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Dating the Origin of the Major Lineages of Branchiopoda

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Dating the Origin of the Major Lineages of Branchiopoda Available online at www.sciencedirect.com ScienceDirect Palaeoworld 25 (2016) 303–317 Dating the origin of the major lineages of Branchiopoda a,∗ b a,∗ Xiao-Yan Sun , Xuhua Xia , Qun Yang a LPS, Nanjing Institute of Geology and Palaeontology, Chinese Academy of Sciences, Nanjing 210008, China b Department of Biology, University of Ottawa, Ontario K1N 6N5, Canada Received 3 June 2014; received in revised form 30 October 2014; accepted 3 February 2015 Available online 14 February 2015 Abstract Despite the well-established phylogeny and good fossil record of branchiopods, a consistent macro-evolutionary timescale for the group remains elusive. This study focuses on the early branchiopod divergence dates where fossil record is extremely fragmentary or missing. On the basis of a large genomic dataset and carefully evaluated fossil calibration points, we assess the quality of the branchiopod fossil record by calibrating the tree against well-established first occurrences, providing paleontological estimates of divergence times and completeness of their fossil record. The maximum age constraints were set using a quantitative approach of Marshall (2008). We tested the alternative placements of Yicaris and Wujicaris in the referred arthropod tree via the likelihood checkpoints method. Divergence dates were calculated using Bayesian relaxed molecular clock and penalized likelihood methods. Our results show that the stem group of Branchiopoda is rooted in the late Neoproterozoic (563 ± 7 Ma); the crown-Branchiopoda diverged during middle Cambrian to Early Ordovician (478–512 Ma), likely representing the origin of the freshwater biota; the Phyllopoda clade diverged during Ordovician (448–480 Ma) and Diplostraca during Late Ordovician to early Silurian (430–457 Ma). By evaluating the congruence between the observed times of appearance of clade in the fossil record and the results derived from molecular data, we found that the uncorrelated rate model gave more congruent results for shallower divergence events whereas the auto-correlated rate model gives more congruent results for deeper events. © 2015 Elsevier B.V. and Nanjing Institute of Geology and Palaeontology, CAS. All rights reserved. Keywords: Branchiopoda; Fossil calibrations; Relaxed molecular clock; Likelihood checkpoints; Origin of freshwater biota 1. Introduction Cyclestherida, were originally included in a single order ‘Con- chostraca’, which later proved to be paraphyletic with respect Branchiopods are one of the most diverse groups of crus- to the Cladocera (Olesen, 1998; Taylor et al., 1999; Spears and taceans with approximately 1200 described species in 28 Abele, 2000; Braband et al., 2002; Swain and Taylor, 2003; families (Adamowicz and Purvis, 2005), occurring in fresh- DeWard et al., 2006; Stenderup et al., 2006; Sun et al., 2006). water, brackish and marine habitats. The class Branchiopoda But ‘Conchostraca’ is still commonly used in paleontology. The is divided into two subclasses: Sarsostraca and Phyllopoda higher-level relationships within Branchiopoda based on the (Fig. 1). Sarsostraca contains an extinct order Lipostraca and morphological characters have been partly confirmed by some the single extant order Anostraca, with some 300 species in 8 molecular analyses, suggesting the monophyly of Phyllopoda, families. Phyllopoda is divided into two subgroups: Calmanos- Cladocera, and Diplostraca with Laevicaudata as a basal lineage traca (including the extant order Notostraca and the extinct (e.g., Fryer, 1987; Olesen, 1998, 2007, 2009; Negrea et al., 1999; order Kazacharthra) and Diplostraca (= Onychura, including Sun et al., 2006; Richter et al., 2007; Regier et al., 2010; Regier Spinicaudata, Laevicaudata, Cyclestheria, and Cladocera). The and Zwick, 2011). clam shrimps, referring to Spinicaudata, Laevicaudata, and With the rich and well-studied fossil record, the earliest known branchiopod Rehbachiella kinnekullensis (Fig. 1), from the Orsten Lagerstätte of Cambrian Series 3 (Agnostus pisi- ∗ formis Zone of Alum Shale) in Sweden, is a marine crustacean Corresponding authors. Tel.: +86 25 8328 2103. (Walossek, 1993, 1995), interpreted as a stem-group represen- E-mail addresses: [email protected] (X.-Y. Sun), [email protected] (Q. Yang). tative of Branchiopoda (Schram and Koenemann, 2001; Olesen, http://dx.doi.org/10.1016/j.palwor.2015.02.003 1871-174X/© 2015 Elsevier B.V. and Nanjing Institute of Geology and Palaeontology, CAS. All rights reserved. 304 X.-Y. Sun et al. / Palaeoworld 25 (2016) 303–317 Fig. 1. Branchiopod phylogeny sensu Olesen (2009) superimposed on the known stratigraphic record. Geological dates from the IUGS International Stratigraphic Chart (Cohen et al., 2013). 1. Rehbachiella kinnekullensis (Walossek, 1993; Olesen, 2009); 2. Riley Lake taxa (Harvey et al., 2012); 3. Unnamed Silurian Species (Schram, 1986); 4. Lepidocaris rhyniensis (Scourfield, 1926, 1940a,b; Walossek, 1993, 1995); 5. Palaeochirocephalus sp. (Shen and Huang, 2008); 6. Palaeochirocephalus rasnitsyni (Trussova, 1971); 7. Branchiopodites vectensis (Woodward, 1879); 8. Archaebranchinecta barstowensis (Belk and Schram, 2001); 9. Artemia salina (Djamali et al., 2010); 10. Castracollis wilsonae (Fayers and Trewin, 2003); 11. Notostracan indet (Garrouste et al., 2012); 12. Triops ornatus (Voigt et al., 2008); 13. Notostracan trace fossil (Minter and Lucas, 2009); 14. Lepidurus occitaniacus (Gand et al., 1997); 15. Lepidurus stormbergensis (Townrow, 1966); 16 and 18. Prolynceus (Shen and Chen, 1984; Shen et al., 2006); 17. Paleolynceus (Tasch, 1956); 19. Cyclestherioides pintoi (Raymond, 1946); 20. Cyclestheria detykteica (Novojilov, 1959); 21. Cyclestheria sp. (Gallego and Breitkreuz, 1994); 22. Euestheria sparsa (Zhang et al., 1976); 23. E. atsuensis (Kobayashi, 1952); 24. Cyclestheria wyomingensis (Shen et al., 2006); 25. Ebullitiocaris oviformis (Anderson et al., 2004); 26. E. elatus (Womack et al., 2012); 27. Leptodorosida zherikhini (Kotov, 2007); 28. Smirnovidaphnia smirnovi (Kotov, 2007); 29. Leposida ponomarenkoi (Kotov, 2007); 30. Archelatona zherikhini (Kotov and Korovchinsky, 2006). Bold lines indicate relatively higher diversity. Translucent pinkish box indicates the gap of some 68 million years between the earliest Cambrian marine and Devonian non-marine branchiopod fossils. (For interpretation of the references to color in this figure legend, the reader is referred to the web version of this article.) X.-Y. Sun et al. / Palaeoworld 25 (2016) 303–317 305 2009). Branchiopod-type appendages, particularly the mandibu- checkpoints method (Pyron, 2010) to assess alternate placement lar gnathal edges (autapomorphies of Anostraca), occur in of Yicaris and Wujicaris in the arthropod tree of Regier et al. shallow marine deposits of the Cambrian Series 3 and Furongian (2010). Series (ca. 488–510 Ma; Harvey et al., 2012). Despite well-established phylogenetic relationships and their Non-marine branchiopods abundantly occur in the Devonian, good fossil record, a consistent macroevolutionary time scale for with representatives of all four extant orders. However, bran- branchiopods has remained elusive. This study focuses on this chiopod fossil record is missing from Early Ordovician to late time interval aiming to decode the deep time evolution where Silurian when most of the deep divergences most likely have fossil record is extremely fragmentary or missing, using the pan- occurred, highlighting an apparent gap of some 68 million years crustacean part of the phylogenomic dataset of Regier and Zwick between the Cambrian marine and Devonian non-marine fos- (2011). This time interval is also a critical period for the early sils. It has been suggested that the branchiopod major groups evolution of the freshwater ecosystem. are rooted deep within the Silurian (Tasch, 1969; Negrea et al., This is the first attempt to approach the branchiopod phy- 1999). These paleontological inferences have been dismissed as lochronology using a comprehensive molecular dataset and ‘non-evidence’ due to the high preservation potential of Noto- carefully devised fossil calibrations. We mainly carried out the straca and ‘Conchostraca’. following: (1) estimating the quality of the branchiopod fossil A number of attempts have been recently made in molec- record by calibrating this tree against the observed record of ular dating of the arthropod tree, branchiopods involved (e.g., first occurrences; (2) estimating divergence time using relaxed Rehm et al., 2011; Oakley et al., 2013; Wheat and Wahlberg, molecular clock; (3) quantifying the match between the observed 2013). The reported time estimates for some crustacean lineages times of appearance of clade in the fossil record and the results appear to be significantly younger than corresponding fossil derived from molecular data. dates, especially for the divergence time of crown-Branchiopoda (see Fig. 2). Critical to molecular dating is the use of fossil infor- 2. Paleontological time for branchiopod early evolution mation to calibrate the clock. The incompleteness of the fossil record may cause underestimation of node ages in a phyloge- Traditionally, Branchiopoda comprise four extant orders: netic tree (Springer, 1995). Hug and Roger (2007) suggested Anostraca, Notostraca, Cladocera, and ‘Conchostraca’. Because that the best dating strategy was to maximize the number of Anostraca has thin and flexible exoskeletons lacking a cara- reliable and reasonably narrow calibration constraints, rather pace, Cladocera is small and fragile, whereas ‘conchostracans’
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