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Palaeoworld 25 (2016) 303–317

Dating the origin of the major lineages of

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 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 to Early (478–512 Ma), likely representing the origin of the freshwater

biota; the Phyllopoda diverged during Ordovician (448–480 Ma) and during Late Ordovician to early (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 ‘Con-

chostraca’, which later proved to be paraphyletic with respect

Branchiopods are one of the most diverse groups of crus- to the (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 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 , 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 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 , 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

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.

(Djamali et al., 2010); 10. Castracollis wilsonae (Fayers and Trewin, 2003); 11. Notostracan indet (Garrouste et al., 2012); 12. ornatus (Voigt et al., 2008);

13. Notostracan trace fossil (Minter and Lucas, 2009); 14. 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

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 , 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 (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’

than to maximize the number of sequences included. The and notostracans have hard exoskeletons well-preserved as

potential sources of error in the calibration process generally fossils, the branchiopod fossil records are taphonomically

include the incompleteness of the fossil record, erroneous fossil biased. Here we summarize general stratigraphic occur-

age estimates, and the placement of fossils on the tree (Forest, rence of major branchiopod groups in order to assess its

2009). completeness/incompleteness in geological record and to

The age of a lineage’s first appearance in the fossil record evaluate its congruence with molecular divergence time esti-

is generally treated as a minimum constraint in calibration pro- mates.

cedures; however, the maximum age constraints are difficult to All four extant branchiopod orders are known from the Paleo-

establish. Marshall (2008) developed a quantitative approach to zoic. The small carbonaceous branchiopod appendages recently

estimate maximum age constraints of lineages on the basis of discovered from the Cambrian of Canada indicate that crown-

adding a confidence interval onto the end point of the calibration Branchiopoda may have originated at least 488 Ma (Harvey and

lineage, which is adopted in this study. Butterfield, 2008; Harvey et al., 2012). The ‘conchostracan’ fos-

The fragmentary nature of the fossil record and the lin- sil records indicate that the crown-Diplostraca at least originated

∼

eage extinction have important consequences for the accurate in the late Silurian ( 420 Ma) (Tasch, 1969) (see Fig. 1).

placement of fossil calibration points. For example, two early The anostracan fossil records are only sporadically known.

Cambrian , Yicaris dianensis (Zhang et al., 2007) As mentioned earlier, Anostraca-related appendages, assignable

and Wujicaris muelleri (Zhang et al., 2010) both occurring to Sarsostraca (Fig. 1), occurred in the Cambrian Series 3

in the Yu’anshan Formation (Eoredlichia-Wutingaspis Zone, and Furongian Stage (Harvey and Butterfield, 2008; Harvey

Yunnan, China), are commonly used as calibration points in et al., 2012), at least 488 Ma. After a long gap in the fos-

divergence dating of (Oakley et al., 2013; Wheat sil record, occurred the oldest possible anostracan in Silurian

and Wahlberg, 2013). Yicaris, compared to branchiopods and terrestrial sediments of Indiana (Schram, 1986). The extinct

cephalocarids based on similarities in the endites on its pro- order Lipostraca, interpreted as the stem-Anostraca (Fig. 1),

topodites, was assigned to the . Wujicaris, known was found from the Devonian in Aberdeen-

from metanauplius larvae resembling those of and shire, Scotland (ca. 411 Ma; Walossek, 1993; Schram and

, is also considered of entomostracan grade. But the Koenemann, 2001; Olesen, 2004, 2009). True fairy shrimps

subclass Entomostraca is considered as an outdated classifica- (Anostracina) first occurred in the Middle Jiulong-

tion that is consistently resolved in molecular phylogenies as shan Formation, Inner Mongolia, China (Shen and Huang,

polyphyletic (Regier et al., 2010; Regier and Zwick, 2011). In 2008) (ca. 165 Ma; Gao and Ren, 2006). , Paleogene

current crustacean classification, the phylogenetic position of and Neogene anostracans, assignable to extant genera, include

Yicaris and Wujicaris is uncertain. Thus, we used the likelihood Palaeochirocephalus rasnitsyni from Lower Cretaceous of

306 X.-Y. Sun et al. / Palaeoworld 25 (2016) 303–317

Fig. 2. Phylogeny of Pan-crustacea and related groups plotted in a chronostratigraphic framework. Black boxes: reliable earliest fossil occurrences (see Appendix for

details); blue lines: indicating divergence time deduced from fossil record; dashed lines: the divergence time from Wheat and Wahlberg (2013); red dots: divergence

time estimates significantly younger than corresponding fossil dates, especially for the crown-Crustacea. Clado-gram based on Regier et al. (2010) and geological

dates from the IUGS International Stratigraphic Chart (Cohen et al., 2013). (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) 303–317 307

eastern Transbaikal, Russia (Trussova, 1971), Branchiopodites 3.1. Stratigraphic completeness estimate

vectensis from Eocene of freshwater (Bembridge) Limestone

of Gurnet Bay, Isle of Wight (Woodward, 1879; Rolfe, Relative completeness index (RCI), gap excess ratio (GER)

1967), Archaebranchinecta barstowensis from Middle Miocene (Benton, 1995, 2001), and the stratigraphic consistency index

Barstow Formation, California (Belk and Schram, 2001), and the (SCI) (Huelsenbeck, 1994) were used to measure the fit of strati-

brine shrimps, Artemia salina, from Pleistocene (Lake Urmia, graphic data to the current branchiopod topology (Fig. 1). This

NW Iran; Djamali et al., 2010). measures the amount of missing range that must be added to

Calmanostraca contains Notostraca (extant) and make stratigraphic record fit the phylogeny. The geological ages

Kazacharthra (extinct). Notostraca has two extant genera, of the earliest fossil representative of each clade at the suborder

Triops and Lepidurus, in the Triopsidae. Castracollis level included in this analysis are listed in Appendix.

wilsonae from the Rhynie Chert (ca. 411 Ma; Parry et al., 2011)

is probably a stem-lineage Calmanostraca (Fayers and Trewin, 3.2. Molecular clock tests

2003; Olesen, 2007, 2009). The first notostracan fossil is found

from the upper Famennian strata (ca. 360 Ma; Garrouste et al., To test whether evolutionary rate is constant across the whole

2012). The oldest confirmed Triops dated back to the late phylogeny, we used a likelihood ratio test to compare the likeli-

Carboniferous (Voigt et al., 2008) and Lepidurus in the hood of a model that enforces a strict molecular clock to a model

(Gand et al., 1997). Kazacharthra is the closest known relative with rates free to vary on each branch implemented in PAUP*

of the Notostraca, with fossils discovered from the Upper (Swofford, 2003). For this global clock test, we assumed the

Triassic to Lower Jurassic (Briggs et al., 1993; Olesen, 2009). best-fit model of molecular evolution as estimated in Modeltest

According to Tasch (1969), the Calmanostraca diverged from (Posada and Crandall, 1998).

Diplostraca during the Silurian. We further tested the rates on each branch via PATHd8

The earliest ‘Conchostraca’ fossils are Early Devonian spini- (Britton et al., 2006) using Mean Path Length (MPL) analyses.

caudatans with 10 families occurring almost simultaneously, Finally, we tested two clade-specific molecular clock

followed by 4 periods of rapid radiation in late Paleozoic hypotheses by multiple pair-wise relative rate tests, implemented

and Mesozoic. The rapid diversification of spinicaudatan fauna in HyPhy (Kosakovsky Pond et al., 2005), assuming the best-fit

makes them biostratigraphically useful for subdivision and cor- model of molecular evolution to be estimated with Modeltest.

relation of non-marine successions (Kozur and Weems, 2010).

Laevicaudata as a basal lineage of Diplostraca first appeared 3.3. Fossil calibration age priors

during the Middle Jurassic (Shen and Chen, 1984). According

to the diversification of Spinicaudata in the Devonian, ‘Con- Paleontological data of fossil Branchiopoda and their rela-

chostraca’ was presumed to have originated in the late Silurian tives were reviewed from available summaries and the original

(Tasch, 1969; Negrea et al., 1999). literature, together with hypotheses about their probable stem

Cladoceromorpha includes Cladocera and Cyclestherida, as lineages and evolutionary relationships (Appendix). The evolu-

suggested by molecular and morphological cladistic analy- tionary tree combining cladograms with the fossil record was

sis (Crease and Taylor, 1998; Ax, 1999; Spears and Abele, used to calibrate molecular clock or to constrain estimates of

2000). The earliest known cladoceran Ebullitiocaris oviformis divergence times (Fig. 2).

comes from the Early Devonian Rhynie Chert (ca. 411 Ma)

(Anderson et al., 2004). Fossils of two cladoceran suborders, 3.4. Maximum age bracket for divergence time estimates

Anomopoda and , are found from Mesozoic (Kotov

and Korovchinsky, 2006; Kotov, 2007, 2009; Kotov and Taylor, The maximum age constraints were obtained by adding a

2011). Cyclestherida ranged from late Permian to Holocene, confidence interval onto the end point of the calibration lineage,

with an extended gap in Jurassic and Cretaceous (Shen et al., estimated from the equation given in Marshall (2008): 2006). = √FAcal

FAc nH¯

(1 − C)

3. Data and methods where FAc is the maximum age bracket, FAcal is the calibration

date (age of the oldest fossil in the lineage), C is the confidence

We analyzed the molecular data of Regier et al. (2010; also level, and n is the number of lineages with a fossil record, each

see Regier and Zwick, 2011), focusing on major pancrustacean known from an average of fossil localities, which is set to 1 here

, including 68 single-copy nuclear -coding gene as recommended by Marshall (2008).

loci of 36 species (29 pancrustacean species, and 6 myriapods

plus one onychophoran as outgroups). We realigned each of 3.5. Molecular estimates of divergence times

the 68 gene fragments by alignments of coding DNA from

aligned sequences using DAMBE (Xia and Xie, We performed dating analyses using four different relaxed

2001). The reference topology of Regier et al. (2010; also see molecular clock methods, which have complementary advan-

Regier and Zwick, 2011) was used for molecular dating in this tages and limitations. The Bayesian relaxed molecular methods

study. were implemented by the program MCMCTree v. 4.4e (Yang,

308 X.-Y. Sun et al. / Palaeoworld 25 (2016) 303–317

2007), Multidivtime (Thorne et al., 1998), and BEAST v1.5.4 not significant, indicating that the fossil record may be relatively

(Drummond and Rambaut, 2007). Analyses with penalized like- poor. The relatively poor SCI (0.4) indicates that the majority of

lihood (PL) method were performed with the r8s software their nodes are stratigraphically inconsistent.

(Sanderson, 2003).

Bayesian relaxed molecular clocks, which assume rates of

4.2. Molecular clock tests

molecular evolution are uncorrelated but lognormally distributed

among lineages (Drummond et al., 2006), as implemented in

A global molecular clock was rejected in a likelihood

BEAST v1.5.4, were used for dating analyses. The Yule model

ratio test. The log likelihood assuming a molecular clock

was applied to model cladogenesis in all analyses. The effective −

was 10 643.74 compared to the non-clock likelihood of

sample sizes (ESS, >300) and convergence were summarized

−10 564.38, resulting in a likelihood ratio statistic of 158.72

using Tracer (version 1.5) included in the BEAST program

(P < 0.005, df = 35).

package.

The null hypothesis of constant rate of evolution was rejected

for two a priori clade-specific hypotheses. Branchiopod Artemia

3.6. Likelihood checkpoint test for uncertain fossil

salina showed a significant slow rate of molecular evolution.

calibrations

Most (28 of 34) of the possible 3-taxon relative rate compar-

isons using Peripatus sp. as outgroup and Artemia salina as one

In order to evaluate the alternative placement of Yicaris and

ingroup rejected the null hypothesis (P < 0.05). In every pair-

Wujicaris, we used the likelihood checkpoints method (Pyron,

wise comparison, Artemia salina’s branch was shorter than the

2010). It is a posterior method for an objective assessment of the

other ingroups, indicating a relatively slow rate of evolution.

likelihood of inferred divergence times to evaluate the place-

Of the six comparisons that did not show significantly slower

ment of fossil constraints. Given the fossil constraints F , the

t evolution in Anostraca, four were comparisons with branchio-

likelihood of a chronogram T can be assessed by calculating the

pod species, suggesting that branchiopods also may have a slow

joint probability densities of the inferred ages for the likelihood evolutionary rate.

checkpoints, Nˆ t i :

( ) showed a significantly elevated rate of molecu-

V lar evolution. Most (31 of 34) of possible 3-taxon relative rate

comparisons using Peripatus sp. as outgroup and Speleonectes

L(T |Ft) = P(Nˆ t(i)).

i=1 tulumensis as one ingroup rejected the null hypothesis (P < 0.05).

The ucld.stdev parameter estimated by BEAST program

Three fossil dates were used as likelihood checkpoints on

can reflect the extent of molecular rate heterogeneity. The

labeled nodes (D, E, G) to evaluate the likelihood for the three

mean substitution rate is 2.01% per Myr, and the parameter

alternative placements for Yicaris and Wujicaris (C1, C2, C3;

ucld.stdev = 0.286 (ESS = 739) indicates a slight deviation from

Fig. 3, Table 2). A lognormal distribution was assumed for

the constant molecular clock based on this data set.

calibration points and check points.

4.3. Fossil calibration points

3.7. Congruence measures of fossil and molecular

divergence

The fossil record of Pancrustacea is extensive. To obtain cali-

bration points for the node-dating method, we assigned fossils to

On the basis of the paleontological and molecular estimates,

particular well-supported nodes of the tree of Regier et al. (2010)

we calculated a congruence metric of WSS (weighted sum of

(Fig. 2). This study adopted new fossil data (see Appendix) to

squares; Tinn and Oakley, 2008), using equation

  give a total of 35 fossil points, including 33 within Pancrustacea

n

2 2 and 2 myriapod outgroups. Fifteen of the fossil calibration points F − M /F

1( n n) n

WSS = 1 −

n were selected via relative completeness and consistency evalua-

tion (analysis not included herein) (Table 1, Fig. 2). While other

where n is each node with independent fossil and molecular calibration points are used as in previous studies (e.g., Rota-

divergence estimates. Fn is the fossil divergence estimate at node Stabelli et al., 2013), the following 7 fossil calibration points

n, and Mn is the molecular divergence estimate at node n. are newly applied or updated.

4. Results Branchiopoda: Spinicaudata-Cladocera (min: 416 Ma);

Node E in Fig. 3

4.1. Stratigraphic completeness estimate Because the fossil record of Spinicaudata is one of the oldest

among Diplostraca, extending at least from the Lower Devo-

For the current branchiopod topology (Fig. 1), the duration nian and ‘Conchostraca’ was presumed to have originated

of standard range lengths (SRL) observed is 2196 Myr, of which during the late Silurian (Tasch, 1969; Negrea et al., 1999), we

ghost lineages implied at suborder level constitute approxi- advocate a minimum constraint of 416 Ma as a conservative

mately 31.9% of the total duration. Despite a relatively high calibration point for the divergence time of Spinicaudata-

fossil completeness estimate (RCI = 68.1%), the GER (=0.49) is Cladocera.

X.-Y. Sun et al. / Palaeoworld 25 (2016) 303–317 309

Fig. 3. Fifteen fossil calibration points (green circles with letters in them; data in Table 1) on the tree. Alternative placements of Yicaris and Wujicaris labeled as C1,

C2, C3. The nodes used as checkpoints are indicated with an asterisk. Numbered nodes (1–5): targets for time estimation in this study (see results in Table 3; Fig. 5).

Outgroup (onychophoran species Peripatus) not shown. (For interpretation of the references to color in this figure legend, the reader is referred to the web version of this article.)

Table 1

Selected fossil calibration points with estimated maximum dates.

a b

Node Clade Min. calib. (Ma) Max. age (Ma)

A - 318 394

B - 396 490

C - 390 483

D Collembola- 396 490

E Cladocera-Spinicaudata 416 515

F Hoplocarida-Peracarida 411 509

G Eumalacostraca-Phyllocarida 485 601

H Pedunculata-Sessilia 306 379

I Copepoda-(, ) 500 619

J Myodocopa- 478 592

K Sarsielloidea-Cypridinidae 387 479

L - 500 619

M Miracrustacea-Vericrustacea 520 644

N Notostigmophora-Pleurostigmophora 420 520

O Diplopoda 419 519

a

Node letters used here are the same as in Fig. 3.

b

Maximum age estimated based on Marshall (2008) with confidence interval at 0.95.

310 X.-Y. Sun et al. / Palaeoworld 25 (2016) 303–317

Ostracoda: Myodocopa (Sarsielloidea-Cypridinoidea, 2009), whereas the Silurian Ramphoverritor reduncus is con-

min: 387 Ma), Podocopa (min: 478 Ma); Nodes K and J in sidered as sister-group to all extant Cirripedia (Høeg et al.,

Fig. 3 2009). The oldest undisputed crown-Cirripedia is the peduncu-

The earliest occurrence of with calcified cara- latan Illilepas damrowi (Schram, 1975) from the

paces is the Lower Ordovician (Tinn and Meidla, 2004). These (359–259 Ma) and Praelepas jaworski from the Middle Penn-

ostracods are multi-lobate forms such as the palaeocopids sylvanian (311–306 Ma) (Glenner et al., 1995; Høeg et al.,

Nanopsis nanella (Moberg and Segerberg, 1906), podocops 1999). The earliest fossils of Sessilia have been reported from

Elliptocyprites nonumbonatus (Tinn and Meidla, 2004) and Jurassic and Cretaceous. Thus we set the minimum constraint

the binodicopid Kimsella (Salas et al., 2007). for calibrating the Lepas-Semibalanus divergence at 306 Ma

The oldest myodocopids with preserved limbs and in situ (the youngest date of Pennsylvanian).

embryos are from the Upper Ordovician Katian Stage Lor- Altocrustacea-Oligostraca: the placement of Yicaris and

raine Group of New York State (ca. 450 Ma; Siveter et al., Wujicaris (min: 520 Ma); Node M (C1) in Fig. 3

2014). We advocate a minimum constraint of 478 Ma (youngest Wujicaris muelleri and Yicaris dianensis were discovered

date of Tremadocian) as the divergence time of Myodocopa- from an Orsten-type Konservat-Lagerstätte of the lower Cam-

Podocopa, on the basis of the events that major diversification brian, Southwest China (Zhang et al., 2007, 2010). According

of ostracods occurred after the Tremadocian Age (Williams to Zhang et al. (2010), the current species occurs in the

et al., 2008). Eoredlichia-Wutingapsis trilobite Zone, belonging to Cam-

Cypridinid-like myodocopids appeared in the Late Ordovi- brian Stage 3, dated 515–521 Ma.

cian (Tolmacheva et al., 2003). However, the typical pattern of Yicaris or Wujicaris can be assigned to three different nodes

fan-like adductor muscle scar first appeared in the Devonian in the phylogeny of Regier et al. (2010) (Fig. 2). The results

with Eocypridina campbelli (Wilkinson et al., 2004). The fossil from the likelihood checkpoints (Table 2) indicate a signifi-

record of Sarsielloidea is scant. On the basis of the finding that cantly better fit of the C1 calibration set. Thus, the minimum

Hamaroconcha kornickeri from the Eifelian (Middle Devo- calibration point for divergence node M is also set at 515 Ma.

nian) of southern Morocco is morphologically similar to that

of some Mesozoic and Cenozoic philomedidids (Sarsielloidea,

4.4. Divergence time estimates

Philomedidae) (Olempska and Belka, 2010), we advocate a

minimum constraint of 387 Ma (youngest date of Eifelian)

The phylogeny obtained with the software BEAST resembles

as calibration point for the Cypridinoidea-Sarsielloidea diver-

that of Regier et al. (2010). Fourteen external and one internal

gence.

fossil calibration points were used to estimate the divergence

Malacostraca: Phyllocarida (min: 485 Ma), Hoplocarida-

dates within the Branchiopoda. The divergence time estimates

Peracarida (min: 411 Ma); Nodes G and F in Fig. 3

with Multidivtime (MLT), r8s, MCMCTree, based on the super-

Phyllocarids are divided into two classes, the extinct

matrix of 62 and multiple calibrations dataset as discussed

Archaeostraca (Cambrian–Permian) and the extant Leptostraca

above, are generally concordant, overlapping within the 95%

(Permian–Recent). The oldest phyllocarid is Arenosicaris

CI limits (Table 3), although progressively older time estimates

inflata from Elk Mound Group, Cambrian Furongian of Mosi-

with broader confidence intervals toward the deeper divergences

nee, Wisconsin (Collette and Hagadorn, 2010). Phyllocarids

produced by BEAST were observed when compared to results

diversified substantially in the early Paleozoic with 83–93

of MCMCTree, r8s and MLT (Fig. 4).

named species. Thus the minimum constraint for calibrating

crown-Malacostraca is 485 Ma (youngest date of Furongian).

Hoplocarida is represented by one extant order, the Stom- 5. Discussion

atopoda, and the extinct order, Aeschronectida (Middle

Pennsylvanian). Stomatopoda includes Palaeostomatopoda 5.1. Congruence between paleontological and molecular

(Late Devonian–Late Mississippian), the Archaeostom- time scales for branchiopod evolution

atopodea (Middle Pennsylvanian–Upper Pennsylvanian), and

the Unipeltata (Upper Jurassic–Recent). The oldest hoplocarid The application of seven relaxed molecular clock methods in

is Pechoracaris aculicauda from the Early Devonian (Lochko- dating early divergences of branchiopods yields strikingly con-

vian Age) of northern Russia (Dzik et al., 2004), setting 411 Ma gruent time scales except for estimates via BEAST (see remarks

(youngest date of Lochkovian Age) as the minimum constraint above in Section 4.4.). On the basis of the paleontological and

on the divergence of Hoplocarida and Peracarida. molecular estimates, we calculated a metric WSS (weighted sum

Lepas-Semibalanus (min: 306 Ma); Node H in Fig. 3 of squares, Tinn and Oakley, 2008) to measure the congruence

This represents the divergence of Pedunculata and Ses- between paleontological and molecular time estimates (Table 3).

silia within Cirripedia (Thecostraca). Although the earliest Our congruence analyses of the molecular estimates obtained

possible cirripede has been reported from the Burgess Shale against the fossil dates of branchiopods suggest that the MCM-

(middle Cambrian), its affiliation with cirripedes or even CTree estimates based on IR (independent rate) model are

is questionable (Briggs et al., 2005). The Silu- relatively more congruent with the fossil records (see Table 3).

rian Cyprilepas holmi is interpreted to be phylogenetically Nevertheless, congruence measures for individual nodes indi-

between the cirripede stem and the Thoracica (Høeg et al., cate that for deeper divergences (nodes 5, 3, 2, Table 3; Fig. 5),

X.-Y. Sun et al. / Palaeoworld 25 (2016) 303–317 311

Table 2

Parameter and likelihood values for checkpoints used to assess fossil calibrations.

Node of divergence Distribution Mean (SD) −Ln

C1 C2 C3

D: Collembola-Diplura Lognormal 6.088 (0.054) 5.85 5.96 5.92

E: Spinicaudata-Cladocera Lognormal 6.137 (0.054) 9.97 10.08 10.04

G: Phyllocarida-Eumalacostraca Lognormal 6.295 (0.055) 19.93 42.40 48.97

a

AIC 74.51 84.80 101.95

a

AIC (Akaike Information Criterion, Akaike, 1974): to evaluate the relative goodness of fit of models of evolution.

Table 3

Divergence time estimates (Ma) using BEAST, Multidivtime, MCMCTree and r8s for major branchiopod nodes from the supermatrix and multiple calibration data

set and their compatibility with real fossil dates.

Node Fossil BEAST r8s (independent clock)

b b

Ave 95% CI WSS Ave 95% CI WSS

2 420 548 469–656 0.91 465 448–480 0.99

3 488 606 510–713 0.94 495 478–512 1.00

4 162 216 196–394 0.89 310 218–402 0.41

5 500 678 485–829 0.87 580 562–598 0.97

WSS = 0.91 WSS = 0.78

Node Fossil Multidivtime MCMCTree-IR-AA

b b

Ave 95% CI WSS Ave 95% CI WSS

2 420 491 450–522 0.97 515 475–558 0.95

3 488 532 509–552 0.99 564 522–600 0.98

4 162 278 162–384 0.49 210 92–388 0.91

5 500 562 550–575 0.98 621 595–643 0.94

WSS = 0.86 WSS = 0.94

Node Fossil MCMCTree-CR-AA MCMCTree-IR-Nuc

b b

Ave 95% CI WSS Ave 95% CI WSS

2 420 513 488–544 0.95 503 474–537 0.96

3 488 549 517–583 0.98 562 531–591 0.98

4 162 277 58–455 0.50 176 108–264 0.99

5 500 611 584–634 0.95 620 602–638 0.94

WSS = 0.85 WSS = 0.97

Notes: Node numbers used here are the same as in Fig. 3. WSS, weighted sum of squares.

MCMCTree and BEAST estimates are more congruent with the Ordovician). This result supports the hypothesis put forward by

fossil dates (with higher WSS values). Walossek (1993, 1995) that the two suborders of ‘Conchostraca’,

The time estimate for the origin of crown branchiopods (node Laevicaudata and Spinicaudata, separated from the ancestral

3) at about 495 ± 17 Ma (r8s, WSS = 1.0, Table 3) during the phyllopod probably in late Silurian. This implies that the fos-

earliest Ordovician to late Cambrian is consistent with the ear- sil record for ‘Conchostraca’ (especially for Laevicaudata) has

liest confirmed anostracan fossil (Riley Lake taxa) from the missed a substantial part of the evolutionary history, potentially

Cambrian Furongian (Harvey et al., 2012). The origin of the significant for future paleontological investigation for the group.

Phyllopoda (node 2) dated at about 465 ± 16.2 Ma It is noted that the molecular based divergence time esti-

(r8s, with highest WSS = 0.99, Table 3) possibly indicates the mation for Branchiopoda by various techniques of relaxed

time of origin of freshwater phyllopods during late Cambrian to molecular clock shows reasonably good congruence with the

Ordovician interval. fossil record (Table 3). It is interesting to note that on the

Although the fossil record so far established of Laevicau- basis of the overall WSS values for the various dating mod-

data only dates back to the Middle Jurassic and Spinicaudata els, MCMCTree estimates are most congruent (highest model

originated during the Early Devonian (Shen et al., 1982; Shen WWS = 0.97); however, when comparing the individual WSS

and Chen, 1984), the divergence between Laevicaudata and values for the deep time estimates, we found that MCMC-

the ancestor of (Spinicaudata + Cladocera) (node 1) is dated Tree produced more congruent dates for shallower divergences,

in this study at about 430–457 Ma (early Silurian to the Late whereas Multidivitime and r8s produced more congruent dates

312 X.-Y. Sun et al. / Palaeoworld 25 (2016) 303–317

Fig. 4. Comparison of divergence time estimates across four dating analyses (MCMCTree, Multidivtime, r8s, BEAST) with variable models. Each bar shows mean

and 95% confidence intervals. Node numbers are the same used in Fig. 3. CR: correlated rate model; Nuc: nucleotide sequence; IR: independent rate model; AA:

amino acid sequence; PL: penalized likelihood model.

Fig. 5. Comparison between fossil dates and molecular divergence time estimates at major branchiopod divergence nodes (node numbers refer to Fig. 3 and Table 3).

Dot line: y = x.

for deeper divergences (Table 3). We suggest that without other (mean time estimate, node 5, Table 3; Fig. 3), which is appar-

available criteria for selecting the dating models, the congruence ently too early from the view point of identifiable fossil record

measures could be adopted for choosing among varying dating for all arthropods; however, the crown group branchiopods likely

results from the different models. diverged at about during late Cambrian to earliest Ordovician,

confirming the fossil findings (see remarks above in Section 2.).

Rehm et al. (2011) utilized a large multiple sequence alignment

5.2. Comparison with previous estimates of branchiopod

derived from EST (Expressed Sequence Tags) and genomes,

divergence times

only including four representative crustaceans, resulting in a

Our divergence time estimate shows that branchiopod stem time estimate for the branchiopod-hexapod divergence in mid-

∼

lineage may be rooted deep in the Ediacaran Period at 562.9 Ma dle Cambrian ( 520 Ma) with no inference for branchiopod

X.-Y. Sun et al. / Palaeoworld 25 (2016) 303–317 313

crown group divergence timing. Wheat and Wahlberg (2013) and freshwater phyllopods originated in the Middle Ordovician.

analyzed a large phylogenomic dataset (122 panarthropod taxa, These estimated time interval fills the gap in the terrestrial fos-

62 genes) to reconstruct the arthropod time tree, resulting in sil record which is normally very poor, probably signifying the

the branchiopod-other vericrustacea divergence in the Cam- initial phase of invertebrate ’s invasion into the terrestrial

∼

brian ( 500 Ma) and the branchiopod crown group divergence environment.

at 410 Ma. Rota-Stabelli et al. (2013) presented a timescale of Although studies of molecular clock are still in their infancy,

ecdysozoan evolution using a total of 402 gene partitions across it could be shown that this interdisciplinary study can contribute

all major lineages of ecdysozoans, with 78 calibration points to a better understanding and reconstruction of evolutionary

involved, indicating the Late Ordovician radiation of crustacean processes. We suggest that fossil calibration evaluation and

and an Ordovician–Silurian divergence of branchiopod crown strategies are critical for phylochronological analyses based on

group at about 443 Ma. As discussed earlier, the branchiopod large genomic datasets and the congruence measures should

fossils assignable to crown lineages are much older than the always be used as a reference for choosing among results by

molecular time estimates by Wheat and Wahlberg (2013) and different dating models.

Rota-Stabelli et al. (2013), which probably need further investi-

gation. Our preliminary analysis suggests that a possible cause Acknowledgments

for such under-estimates may have been derived from a two strin-

gent fossil calibration constraints near the divergence notes in This work was supported by the National Natural Sci-

concern. The fragmentary nature of the fossil record and lineage ence Foundation of China (40902004, 40572070, 41272008,

extinction may also lead to the underestimation of node ages TSXK0801), Chinese Academy of Sciences (KZCX2-YW-

in a phylogenetic tree (Springer, 1995). Different branchiopod JC104), the CAS/SAFEA International Partnership Program

groups have significantly different preservation potential, thus for Creative Research Teams and the State Key Laboratory of

the fossil record is biased towards groups and structures more Palaeobiology and Stratigraphy at Nanjing Institute of Geology

conducive to fossilization, producing false signals of clustered and Palaeontology, Chinese Academy of Sciences. We thank

lineage origins that could mislead divergence time studies. The Yan-Bin Shen (NIGP, CAS) and Di-Ying Huang (NIGP, CAS)

antiquity of branchiopods and the tempo of early branchiopod for valuable discussion and comments; Jia-Sheng Hao (Anhui

diversification remain open questions in evolutionary biology. Normal University) and Gang Li (NIGP, CAS) for reviewing

In conclusion, this study shows that the crown groups of Bran- the manuscripts with encouragement and important suggestions

chiopoda originated in late Cambrian–earliest Ordovician time which helped improving the manuscript.

314 X.-Y. Sun et al. / Palaeoworld 25 (2016) 303–317 a 1 2 3 4 5 6 7 8 9 Numbers 10 11 12 13 14 15 16 17 18 19 20 21 22 23 24 25 26 27 28 29 31 32

and

(2010)

(2006) (1984) and

(2010)

(2004) (1994)

Olesen (2010)

(2004) (1981)

(1988)

(2003)

1940a)

(1926)

and

(1988) (2004) (2008)

(2007) (2012) (1987) (1987) (2004) (1984)

(2006)

(1969)

Belka (2012)

Schweitzer

Müller

al.

(2012) Jarzembowski (2010) al. (2005) Hagadorn al.

al. (2007) (2010)

Rudkin Nel al. Anderson

al.

et (1998) (1999) Trewin

(1982) Korovchinsky (2004) (1926,

and Grimaldi and Bonamo

et

(1946)

et al.

(1993) and et

Huang Chen al. Maulik

(1949) al.

et Kukalová-Peck

Meidla et al. al.

and

al. and al.

(1986)

al.

al. et and and

and

reference(s)

et et

and

et et

and (1998)

and (1969)

et and

et

and and et and et

and and

(1981) (2009) Source Walossek Harvey Scourfield Schram Shen Fayers Garrouste Tasch Shen Shen Raymond Anderson Womack Kotov Hessland Olempska Tinn Collette Dzik Feldmann Selden Collins Briggs Newman Høeg Walossek Walossek Hirst Whalley Kukalová-Peck Labandeira Engel Sturm Kukalová-Peck Riek Prokop Zhang Zhang Wilson Shear Shear

Ma

Ma

Ma)

>306

Ma Ma

Ma Ma Ma Ma

Ma

Ma

>416 Ma

Ma

318 315

>94 Ma

>318 >303 >307 ∼ ∼ >145 >164

(220–187

Ma Ma

>360 Ma

>307

Ma

Ma Ma Ma

>478 Ma

Permian, Ma Ma Ma

Ma

Ma Ma Ma Ma Ma

Ma Ma

Ma Ma

>411 >419 >140

Ma Ma Pennsylvanian, to

>359

Ma

>488 >485 >500

Jurassic

Ma

Formation, >390 >499 >515 >515 boundary,

>145

>411 >411 >407 >411 >407

>425

>505 >387 >385

>421 >420 3, 3, 3, >272

Famennian,

Early >358 Pennsylvanian, Pennsylvanian, Middle Westphalian, Pennsylvanian, Pennsylvanian, Pennsylvanian,

to

Tremadocian, Berriasian, Santana

Series Furongian, Furongian, Furongian, Series Series Pragian, Pragian, upper Lochkovian Pragian, Lochkovian, Famennian, Pragian, Givetian, Pragian, Lochkovian,

Ludlow, Wenlock, Ludlow, Bajocian–Bathonian, Tithonian,

Permian, Devonian, Cambrian, Devonian,

record

Triassic Devonian,

Oldest Cambrian, Devonian, Silurian, Jurassic, Devonian, Jurassic/Cretaceous Middle Late Devonian, Devonian, Carboniferous, Middle Silurian, Cretaceous, Carboniferous, Cambrian, Devonian, Carboniferous, Devonian, Devonian, Cretaceous, Carboniferous, Middle Devonian, Cambrian, Cambrian, Devonian, Carboniferous, Cambrian, Ordovician, Middle Cambrian, Devonian, record

Kungejia Late

sp. Jurassic,

fossil

pelturae barnetti

Protodonata Carboniferous,

pintoi reduncus

of

kornickeri

nonumbonatus fragment

hirsti the oviformis elatus

aculicauda kinnekullensis

tuberculatus

inflata mapesi

campbelli zherikhini wilsonae

rhyniensis delta

fragments beipiaoensis taxa spp. Silurian, indet. Devonian, Ketmenia,

thomasi

Paoliidae Carboniferous,

jaworski

in

Lepismatidae muelleri praecursor

species of

dianensis

Lake

Gaspé

abdominal

Yicaris Arenosicaris Lepidocaris Palaeochirocephalus Notostraca Ebullitiocaris Rehbachiella Almatium, Prolynceus Palaeolimnadiopseidae Cyclestherioides Archelatona Elliptocyprites Hamaroconcha Eocypridina Pechoracaris Aciculopoda Fragments Priscansermarinus Ramphoverritor Brachylepascretacea Praelepas Bockelericambrian Rhyniella Testajapyx Two Unnamed Lithoneura Various Species Wujicaris Paleodesmus Crussolum Devonobius Riley Castracollis An Ebullitiocaris

of

group

group

group

group

part

stem

stem

stem crown

and

Sarsielloidea Hoplocarida Archaeognatha Notostigmophora Phyllocarida Collembola Anostraca Anostraca Notostraca Spinicaudata Cyclestherida Cypridinoidea Peracarida Lepadomorpha Pedunculata Diplura Dicondylia Ephemeroptera Neoptera Pleurostigmophora Kazacharthra Cladocera Metacopa Canthocamptidae Zygentoma Heteralepadomorph Sessilia Laevicaudata Branchiopod Pancrustacea

of

. group 2

group group

Fig.

Myodocopa Eumalacostraca Crown Insecta Chilopoda Stem Sarsostraca Calmanostraca Diplostraca Podoplea Stem Podocopa Dipopoda in

occurrences

those

to

Oldest

Corresponding a Malacostraca Copepoda Thecostraca Pentastomida Eucrustacea Entomostraca Appendix. Taxon Branchiopoda Ostracoda Myriapoda

X.-Y. Sun et al. / Palaeoworld 25 (2016) 303–317 315

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