of scleractinian corals. Mol Phylogenet Evol. 23:137–149. doi: 10.1016/S1055-7903(02)00008-8. [DOI] [PubMed] [Google Scholar]
  12. Chen J J, Sun M, Hurst L D, Carmichael G G, Rowley J D. Human antisense genes have unusually short introns: Evidence for selection for rapid transcription. Trends Genet. 21:203–207. doi: 10.1016/j.tig.2005.02.003. [DOI] [PubMed] [Google Scholar]
  13. Dalgaard J Z, Klar A J, Moser M J, Holley W R, Chatterjee A, Mian I S. Statistical modeling and analysis of the laglidadg family of site-specific endonucleases and identification of an intein that encodes a site-specific endonuclease of the hnh family. Nucleic Acids Res. 25:4626–4638. doi: 10.1093/nar/25.22.4626. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Domart-Coulon I J, Elbert D C, Scully E P, Calimlim P S, Ostrander G K. Aragonite crystallization in primary cell cultures of multicellular isolates from a hard coral, pocillopora damicornis. P Natl Acad Sci. 98:11885–11890. doi: 10.1073/pnas.211439698. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Drummond A J, Rambaut A. Beast: Bayesian evolutionary analysis by sampling trees. Bmc Evol Biol; 2007. 7. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Dujon B. Group-I introns as mobile genetic elements-facts and mechanistic speculations-a review. Gene. 82:91–114. doi: 10.1016/0378-1119(89)90034-6. [DOI] [PubMed] [Google Scholar]
  17. Edgell D R, Chalamcharla V R, Belfort M. Learning to live together: Mutualism between self-splicing introns and their hosts. Bmc Biol; 2011. 9. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Emblem A, Okkenhaug S, Weiss E S, Denver D R, Karlsen B O, Moum T, Johansen S D. Sea anemones possess dynamic mitogenome structures. Mol Phylogenet Evol. 75:184–193. doi: 10.1016/j.ympev.2014.02.016. [DOI] [PubMed] [Google Scholar]
  19. Fukami H, Budd A F, Paulay G, Sole-Cava A, Chen C A, Iwao K, Knowlton N. Conventional taxonomy obscures deep divergence between pacific and atlantic corals. Nature. 427:832–835. doi: 10.1038/nature02339. [DOI] [PubMed] [Google Scholar]
  20. Fukami H, Chen C A, Budd A F, Collins A, Wallace C, Chuang Y Y, Chen C, Dai C F, Iwao K, Sheppard C, Knowlton N. Mitochondrial and nuclear genes suggest that stony corals are monophyletic but most families of stony corals are not (order scleractinia, class anthozoa, phylum cnidaria) PLOS ONE; 2008. 3. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Fukami H, Chen C A, Chiou C Y, Knowlton N. Novel group I introns encoding a putative homing endonuclease in the mitochondrial cox1 gene of scleractinian corals. J Mol Evol. 64:591–600. doi: 10.1007/s00239-006-0279-4. [DOI] [PubMed] [Google Scholar]
  22. Fukami H, Knowlton N. Analysis of complete mitochondrial DNA sequences of three members of the montastraea annularis coral species complex (cnidaria, anthozoa, scleractinia) Coral Reefs. 24:410–417. [Google Scholar]
  23. Gagan M K, Ayliffe L K, Beck J W, Cole J E, Druffel Erm, Dunbar R B, Schrag D P. New views of tropical paleoclimates from corals. Quaternary Sci Rev. 19:45–64. [Google Scholar]
  24. Galli M T, Jadoul F, Bernasconi S M, Weissert H. Anomalies in global carbon cycling and extinction at the triassic/jurassic boundary: Evidence from a marine c-isotope record. Palaeogeogr Palaeocl. 216:203–214. [Google Scholar]
  25. Glasspool I J, Scott A C. Phanerozoic concentrations of atmospheric oxygen reconstructed from sedimentary charcoal. Nat Geosci. 3:627–630. [Google Scholar]
  26. Goddard M R, Burt A. Recurrent invasion and extinction of a selfish gene. P Natl Acad Sci. 96:13880–13885. doi: 10.1073/pnas.96.24.13880. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. Goddard M R, Leigh J, Roger A J, Pemberton A J. Invasion and persistence of a selfish gene in the cnidaria. PLOLS ONE; 2006. 1. [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. Gogarten J P. Inteins, introns, and homing endonucleases: Recent revelations about the life cycle of parasitic genetic elements. Bmc Evol Biol; 2006. 6. [DOI] [PMC free article] [PubMed] [Google Scholar]
  29. Guindon S, Dufayard J F, Lefort V, Anisimova M, Hordijk W, Gascuel O. New algorithms and methods to estimate maximum-likelihood phylogenies: Assessing the performance of phyml 3.0. Syst Biol. 59:307–321. doi: 10.1093/sysbio/syq010. [DOI] [PubMed] [Google Scholar]
  30. Huchon D, Szitenberg A, Rot C, Ilan M. Diversity of sponge mitochondrial introns revealed by cox1 sequences of tetillidae. Bmc Evol Biol; 2010. 10. [DOI] [PMC free article] [PubMed] [Google Scholar]
  31. Nylander Jaa. Mrmodeltest 2.0 program distributed by the author. Evolutionary Biology Centre; 2004. [Google Scholar]
  32. Jeffares D C, Penkett C J, Bahler J. Rapidly regulated genes are intron poor. Trends Genet. 24:375–378. doi: 10.1016/j.tig.2008.05.006. [DOI] [PubMed] [Google Scholar]
  33. Kiessling W, Aberhan M, Brenneis B, Wagner P J. Extinction trajectories of benthic organisms across the triassic-jurassic boundary. Palaeogeogr Palaeoclimatol Palaeoecol. 244:201–222. [Google Scholar]
  34. Kiessling W, Baron-Szabo R C. Extinction and recovery patterns of scleractinian corals at the cretaceoustertiary boundary. Palaeogeogr Palaeoclimatol Palaeocol. 214:195–223. [Google Scholar]
  35. Kitahara M V, Cairns S D, Stolarski J, Blair D, Miller D J. A comprehensive phylogenetic analysis of the scleractinia (cnidaria, anthozoa) based on mitochondrial co1 sequence data. PLOS ONE; 2010. 5. [DOI] [PMC free article] [PubMed] [Google Scholar]
  36. Kitahara M V, Lin M F, Foret S, Huttley G, Miller D J, Chen C A. The "naked coral'' hypothesis revisitedevidence for and against scleractinian monophyly. PLOS One; 2014. 9. [DOI] [PMC free article] [PubMed] [Google Scholar]
  37. Lavrov D V, Lang B F. Poriferan mtdna and animal phylogeny based on mitochondrial gene arrangements. Syst Biol. 54:651–659. doi: 10.1080/10635150500221044. [DOI] [PubMed] [Google Scholar]
  38. Librado P, Rozas J. Dnasp v5:A software for comprehensive analysis of DNA polymorphism data. Bioinformatics. 25:1451–1452. doi: 10.1093/bioinformatics/btp187. [DOI] [PubMed] [Google Scholar]
  39. Lin M F, Chou W H, Kitahara M V, Chen C A, Miller D J, Forêt S. Corallimorpharians are not "naked corals'': insights into relationships between Scleractinia and Corallimorpharia from phylogenomic analyses. PeerJ; 2016. 4. [DOI] [PMC free article] [PubMed] [Google Scholar]
  40. Lin M F, Kitahara M V, Luo H W, Tracey D, Geller J, Fukami H, Miller D J, Chen C A. Mitochondrial genome rearrangements in the scleractinia/corallimorpharia complex: Implications for coral phylogeny. Genome Biol Evol. 6:1086–1095. doi: 10.1093/gbe/evu084. [DOI] [PMC free article] [PubMed] [Google Scholar]
  41. Lin M F, Luzon K S, Licuanan W Y, Ablan-Lagman M C, Chen C A. Seventy-four universal primers for characterizing the complete mitochondrial genomes of scleractinian corals (cnidaria; anthozoa) Zool Stud. 50:513–524. [Google Scholar]
  42. Lisacek F, Diaz Y, Michel F. Automatic identification of group-I intron cores in genomic DNA-sequences. J Mol Biol. 235:1206–1217. doi: 10.1006/jmbi.1994.1074. [DOI] [PubMed] [Google Scholar]
  43. Lynch M. Intron evolution as a population-genetic process. P Natl Acad Sci. 99:6118–6123. doi: 10.1073/pnas.092595699. [DOI] [PMC free article] [PubMed] [Google Scholar]
  44. Wpadrm Maddison. Mesquite: A modular system for evolutionary analysis. 2011.
  45. Marzoli A, Bertrand H, Knight K B, Cirilli S, Buratti N, Verati C, Nomade S, Renne P R, Youbi N, Martini R, Allenbach K, Neuwerth R, Rapaille C, Zaninetti L, Bellieni G. Synchrony of the central atlantic magmatic province and the triassic-jurassic boundary climatic and biotic crisis. Geology. 32:973–976. [Google Scholar]
  46. Medina M, Collins A G, Takaoka T L, Kuehl J V, Boore J L. Naked corals: Skeleton loss in scleractinia. P Natl Acad Sci. 103:9096–9100. doi: 10.1073/pnas.0602444103. [DOI] [PMC free article] [PubMed] [Google Scholar]
  47. Olsen P E, Kent D V, Sues H D, Koeberl C, Huber H, Montanari A, Rainforth E C, Fowell S J, Szajna M J, Hartline B W. Ascent of dinosaurs linked to an iridium anomaly at the triassic-jurassic boundary. Science. 296:1305–1307. doi: 10.1126/science.1065522. [DOI] [PubMed] [Google Scholar]
  48. Perlman P S, Butow R A. Mobile introns and intronencoded proteins. Science. 246:1106–1109. doi: 10.1126/science.2479980. [DOI] [PubMed] [Google Scholar]
  49. Pierron D, Wildman D E, Huttemann M, Markondapatnaikuni G C, Aras S, Grossman L I. Cytochrome c oxidase: Evolution of control via nuclear subunit addition. BBABioenergetics. 1817:590–597. doi: 10.1016/j.bbabio.2011.07.007. [DOI] [PMC free article] [PubMed] [Google Scholar]
  50. Posada D, Crandall K A. Modeltest: Testing the model of DNA substitution. Bioinformatics. 14:817–818. doi: 10.1093/bioinformatics/14.9.817. [DOI] [PubMed] [Google Scholar]
  51. Raghukumar C, Raghukumar S. Fungal invasion of massive corals. Mar Ecol. 12:251–260. [Google Scholar]
  52. Ronquist F, Huelsenbeck J P. Mrbayes 3: Bayesian phylogenetic inference under mixed models. Bioinformatics. 19:1572–1574. doi: 10.1093/bioinformatics/btg180. [DOI] [PubMed] [Google Scholar]
  53. Roy S W, Gilbert W. The pattern of intron loss. P Natl Acad Sci. 102:713–718. doi: 10.1073/pnas.0408274102. [DOI] [PMC free article] [PubMed] [Google Scholar]
  54. Schonberg Chl, Wilkinson C R. Induced colonization of corals by a clionid bioeroding sponge. Coral Reefs. 20:69–76. [Google Scholar]
  55. Shearer T L, Van Oppen Mjh, Romano S L, Worheide G. Slow mitochondrial DNA sequence evolution in the anthozoa (cnidaria) Mol Ecol. 11:2475–2487. doi: 10.1046/j.1365-294x.2002.01652.x. [DOI] [PubMed] [Google Scholar]
  56. Shimodaira H, Hasegawa M. Consel: For assessing the confidence of phylogenetic tree selection. Bioinformatics. 17:1246–1247. doi: 10.1093/bioinformatics/17.12.1246. [DOI] [PubMed] [Google Scholar]
  57. Stolarski J, Cairns M. The ancient evolutionary origins of scleractinia revealed by azooxanthellate corals. Bmc Evol Biol; 2011. 11. [DOI] [PMC free article] [PubMed] [Google Scholar]
  58. Talavera G, Castresana J. Improvement of phylogenies after removing divergent and ambiguously aligned blocks from protein sequence alignments. Syst Biol. 56:564–577. doi: 10.1080/10635150701472164. [DOI] [PubMed] [Google Scholar]
  59. Tamura K, Dudley J, Nei M, Kumar S. Mega4: Molecular evolutionary genetics analysis (mega) software version 4.0. Mol Biol Evol. 24:1596–1599. doi: 10.1093/molbev/msm092. [DOI] [PubMed] [Google Scholar]
  60. Tseng C C, Wallace C C. Mitogenomic analysis of montipora cactus and anacropora matthai (cnidaria; scleractinia; acroporidae) indicates an unequal rate of mitochondrial evolution among acroporidae corals. Coral Reefs. 24:502–508. [Google Scholar]
  61. Van Oppen Mjh, Bj Mcdonald N R. The mitochondrial genome of acropora tenuis (cnidaria: Scleractinia) contains a large group I intron and a candidate control region. J Mol Evol. 55:1–13. doi: 10.1007/s00239-001-0075-0. [DOI] [PubMed] [Google Scholar]
  62. Van Oppen Mjh, Hislop N R, Hagerman P J, Miller D J. Gene content and organization in a segment of the mitochondrial genome of the scleractinian coral acropora tenuis: Major differences in gene order within the anthozoan subclass zoantharia. Mol Biol Evol. 16:1812–1815. doi: 10.1093/oxfordjournals.molbev.a026094. [DOI] [PubMed] [Google Scholar]
  63. Zuker M. Mfold web server for nucleic acid folding and hybridization prediction. Nucleic Acids Res. 31:3406–3415. doi: 10.1093/nar/gkg595. [DOI] [PMC free article] [PubMed] [Google Scholar]

Articles from Zoological Studies are provided here courtesy of Biodiversity Research Center, Academia Sinica

RESOURCES