PALEONTOLOGY The nearshore cradle of early vertebrate diversification › content › sci › 362...
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PALEONTOLOGY The nearshore cradle of early vertebrate diversification Lauren Sallan 1 *†, Matt Friedman 2 , Robert S. Sansom 3 , Charlotte M. Bird 4 , Ivan J. Sansom 4 *† Ancestral vertebrate habitats are subject to controversy and obscured by limited, often contradictory paleontological data. We assembled fossil vertebrate occurrence and habitat datasets spanning the middle Paleozoic (480 million to 360 million years ago) and found that early vertebrate clades, both jawed and jawless, originated in restricted, shallow intertidal- subtidal environments. Nearshore divergences gave rise to body plans with different dispersal abilities: Robust fishes shifted shoreward, whereas gracile groups moved seaward. Fresh waters were invaded repeatedly, but movement to deeper waters was contingent upon form and short-lived until the later Devonian. Our results contrast with the onshore-offshore trends, reef-centered diversification, and mid-shelf clustering observed for benthic invertebrates. Nearshore origins for vertebrates may be linked to the demands of their mobility and may have influenced the structure of their early fossil record and diversification. T he ancestral habitat of vertebrates has long been debated, with opinions ranging from freshwater to open ocean habitats (1–3). Inferences have been derived from either the evolutionarily distant modern fauna or qualitative narratives based on select fossils. Ear- ly records of vertebrate divisions, such as jawed fishes and their relatives (total-group gnatho- stomes), consist of long gaps between inferred origination and definitive appearances (ghost lineages), punctuated by suggestive microfossils (4–7). Vertebrates, apart from toothlike conodont elements, were restricted in Ordovician eco- systems as trivial components of the Great Ordo- vician Biodiversification Event (4, 5, 7). Ancestral habitat is a critical factor in determining both pattern and mode of diversification, potential mismatches between biodiversity and available habitat area, and the source of apparent relation- ships with changing sea level (6). A lack of early vertebrate fossil data and habitat information in compendia has limited quantitative approaches (4), preventing resolution of this outstanding is- sue in vertebrate evolution. We developed a database of total-group gnatho- stome occurrences (~480 million to 360 million years ago) (4, 5, 8) during their mid-Paleozoic diversification (n = 2827) (9) (fig. S1). Data collec- tion focused on all occurrences from the interval encompassing the five oldest localities for each major clade (n = 188) (Fig. 1 and figs. S1 and S2) and phylogenetically constrained genera within jawless groups (n = 785) (Figs. 2 and 3 and figs. S1, S3, and S4) for use with Bayesian ancestral state reconstruction. We used environmental, lith- ological, and invertebrate community information from the literature and available databases to assign occurrences to benthic assemblage zones (10) (Fig. 1). Benthic assemblage zones are cate- gorized and ordered as fresh water (BA0); inter- tidal above typical wave base (BA1); shallow subtidal and/or lagoon (BA2); deeper subtidal, in- cluding the start of tabulate coral –stromatoporoid reef systems (BA3); middle to outer shelf (BA4 and BA5); and shelf margin toward the bathyal region (BA6). These zones have been widely used in studies of mid-Paleozoic paleocommunities (1, 10–12) (Fig. 1). We applied Bayesian threshold models to phy- logenies of occurrences using prior probabilities of residence in each benthic assemblage zone. This methodology allowed positive inference of both ancestral habitats and amount of evolution- ary change required to move between zones (“liability” values) (13). All major clades, from the first skeletonizing jawless fishes (astraspids, arandaspids) to jawed bony fishes (osteichthyans), originated within nearshore intertidal and sub- tidal zones (~BA1 to BA3), centered on BA2, over a period of more than 100 million years (Fig. 1A and fig. S3). This area is relatively shallow, in- cludes lagoons in reefal systems, and is located entirely above the storm wave base in the mid- Paleozoic (11) (Fig. 1). We appraised whether nearshore origination in gnathostomes resulted from environmental bias in the record through comparison with habitat distributions for other facets of the mid- Paleozoic captured in independent datasets, including fossiliferous strata, regional paleocom- munities, and global occurrences and richness (number of genera) (Fig. 1B and figs. S11 to S16) (10, 14). Analysis of mid-Paleozoic strata in the Paleobiology Database (PBDB) (14), binned by distinct habitat categories (n = 4437), produced a distribution clustered on deep subtidal and reef environments [equivalent to BA3 and BA4 RESEARCH Sallan et al., Science 362, 460–464 (2018) 26 October 2018 1 of 4 1 Department of Earth and Environmental Science, University of Pennsylvania, Philadelphia, PA 19104, USA. 2 Museum of Paleontology, University of Michigan, Ann Arbor, MI 48109, USA. 3 School of Earth and Environmental Sciences, University of Manchester, Manchester M13 9PT, UK. 4 School of Geography, Earth and Environmental Sciences, University of Birmingham, Birmingham B15 2TT, UK. *Corresponding author. Email: [email protected] (L.S.); [email protected] (I.J.S.) †These authors contributed equally to this work. Fig. 1. Mid-Paleozoic vertebrates preferentially originated in shallow marine habitats. (A) Intertidal (BA1) to subtidal (BA2 and BA3) ancestral habitats for total-group gnathostome clades (n = 188), assuming placoderm paraphyly and Silurian first occurrence for chondrichthyans. Full results are shown in figs. S2 to S5. Wen., Wenlock; Lud., Ludlow; Pri., Pridoli. (B) Silurian and Lochkovian marine distributions for PBDB fossiliferous strata (n = 858), richness (n = 6980), and occurrences (n = 30,004); conodont richness (n = 505) and occurrences (n = 7447); paleocommunities (n = 2401); and gnathostome occurrences (n = 1035) show mid-Paleozoic records peaking on the mid-shelf (BA3 and BA4) with few records in marginal marine settings, in contrast to the shallow-water preferences of early gnathostomes. (C) Early and overall occurrences for total-group gnathostomes (n = 2827), jawed fishes (n = 1343), and jawless fishes (n = 1484) show that early occurrences were significantly more concentrated in shallow marine settings (BA1 and BA2) than overall or later occurrences. See data S2 and figs. S1 and S5 to S9.
Transcript of PALEONTOLOGY The nearshore cradle of early vertebrate diversification › content › sci › 362...
PALEONTOLOGY
The nearshore cradle of earlyvertebrate diversificationLauren Sallan1*†, Matt Friedman2, Robert S. Sansom3,Charlotte M. Bird4, Ivan J. Sansom4*†
Ancestral vertebrate habitats are subject to controversy and obscured by limited, oftencontradictory paleontological data.We assembled fossil vertebrate occurrence and habitatdatasets spanning the middle Paleozoic (480 million to 360 million years ago) and found thatearly vertebrate clades, both jawed and jawless, originated in restricted, shallow intertidal-subtidal environments. Nearshore divergences gave rise to body plans with different dispersalabilities: Robust fishes shifted shoreward, whereas gracile groups moved seaward. Freshwaters were invaded repeatedly, but movement to deeper waters was contingent upon formand short-lived until the later Devonian. Our results contrast with the onshore-offshore trends,reef-centered diversification, and mid-shelf clustering observed for benthic invertebrates.Nearshore origins for vertebrates may be linked to the demands of their mobility and mayhave influenced the structure of their early fossil record and diversification.
The ancestral habitat of vertebrates has longbeen debated, with opinions ranging fromfreshwater to open ocean habitats (1–3).Inferences have been derived from eitherthe evolutionarily distant modern fauna or
qualitative narratives based on select fossils. Ear-ly records of vertebrate divisions, such as jawedfishes and their relatives (total-group gnatho-stomes), consist of long gaps between inferredorigination and definitive appearances (ghostlineages), punctuated by suggestive microfossils(4–7). Vertebrates, apart from toothlike conodontelements, were restricted in Ordovician eco-systems as trivial components of the Great Ordo-vician Biodiversification Event (4, 5, 7). Ancestralhabitat is a critical factor in determining bothpattern and mode of diversification, potentialmismatches between biodiversity and availablehabitat area, and the source of apparent relation-ships with changing sea level (6). A lack of earlyvertebrate fossil data and habitat information incompendia has limited quantitative approaches(4), preventing resolution of this outstanding is-sue in vertebrate evolution.Wedeveloped a database of total-group gnatho-
stome occurrences (~480 million to 360 millionyears ago) (4, 5, 8) during their mid-Paleozoicdiversification (n = 2827) (9) (fig. S1). Data collec-tion focused on all occurrences from the intervalencompassing the five oldest localities for eachmajor clade (n = 188) (Fig. 1 and figs. S1 and S2)and phylogenetically constrained genera withinjawless groups (n = 785) (Figs. 2 and 3 and figs.
S1, S3, and S4) for use with Bayesian ancestralstate reconstruction. We used environmental, lith-ological, and invertebrate community informationfrom the literature and available databases toassign occurrences to benthic assemblage zones(10) (Fig. 1). Benthic assemblage zones are cate-gorized and ordered as fresh water (BA0); inter-tidal above typical wave base (BA1); shallowsubtidal and/or lagoon (BA2); deeper subtidal, in-cluding the start of tabulate coral–stromatoporoid
reef systems (BA3); middle to outer shelf (BA4and BA5); and shelf margin toward the bathyalregion (BA6). These zones have been widely usedin studies of mid-Paleozoic paleocommunities(1, 10–12) (Fig. 1).We applied Bayesian threshold models to phy-
logenies of occurrences using prior probabilitiesof residence in each benthic assemblage zone.This methodology allowed positive inference ofboth ancestral habitats and amount of evolution-ary change required to move between zones(“liability” values) (13). All major clades, fromthe first skeletonizing jawless fishes (astraspids,arandaspids) to jawedbony fishes (osteichthyans),originated within nearshore intertidal and sub-tidal zones (~BA1 to BA3), centered on BA2, overa period of more than 100 million years (Fig. 1Aand fig. S3). This area is relatively shallow, in-cludes lagoons in reefal systems, and is locatedentirely above the storm wave base in the mid-Paleozoic (11) (Fig. 1).We appraised whether nearshore origination
in gnathostomes resulted from environmentalbias in the record through comparison withhabitat distributions for other facets of the mid-Paleozoic captured in independent datasets,including fossiliferous strata, regional paleocom-munities, and global occurrences and richness(number of genera) (Fig. 1B and figs. S11 to S16)(10, 14). Analysis of mid-Paleozoic strata in thePaleobiology Database (PBDB) (14), binned bydistinct habitat categories (n = 4437), produceda distribution clustered on deep subtidal andreef environments [equivalent to BA3 and BA4
RESEARCH
Sallan et al., Science 362, 460–464 (2018) 26 October 2018 1 of 4
1Department of Earth and Environmental Science, Universityof Pennsylvania, Philadelphia, PA 19104, USA. 2Museum ofPaleontology, University of Michigan, Ann Arbor, MI 48109,USA. 3School of Earth and Environmental Sciences,University of Manchester, Manchester M13 9PT, UK. 4Schoolof Geography, Earth and Environmental Sciences, Universityof Birmingham, Birmingham B15 2TT, UK.*Corresponding author. Email: [email protected] (L.S.);[email protected] (I.J.S.)†These authors contributed equally to this work.
Fig. 1. Mid-Paleozoic vertebrates preferentially originated in shallow marine habitats.(A) Intertidal (BA1) to subtidal (BA2 and BA3) ancestral habitats for total-group gnathostome clades(n = 188), assuming placoderm paraphyly and Silurian first occurrence for chondrichthyans. Full results areshown in figs. S2 to S5.Wen.,Wenlock; Lud., Ludlow; Pri., Pridoli. (B) Silurian and Lochkovian marinedistributions for PBDB fossiliferous strata (n = 858), richness (n = 6980), and occurrences (n = 30,004);conodont richness (n = 505) and occurrences (n = 7447); paleocommunities (n = 2401); and gnathostomeoccurrences (n = 1035) show mid-Paleozoic records peaking on the mid-shelf (BA3 and BA4) with fewrecords in marginal marine settings, in contrast to the shallow-water preferences of early gnathostomes.(C) Early and overall occurrences for total-group gnathostomes (n = 2827), jawed fishes (n = 1343), andjawless fishes (n = 1484) show that early occurrences were significantly more concentrated in shallowmarine settings (BA1 and BA2) than overall or later occurrences. See data S2 and figs. S1 and S5 to S9.
(10)], with many fewer records in freshwater-marginal marine (BA0 and BA1) and the basinand slope (~BA5 and BA6) zones (Fig. 1B andfigs. S11 and S12). PBDB records of occurrences(n = 111,364) or genera (n = 24,211) provide dis-tributions that show even greater clustering onthemid-shelf but are highly correlated with sam-pled strata (linear regression: r2 = 0.96,P=0.0004and r2 = 0.94, P = 0.0008, respectively) (fig. S12).Silurian and Lochkovian regional paleocommuni-ties (10) are also centered onBA3 andBA4 (Fig. 1Band fig. S13). These records suggest a global, mid-shelf center for sampling and diversity and a nullexpectation of originations in deep subtidal andreef environments [more so than expected fromprevious studies focused on reef-bearing facies(15)]. This is in stark contrastwith shallowergnatho-stome ancestral habitats (Fig. 1) and is thus un-likely to result from global sampling bias.To evaluate whether apparent nearshore orig-
ination resulted from preservational biases indifferent habitats, we compared gnathostomedistributions to PBDB records for conodonts. Con-odonts are the sister group of extant jawlesscyclostomes or the vertebrate total-group, largelyknown from phosphatic oral elements (4), whichserve as an independent preservational proxy.Conodonts are stratigraphic index fossils andcommon along themarine depth gradient duringthe mid-Paleozoic (Fig. 1B and fig. S14). Conodontoccurrences (n = 11,915) show a different distri-bution from other PBDB records (chi-squaredP < 0.0001), exhibiting a peak in BA2 and moreoccurrences in BA5 and BA6 (figs. S14 and S15).Conodont richness (n = 1308) is more clusteredaround BA3 and BA4, particularly in the Silurian-Lochkovian (n = 505) (Fig. 1B and figs. S14 andS15). This pattern argues against early gnatho-stome restriction resulting from preservationalbias, as does the plurality of vertebrate occur-rences in deeper waters from the early Silurian(Fig. 1C and fig. S1).Jawed and jawless fish distributions are highly
clustered in BA0 to BA2 early in clade history(n = 478), in the Silurian and Lochkovian (n =1035), and over the mid-Paleozoic (n = 2147)(Fig. 1 and figs. S1 and S16 to S18). We recover nosignificant or strong positive correlations betweenthis gnathostome pattern and other fossil records(linear regression r2 range: −0.90 to 0.27, P range:0.41 to 0.9) (Fig. 1B and fig. S16).Ancestral states show that gnathostomes orig-
inated preferentially near shore, even as thediversity of species and body forms increased(Fig. 1A and fig. S2). Early occurrences are sig-nificantly different from later records withingroups (chi-squared P = < 0.00001) (Fig. 1C andfig. S18); gnathostomes as a whole, as well asjawed and jawless fishes specifically, exhibitgreater clustering in shallowmarine settings (BA1and BA2), independent of exact time of first ap-pearance in themid-Paleozoic (Fig. 1C and fig. S18).Shallow ancestral habitats are always supportedby our analyses despite variation in first ap-pearances of jawed fishes (e.g., inclusion of po-tential Ordovician “chondrichthyan” material)(15); placodermmonophyly or paraphyly (8); and
Sallan et al., Science 362, 460–464 (2018) 26 October 2018 2 of 4
Fig. 2. Macromeric, robust jawless fishes exhibit shallower-water diversification and greaterhabitat restriction. Ancestral states for (A) heterostracans and Ordovician (Ord.) stem-gnathostomes (n = 316), (B) galeaspids (n = 112), and (C) osteostracans (n = 158) show thatmacromeric genera preferentially originated in very shallow waters (BA0 to BA2), with the exceptionof more streamlined forms. Full results are shown in figs S6 to S8. (D) Early and overall habitatdistributions for macromeric clades (n = 1123), showing significant shifts toward shallower watersubsequent to their origination. Full distributions are shown in figs. S19 and S20 and data S1.
RESEARCH | REPORT
even increasing the minimum prior probabilityof occurrences in all zones to a minimum of 5 or10% to account for potential of false absence,missing records, or other sampling issues (Fig. 1A,figs. S2 to S5, and table S1). Gnathostomes con-tinued to show a strong tendency to diverge inshallow marine waters long after the invasionof deeper and fresh waters by older lineages,including after the origin of jaws.Threshold liability values suggest that shifts
within the nearshore waters required little evo-lutionary change and were common, as wasinvasion of fresh water (Table 1 and Fig. 1C).Dispersal into deeper waters, including the
forereef, shelf, and open ocean (BA4 to BA6), wasmore restricted (Table 1), complicated by a short-term tendency to return to the ancestral shal-lows [Ornstein-Uhlenbeck deviance informationcriterion (OU DIC) weight = 1; phylogenetichalf-life in Table 1] (16). Yet, threshold valuesalso suggest rapid dispersal across the offshoreshelf (BA4 and BA5) once lineages managedto depart BA3, even though shifts into openwaters (BA6) had much higher requirements(Table 1). However, if sampling probabilities inall bins is increased a priori, shallow-water re-striction of early gnathostomes is explainedby ever-higher thresholds for continued move-
ment offshore, starting at BA2 (Fig. 1A, figs. S2to S5, and table S1).Next, we determined the association between
body form and dispersal ability within majorgroups. Clades were categorized into two bodyforms: (i) macromeric, which are mostly robustand armored with large bony plates (e.g., het-erostracans, osteostracans, and galeaspids) (17)(Fig. 2), or (ii) micromeric, which are mostlygracile and either naked or covered in smallscales (e.g., thelodonts and anaspids) (17) (Fig. 3).These robust or gracile forms can be approxi-mated as having benthic or pelagic and nektoniclifestyles, respectively, given their gross similarityto living fishes (18, 19).Analysis of all gnathostome early occurrences
shows that both micromeric and macromericforms originated around shallow water (BA2)(Fig. 1A and fig. S2). However, group-level ana-lyses suggest that slight shifts shoreward or sea-ward preceded the later diversification of thesegroups. Genus-level diversification of macromericjawless lineages was centered in the shallows(BA1 and BA2) and freshwater (BA0) throughouttheir multimillion-year existence (Fig. 2 and figs.S6 to S8, S19, and S20). Later occurrences weresignificantly more clustered in shallow andfreshwater settings than the earliest members ofthese clades (chi-squared P < 0.0001) (Fig. 2Cand figs. S19 and S20). Threshold values indicatethat moving into deeper waters was more dif-ficult for robust groups than gnathostomes as awhole (Table 1 and tables S1 and S2), and thesefeatured a strong tendency to return to the shal-lows (OU DIC weight range = 0.99 to 1; phylo-genetic half-life in Table 1).The diversification of micromeric gnatho-
stomes was centered in deeper subtidal waters(BA3) following their origination in BA2 (Figs. 1Aand 3 and figs. S9, S10, S21, and S22). Early oc-currences of these clades show a significantlygreater concentration in BA1 and BA2 than laterforms (chi-squared P < 0.0001) (fig. S21 and S22).A handful of early Silurian thelodont taxa werealready resident in deeper waters (BA3 to BA5)following their Late Ordovician appearances inBA1 and BA2 (fig. S21A). Early dispersal intodeeper waters reflects low threshold parameters(Table 1) andmay be a general pattern for gracile
Sallan et al., Science 362, 460–464 (2018) 26 October 2018 3 of 4
Fig. 3. Micromeric, gracile jawless fishes exhibit deeper-subtidal later diversification andeasier dispersal. Ancestral states for (A) thelodonts (n = 99) and (B) anaspids (n = 100), showingdiversification of genera in deeper subtidal waters (BA3) during their evolutionary history. Fullresults are shown in figs. S9 and S10. (C) Early and overall occurrences for micromeric jawlessfishes (n = 353) show a rapid shift to deeper waters following nearshore origination. Full distributionsare shown in figs. S21 and S22 and data S1.
Table 1. Best-fit model parameters for ancestral habitats. ancThresh (Ancestral Character Estimation Under The Threshold Model Using Bayesian MCMC)
(13) holds the threshold for exiting BA0 constant at 0 and the value for exiting BA6 as infinity (Inf). Values for parameters (log-likelihood and alpha) are means
after excluding “burn in.” See figs. S2 and S10 and (29) for ancestral states. Phylogenetic half-lives are given in million years. mil. gen., million generations.
Clade
Mean threshold liabilities
(20 mil. gen., 20% burn-in) Log-likelihood Alpha Half-life
BA0 BA1 BA2 BA3 BA4 BA5 BA6
Gnathostomes 0 2.09 3.98 6.24 6.81 97.48 Inf −657.77 0.13 5.33.. .. ... ... .. ... .. ... ... .. ... ... .. ... .. ... ... .. ... ... .. ... ... .. ... .. ... ... .. ... ... .. ... .. ... ... .. ... ... .. ... ... .. ... .. ... ... .. ... ... .. ... .. ... ... .. ... ... .. ... ... .. ... .. ... ... .. ... ... .. ... .. ... ... .. ... ... .. ... ... .. ... .. ... ... .. ... ... .. ... .. ... ... .. ... ... .. ... ... .. ... .. ... ... .. ... ... .. ... .. ... ... .. ... ... .. ... ... .. ... .. ... ... .. ... ... .
Heterostracans 0 2.92 3.86 7.74 38.20 200.13 Inf −979.86 0.12 5.78.. .. ... ... .. ... .. ... ... .. ... ... .. ... .. ... ... .. ... ... .. ... ... .. ... .. ... ... .. ... ... .. ... .. ... ... .. ... ... .. ... ... .. ... .. ... ... .. ... ... .. ... .. ... ... .. ... ... .. ... ... .. ... .. ... ... .. ... ... .. ... .. ... ... .. ... ... .. ... ... .. ... .. ... ... .. ... ... .. ... .. ... ... .. ... ... .. ... ... .. ... .. ... ... .. ... ... .. ... .. ... ... .. ... ... .. ... ... .. ... .. ... ... .. ... ... .
Galeaspids 0 3.31 5.91 15.53 83.03 200.55 Inf −446.63 0.01 138.63.. .. ... ... .. ... .. ... ... .. ... ... .. ... .. ... ... .. ... ... .. ... ... .. ... .. ... ... .. ... ... .. ... .. ... ... .. ... ... .. ... ... .. ... .. ... ... .. ... ... .. ... .. ... ... .. ... ... .. ... ... .. ... .. ... ... .. ... ... .. ... .. ... ... .. ... ... .. ... ... .. ... .. ... ... .. ... ... .. ... .. ... ... .. ... ... .. ... ... .. ... .. ... ... .. ... ... .. ... .. ... ... .. ... ... .. ... ... .. ... .. ... ... .. ... ... .
Osteostracans 0 1.13 2.90 26.27 51.66 94.34 Inf −433.09 0.08 8.66.. .. ... ... .. ... .. ... ... .. ... ... .. ... .. ... ... .. ... ... .. ... ... .. ... .. ... ... .. ... ... .. ... .. ... ... .. ... ... .. ... ... .. ... .. ... ... .. ... ... .. ... .. ... ... .. ... ... .. ... ... .. ... .. ... ... .. ... ... .. ... .. ... ... .. ... ... .. ... ... .. ... .. ... ... .. ... ... .. ... .. ... ... .. ... ... .. ... ... .. ... .. ... ... .. ... ... .. ... .. ... ... .. ... ... .. ... ... .. ... .. ... ... .. ... ... .
Anaspids 0 0.19 0.34 1.35 1.40 103.24 Inf −142.24 1.95 0.36.. .. ... ... .. ... .. ... ... .. ... ... .. ... .. ... ... .. ... ... .. ... ... .. ... .. ... ... .. ... ... .. ... .. ... ... .. ... ... .. ... ... .. ... .. ... ... .. ... ... .. ... .. ... ... .. ... ... .. ... ... .. ... .. ... ... .. ... ... .. ... .. ... ... .. ... ... .. ... ... .. ... .. ... ... .. ... ... .. ... .. ... ... .. ... ... .. ... ... .. ... .. ... ... .. ... ... .. ... .. ... ... .. ... ... .. ... ... .. ... .. ... ... .. ... ... .
Thelodonts 0 0.61 0.93 2.05 2.15 110.77 Inf −220.20 0.59 1.17.. .. ... ... .. ... .. ... ... .. ... ... .. ... .. ... ... .. ... ... .. ... ... .. ... .. ... ... .. ... ... .. ... .. ... ... .. ... ... .. ... ... .. ... .. ... ... .. ... ... .. ... .. ... ... .. ... ... .. ... ... .. ... .. ... ... .. ... ... .. ... .. ... ... .. ... ... .. ... ... .. ... .. ... ... .. ... ... .. ... .. ... ... .. ... ... .. ... ... .. ... .. ... ... .. ... ... .. ... .. ... ... .. ... ... .. ... ... .. ... .. ... ... .. ... ... .
RESEARCH | REPORT
clades. Jawed fishes show a significant shift ontoreefs and deeper settings in the later Devonian(chi-squared P < 0.0001) (Fig. 1C and figs. S1 andS18), after the appearanceofmost subclades.Robustjawless groups contain exceptions that may provethis rule: A few subcladeswith fusiform bodies (e.g.,tremataspid osteostracans) originated in BA3 andregister deeper-water occurrences than their rela-tives by themid-Silurian (Fig. 2 and figs. S6 to S8).Dispersal in multiple directions appears to
have been enabled by body-form evolution anddid not precede the origin of new phenotypes innew habitats. These shifts affected subsequentsurvival. Freshwater habitats were marked bythe persistence of robust clades such as osteos-tracans and gracile forms such as anaspids, with-out further changes to their gross body plan (Figs.2 and 3). Sometimes, identical deep-water lineagesappear short-lived and did not exhibit apparentfurther diversification, even on reefs (Fig. 1) (20).Jawless gnathostomes show a significant shift indistribution (chi-squared P < 0.00001) back intothe ancestral nearshore habitats and adjacentestuarine areas following a peak in distributionacross the depth gradient in the Silurian to EarlyDevonian (Fig. 1C and figs. S1 and S18). Thisshift occurred just as jawed fishes moved out ofnearshore habitats in the Devonian (Fig. 1A andfig. S18) (4, 21). This pattern is reflected in thegreater representation of benthic forms in latermarine jawless fishes versus nektonic forms injawed vertebrates (22).Overall, our results show that the nearshore
served as the cradle of early vertebrate taxo-nomic and gross morphological diversification(Figs. 1 to 3). Specific body forms evolved incoastal waters subsequently favoring expan-sion into shallower (e.g., macromeric jawlessfishes) or deeper areas (e.g., micromeric jawlessfishes, jawed fishes). This mirrors observationswithin living fishes of repeated splits into ben-thic or pelagic and nektonic forms (18, 23), aswell as the gross division of fish phenotype-environment associations (19).A persistent diversification center within the
shallows may explain features of the early verte-brate record (7, 24). Ordovician gnathostomes
are primarily represented by microfossils re-stricted to a small subset of nearshore facies(fig. S1) subject to wave action (11), despiteworldwide distributions (4, 7, 17, 24). Ghost lin-eages for gnathostomes might be caused by envi-ronmental endemicity, low abundance, and/or arelative lack of marginal marine strata (figs. S1and S11 to S13). Alternatively, a relationship be-tween Ordovician diversity and sea level (6)might have a common cause in changing shallowhabitat area; reduction in such environmentswould have delayed apparent diversification andincreased extinction risk (6, 25, 26).Endemicity in coastal waters may have later
promoted origination of new clades. Biogeographicpatterns suggest that body-form divergence oc-curred in multiple shallow settings, increasingoverall diversity.Micromeric forms occur alongsidemacromeric astraspids in the Ordovician ofLaurentia, whereas robust galeaspids existedalongside gracile chondrichthyans in the earlySilurian of Gondwana (4–7, 15, 17, 24, 27, 28).Nektonic body plans developed in these hotspotsenableddispersal acrossdeep early Silurianoceans,away from local competition, leading to furtherdiversification in nearshore settings elsewhere(1, 15, 28). In contrast, benthic groups showedstructured geographic patterns (27),moving alongcoastlines and inshore, perhaps toward nutrientinputs essential to their likely bottom-feeding andfiltering lifestyles and away from increased com-petition. Thus, continuous origination in shallowwaters shaped the evolution of vertebrates, atleast during their first phase of diversification.
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ACKNOWLEDGMENTS
We thank Z. Min, for assistance with galeaspid occurrences;L. Revell, G. Lloyd, and J. Mitchell for advice on phylogeneticmethods; S. Wang for assistance with statistical tests; N. Tamurafor providing the reconstructions used in Figs. 1 to 3; andD. Fraser and three anonymous reviewers for comments. Funding:This work was supported by the University of Pennsylvania(L.S.), a Palaeontological Association Undergraduate ResearchBursary (C.M.B.), and the University of Birmingham (I.J.S). Authorcontributions: L.S. and I.J.S. designed the study, assembledthe figures, interpreted results, and drafted the manuscript. L.S.,R.S.S., C.M.B., and I.J.S. contributed data. L.S. performed analyses.L.S., M.F., R.S.S., C.M.B., and I.J.S. participated in designing analyses,discussing results, and editing the manuscript. Competinginterests: None declared. Data and materials availability: Alldata are available in the supplementary materials and at (29).
SUPPLEMENTARY MATERIALS
www.sciencemag.org/content/362/6413/460/suppl/DC1Materials and MethodsSupplementary TextFigs. S1 to S23Tables S1 to S3References (30–61)Data S1 to S3
31 October 2017; accepted 2 October 201810.1126/science.aar3689
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