Phylogenomic analyses of echinoid diversification prompt a re-evaluation of their fossil record
- Department of Earth & Planetary Sciences, Yale University, United States
- Scripps Institution of Oceanography, University of California San Diego, United States
- Department of Earth Sciences, Natural History Museum, United Kingdom
- University College London Center for Life’s Origins and Evolution, United Kingdom
- Department of Invertebrate Zoology and Geology, California Academy of Sciences, United States
- Bader International Study Centre, Queen's University, Herstmonceux Castle, United Kingdom
- Departamento de Bioquímica y Biología Molecular, Facultad de Ciencias Biológicas, Universidad de Concepción, Chile
- School of Zoology, Faculty of Life Sciences, Tel Aviv University, Israel
- Steinhardt Museum of Natural History, Israel
- Department of Geology and Palaeontology, Natural History Museum Vienna, Austria
Figures
Figure 1
Neognathostomate diversity and phylogenetic relationships.
(A) Fellaster zelandiae, North Island, New Zealand (Clypeasteroida). (B) Large specimen: Peronella japonica, Ryukyu Islands, Japan; Small specimen: Echinocyamus crispus, Maricaban Island, …
Figure 2
Phylogenetic relationships among major clades of Echinoidea.
(A) Favored topology, as obtained using the full supermatrix and a best-fit partitioning scheme in IQ-TREE (Nguyen et al., 2015). With the exception of a single contentious node within Echinacea …
Figure 3
Estimated branch lengths across different models of molecular evolution.
Different site-homogeneous models (left) infer similar levels of divergence, and the choice between them induces little distortion in the general tree structure. Site-heterogeneous models on the …
Figure 4 with 1 supplement
The 10 most sensitive node dates are found within Cidaroidea, Aulodonta, Neognathostomata, and among outgroup nodes.
For each, the range shown spans the interval between the minimum and maximum ages found among the consensus topologies of the 80 time-calibrated runs performed.
Figure 4—figure supplement 1
Median ages for selected clades across the consensus trees of the 80 time-calibrated experiments performed.
Figure 5 with 5 supplements
Sensitivity of divergence time estimation to methodological decisions.
Between-group principal component analysis (bgPCA) was used to retrieve axes that separate chronograms based on the clock model (A), model of molecular evolution (B), and gene sampling strategy (C) …
Figure 5—figure supplement 1
Sensitivity of divergence time estimation to the use of alternate prior distributions on calibrated nodes.
Between-group principal component analysis (bgPCA) was used to retrieve the axes of maximum discrimination between chronograms estimated by enforcing either uniform or Cauchy prior distributions. …
Figure 5—figure supplement 2
Distribution of posterior probabilities for node ages that show an average difference larger than 20 Myr depending on the choice of clock prior.
Figure 5—figure supplement 3
Distribution of posterior probabilities for node ages that show a maximum difference larger than 20 Myr depending on the gene sampling strategy.
The largest differences can be seen in the relatively younger ages of Ambulacraria and Echinodermata when using clock-like genes, and in the relatively older ages for some nodes within cidaroids and …
Figure 5—figure supplement 4
Distribution of posterior probabilities for node ages that are the most affected by the choice of model of molecular evolution.
No node showed average differences larger than 20 Myr, so those suffering the biggest changes are shown instead.
Figure 5—figure supplement 5
Distribution of posterior probabilities for node ages that are the most affected by the choice of prior distributions on calibrated nodes.
No node showed average differences larger than 20 Myr, so those suffering the biggest changes are shown instead.
Figure 6 with 2 supplements
Divergence times among major clades of Echinoidea and other echinoderms.
(A) Consensus chronogram of the two PhyloBayes (Lartillot et al., 2013) runs using clock-like genes under a CAT + GTR + G model of evolution, an autocorrelated log-normal (LN) clock, and Cauchy …
Figure 6—figure supplement 1
Number of lineages inferred to have crossed the Permian-Triassic (P-T) boundary.
The probabilities of each scenario are estimated from the inferred divergence times of the 16,000 chronograms sampled across all of the analyses performed (200 for the two runs of each combination …
Figure 6—figure supplement 2
Prior distributions of all constrained nodes.
Five-hundred replicates were sampled from the joint prior, showing appropriately broad distributions of node ages. Blue lines show minima and yellow ones maxima (when enforced); dotted lines show …
Figure 7
Relationship between the root-to-tip variance (a proxy for the clock-likeness of loci) and the rate of evolution.
The most clock-like loci (shown in red), which are often favored for the inference of divergence times (e.g., Smith et al., 2018; Carruthers et al., 2020), are among the most highly conserved and …
Appendix 3—figure 1
Ordering of loci enforced using genesortR (Mongiardino Koch, 2021b) and its relationship to the seven gene properties employed.
High ranking loci (i.e., the most phylogenetically useful) show low root-to-tip variances (or high clock-likeness), low saturation, and low compositional heterogeneity, as well as high average …
Appendix 3—figure 2
Trace plots of the log-likelihood of different time calibration runs.
All runs show evidence of reaching convergence and stationarity before our imposed burn-in fraction of 10,000 generations (dashed lines). For simplicity, only runs under the CAT + GTR + G model and …
Tables
Appendix 1—table 1
Transcriptomic/genomic datasets added in this study relative to the taxon sampling of Mongiardino Koch et al., 2018 and Mongiardino Koch and Thompson, 2021d.
Taxa with citations were taken from the literature, and details can be found in the corresponding studies and associated NCBI BioProjects. Taxa are shown in alphabetical order; those identified with …
| Taxon | Citation | Tissue type | Collector | Locality (depth) | Voucher | GenBank accession number |
|---|---|---|---|---|---|---|
| Amphiura filiformis (OG) | Dylus et al., 2016 | – | – | – | – | SRX2255774 |
| Apatopygus recens | This study | Mixed | Owen Anderson | Foveaux Strait, South Island, New Zealand | SIO-BIC E7142 | SRR16134561 |
| Aspidodiadema hawaiiense | This study | Mixed | Greg Rouse, Avery Hiley | Seamount 4, Costa Rica, Pacific Ocean (1003 m) | SIO-BIC E7363 | SRR16134560 |
| Asterias rubens (OG) | Reich et al., 2015 | – | – | – | – | SRX445860 |
| Astrophyton muricatum (OG) | Janies et al., 2016; Linchangco et al., 2017 | – | – | – | – | SRX1391908 |
| Bathysalenia phoinissa | This study | Tube feet, spine muscles | BIOMAGLO Cruise Team | Mozambique Channel, Mayotte (295–336 m) | MNHN-IE-2016–23 | SRR15130003 |
| Clypeaster japonicus | This study | Eggs | Frances Armstrong | Misaki Marine Biological Station, Kanagawa, Japan | – | SRR16134552 |
| Echinothrix calamaris | This study | Male gonad | – | Philippines | – | SRR16134551 |
| Encope emarginata | This study | Eggs | Gulf Specimen Marine Lab | Apalachee Bay, FL, USA | – | SRR16134550 |
| Eucidaris metularia | This study | Mixed | Greg Rouse | Al-Fahal Reef, Red Sea, Makkah, Saudi Arabia | SIO-BIC 2017–008 | SRR16134549 |
| Fellaster zelandiae | This study | Spines, tube feet, gut, joining tissue of Aristotle’s lantern | Wilma Blom | Western end of Cornwallis Beach, Auckland, New Zealand | SIO-BIC E7920 | SRR16134548 |
| Histocidaris variabilis | This study | Gonad | Greg Rouse, Avery Hiley | Las Gemelas Seamount, near Isla del Coco, Costa Rica, Pacific Ocean (571 m) | SIO-BIC E7350 | SRR16134547 |
| Lamberticrinus messingi (OG) | Clouse et al., 2015; Janies et al., 2016 | – | – | – | – | SRX1397823 |
| Leodia sexiesperforata | This study | Eggs | Frances Armstrong | Bocas del Toro, Panama | – | SRR16134546 |
| Metacrinus rotundus (OG) | Koga et al., 2016 | – | – | – | – | DRX021520 |
| Micropyga tuberculata | This study | Tube feet, spine muscles | BIOMAGLO Cruise Team | Mozambique Channel, Îles Glorieuses (385–410 m) | MNHN-IE-2016–39 | SRR15130004 |
| Ophiocoma echinata (OG) | Reich et al., 2015 | – | – | – | – | SRX445856 |
| Peronella japonica | This study | Eggs | Frances Armstrong | Kanazawa, Japan | – | SRR16134545 |
| Rhyncholampas pacificus | This study | Mixed | Carlos A. Conejeros-Vargas | Panteón Beach, Puerto Ángel Bay, Oaxaca, Mexico | SIO-BIC E7918 | SRR16134558 |
| Scaphechinus mirabilis | Simakov et al., 2015 | – | – | – | – | DRX187887DRX187888 |
| Sinaechinocyamus mai | This study | Gregory’s diverticulum | Jih-Pai Lin | Miaoli County, Taiwan | SIO-BIC E7919 | SRR16134557 |
| Sterechinus neumayeri | Collins et al., 2021 | – | – | – | – | ERX3498697ERX3498698ERX3498699ERX3498700ERX3498701 |
| Stereocidaris nascaensis | This study | Muscle surrounding Aristotle’s lantern | Charlotte Seid | Off San Ambrosio, Desventuradas Islands, Chile (215 m) | SIO-BIC E7154 | SRR16134559 |
| Tetrapygus niger | This study | Female gonad, tube feet | Felipe Aguilera | Dichato Bay, Chile | – | SRR16134553SRR16134554 |
| Tripneustes gratilla | This study | Pedicellariae | – | Philippines | – | SRR16134556 |
| Tromikosoma hispidum | This study | Tube feet | Lisa Levin, Todd Litke | Quepos Plateau, Costa Rica, Pacific Ocean (2067 m) | SIO-BIC E7251 | SRR16134555 |
Appendix 1—table 2
Details of molecular datasets and supermatrix.
Statistics for raw reads and assemblies are shown for datasets incorporated in this study relative to the sampling of Mongiardino Koch et al., 2018 and Mongiardino Koch and Thompson, 2021d, where …
| Species | Mean insert size | Read pairs (initial) | Read pairs (retained) | Assembled transcripts/contigs | Number of loci | Removed by TreeShrink | Final occupancy |
|---|---|---|---|---|---|---|---|
| Abatus agassizii | – | – | – | – | 522 | 5 | 38.4 |
| Abatus cordatus | – | – | – | – | 497 | 2 | 36.8 |
| Acanthaster planci (OG) | – | – | – | – | 864 | 8 | 63.6 |
| Amphiura filiformis (OG) | 180.1 | 61,558,173 | 52,206,727 | 416,946 | 761 | 8 | 55.9 |
| Apatopygus recens | 415.3 | 74,315,687 | 56,898,850 | 274,380 | 1152 | 5 | 85.2 |
| Apostichopus japonicus (OG) | – | – | – | – | 849 | 9 | 62.4 |
| Araeosoma leptaleum | – | – | – | – | 1184 | 2 | 87.8 |
| Arbacia lixula | – | – | – | – | 1234 | 1 | 91.6 |
| Aspidodiadema hawaiiense | 228.7 | 109,716,219 | 104,518,714 | 311,032 | 1060 | 11 | 77.9 |
| Asterias rubens (OG) | 230.4 | 31,890,613 | 25,495,009 | 103,090 | 805 | 9 | 59.1 |
| Asthenosoma varium | – | – | – | – | 1254 | 7 | 92.6 |
| Astrophyton muricatum (OG) | 195.9 | 25,191,954 | 22,281,829 | 149,146 | 478 | 5 | 35.1 |
| Bathysalenia phoinissa | – | – | – | 154,120 | 605 | 6 | 44.5 |
| Brissus obesus | – | – | – | – | 773 | 0 | 57.4 |
| Caenopedina hawaiiensis | – | – | – | – | 1094 | 2 | 81.1 |
| Clypeaster japonicus | 198.6 | 10,505,520 | 9,298,316 | 74,743 | 829 | 1 | 61.5 |
| Clypeaster rosaceus | – | – | – | – | 1242 | 2 | 92.1 |
| Clypeaster subdepressus | – | – | – | – | 1233 | 3 | 91.4 |
| Colobocentrotus atratus | – | – | – | – | 1158 | 0 | 86.0 |
| Conolampas sigsbei | – | – | – | – | 1001 | 5 | 74.0 |
| Cystechinus c.f. giganteus | – | – | – | – | 661 | 0 | 49.1 |
| Dendraster excentricus | – | – | – | – | 337 | 1 | 25.0 |
| Diadema setosum | – | – | – | – | 305 | 1 | 22.6 |
| Echinarachnius parma | – | – | – | – | 1187 | 3 | 88.0 |
| Echinocardium cordatum | – | – | – | – | 1012 | 2 | 75.0 |
| Echinocardium mediterraneum | – | – | – | – | 1185 | 1 | 88.0 |
| Echinocyamus crispus | – | – | – | – | 709 | 6 | 52.2 |
| Echinometra mathaei | – | – | – | – | 1055 | 0 | 78.4 |
| Echinothrix calamaris | 203.9 | 68,871,087 | 60,443,904 | 251,788 | 1252 | 4 | 92.7 |
| Encope emarginata | 206.2 | 12,015,888 | 10,461,870 | 66,241 | 1076 | 1 | 79.9 |
| Eucidaris metularia | 321.6 | 38,802,159 | 29,047,401 | 83,318 | 412 | 2 | 30.5 |
| Eucidaris tribuloides | – | – | – | – | 414 | 0 | 30.8 |
| Evechinus chloroticus | – | – | – | – | 1196 | 1 | 88.8 |
| Fellaster zelandiae | 313.9 | 62,619,791 | 51,742,748 | 168,598 | 1269 | 1 | 94.2 |
| Heliocidaris erythrogramma | – | – | – | – | 931 | 0 | 69.2 |
| Histocidaris variabilis | 329.2 | 84,103,672 | 73,884,180 | 144,044 | 1189 | 5 | 88.0 |
| Holothuria forskali (OG) | – | – | – | – | 743 | 8 | 54.6 |
| Lamberticrinus messingi (OG) | 195.0 | 22,989,820 | 20,234,597 | 59,049 | 351 | 3 | 25.9 |
| Leodia sexiesperforata | 203.8 | 16,211,182 | 14,174,475 | 68,964 | 1064 | 1 | 79.0 |
| Leptosynapta clarki (OG) | – | – | – | – | 403 | 4 | 29.6 |
| Lissodiadema lorioli | – | – | – | – | 770 | 0 | 57.2 |
| Loxechinus albus | – | – | – | – | 1265 | 1 | 93.9 |
| Lytechinus variegatus | – | – | – | – | 1257 | 2 | 93.2 |
| Mellita tenuis | – | – | – | – | 1002 | 1 | 74.4 |
| Meoma ventricosa | – | – | – | – | 1053 | 0 | 78.2 |
| Mesocentrotus nudus | – | – | – | – | 1247 | 0 | 92.6 |
| Metacrinus rotundus (OG) | 198.5 | 23,791,832 | 20,900,345 | 83,718 | 642 | 7 | 47.2 |
| Micropyga tuberculata | – | – | – | 170,514 | 415 | 4 | 30.5 |
| Ophiocoma echinata (OG) | 278.5 | 28,427,026 | 24,836,025 | 130,153 | 712 | 7 | 52.4 |
| Paracentrotus lividus | – | – | – | – | 1266 | 0 | 94.1 |
| Patiria miniata (OG) | – | – | – | – | 740 | 8 | 54.4 |
| Peronella japonica | 208.3 | 17,696,287 | 15,707,931 | 106,110 | 1043 | 6 | 77.0 |
| Prionocidaris baculosa | – | – | – | – | 794 | 3 | 58.8 |
| Psammechinus miliaris | – | – | – | – | 1173 | 1 | 87.1 |
| Rhyncholampas pacificus | 346.8 | 63,116,413 | 52,160,741 | 234,910 | 1070 | 2 | 79.3 |
| Saccoglossus kowalevskii (OG) | – | – | – | – | 668 | 6 | 49.2 |
| Scaphechinus mirabilis | 401.7 | 10,169,195 | 8,796,067 | 127,664 | 974 | 4 | 72.1 |
| Sinaechinocyamus mai | 297.2 | 60,208,172 | 52,265,201 | 164,646 | 1233 | 1 | 91.5 |
| Sphaerechinus granularis | – | – | – | – | 1214 | 1 | 90.1 |
| Sterechinus neumayeri | 207.3 | 26,376,279 | 21,308,840 | 122,001 | 1097 | 1 | 81.4 |
| Stereocidaris nascaensis | 327.0 | 69,962,495 | 60,316,050 | 121,508 | 1200 | 6 | 88.7 |
| Stomopneustes variolaris | – | – | – | – | 908 | 0 | 67.5 |
| Strongylocentrotus purpuratus | – | – | – | – | 1266 | 5 | 93.7 |
| Tetrapygus niger | 202.5 | 63,040,541 | 52,761,671 | 163,084 | 1287 | 2 | 95.5 |
| Tripneustes gratilla | 154.6 | 62,962,239 | 57,015,692 | 130,376 | 1309 | 1 | 97.2 |
| Tromikosoma hispidum | 300.4 | 57,208,357 | 47,909,038 | 234,502 | 1238 | 7 | 91.5 |
