Supplementary Material

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Supplementary Material

Paleogenomics of Pterosaurs and the Evolution of Small Genome Size in Flying

Vertebrates

Chris L. Organ and Andrew M. Shedlock

Supplementary Figure 1: Pterodactylus (wing phalanx)

Supplementary Table 1: Summary of Bone Histology and Genome Size Data. Descriptive statistics of primary histological measurements. Gray text indicates data taken from Organ et al. 2007. The data from the extinct species were used to infer genome size using the Bayesian comparative method detailed below. Data from the genus Xenopus were included from Reumer and Thiebaud (1987), in which measurements of osteocyte lacunae were performed on the thin central area of the ossified suprascapular.

 is the standard deviation and C-Val is the haploid genome size in picograms.

Taxon Bone Element n

Lacunae

Avg Vol

(

 m3)

 C-Val

(pg)

Extant Taxa

Bison bison

Sorex araneus

Femur

Mandible

30

34

303.64

161.27

101.12

45.6

4.9

2.91

Loxodonta africana

Falco sparverius

Tyto alba

Corvus brachyrhynchos

Femur

Vomeronasal

Vomeronasal

Vomeronasal

29

20

208.68

58.52

87.84

25.95

4.28

1.43

27 128.39 41.57 1.63

28 37.99 12.78 1.25

Phalacrocorax auritus

Erinaceus europaeus

Regulus calendula

Xenopus laevis

Xenopus ruwenzoriensis

Xenopus vestitus

Vomeronasal

Tibia

Vomeronasal

Suprascapular

Suprascapular

Suprascapular

28

26 106.81 54.23 3.66

26

50

50

25

52 16.08 1.43

35.08

636

1143

14.08

180

1979 1535

757

1.33

3.3

7.9

6.1

Alligator mississippiensis

Ateles paniscus

Bos taurus

Femur

Turbinates

Tibia

33 197.98 25.56 2.49

20 290.3 50.55 3.47

37 207.04 20.45 3.59

Organ and Shedlock, Page 2

Taxon Bone Element

Canis familiaris

Canis latrans

Capra hircus

Chrysemys picta

Corvus corax

Crocodylus niloticus

Dendroica dominica

Didelphis virginiana

Dromaius novaehollandiae

Eptesicus fuscus

Gekko sp.

Homo sapiens

Iguana iguana

Meleagris gallopavo

Turbinates

Femur

Tibia

Humerus

Turbinates

Humerus

Turbinates

Femur

Tibia

Turbinates

Skull

Femur

Skull

Femur

Ornithorhynchus anatinus

Oryctolagus cuniculus

Phylloderma stenops

Pteropus giganteus

Rana pipiens

Rattus norvegicus

Struthio camelus

Ursus arctos

Tibia

Femur

Turbinates

Turbinates

Ilium

Turbinates

Tibia

Femur

Varanus sp. Femur

Basal Archosauromorphs (extinct)

Champsosaurid indet. Femur, humerus

Desmatosuchus haploceros Scute

Basal alligatorid

(Leidyosuchus sp.)

Phytosaurid indet.

Scute

Scute

Postosuchus kirkpatricki

Rutiodon sp.

Typothorax meadei

Pterosaurs (extinct)

Humerus

Femur

Femur

Dimorphodon macronyx Tibia, wing phalanx

Rhamphorhynchus muensteri Radius

Pteranodon sp.

Pterodactylus sp.

Wing phalanx

Femur, wing phalanx n

Lacunae

Avg Vol

(

 m3)

 C-Val

(pg)

20 142.97 26.64 3.12

40 149.18 19.51 2.82

40 160.86 15.9 3.24

40 166.97 24.93 2.8

20 95.12 9.58 1.21

37 245.81 31.86 3.21

20 53.27

40 110.35

5.46 1.4

9.49 4.12

40 95.22 12.76 1.63

20 115.38 17.96 2.37

38 337.2 53.93 2.56

20 274.04 39.05 3.5

27

40

270.8

58.82

47.49

6.36

2.89

1.54

35 160.04 15.85 3.06

40 196.76 20.6 3.18

20 145.26 27.02 2.48

18 155.28 25.31 2.22

40 444.36 56.93 6.76

20 240.68 36.84 3.36

40

40

83.83

173.4

9.72

19.5

2.16

2.75

40 138.3 14.66 2.05

22

32

16

34

32

22

38

583.7 248.1 ?

340.4 130.91 ?

375.6 167.11 ?

16 429.04 196.91 ?

28 86.97 28.38 ?

27 100.29 27.67 ?

22 330.28 125.74 ?

81.19 32.64 ?

76.21 21.96 ?

84.95 24.25 ?

99.28 27.01 ?

Phylogenetic Framework and Divergence Times

For the cell size-genome size analysis tree topology and divergence times were maintained from

Organ et al. (2007), with divergence times for the additional extant taxa obtained using http://www.timetree.net

(Hedges et al. 2006) and data from the literature (Rest et al. 2003; Evans et al.

2004; Springer et al. 2004; Benton and Donoghue 2007). Topology and divergence times were estimated for the additional genera using a mixture of fossil and molecular divergence dates as follows:

Organ and Shedlock, Page 3

Rana and Xenopus (Evans et al. 2004; Marjanović and Laurin 2007); Phalacrocorax, Falco, Tyto, Corvus, and Regulus (Ericson et al. 2006); Erinaceus, Sorex, Loxodonta, Bison (Springer et al. 2003; Delsuc et al.

2004; Hassanin and Ropiquet 2004). Phylogenetic information for extinct species were also collected for Pterosauria (Kellner 2003; Unwin 2003), Archosauria (Benton 2004), Archosauromorpha (Gao and

Fox 1998; Modesto and Sues 2004). Portions of the avian tree are still unresolved (Brown et al. 2007).

For the body size, ancestral state reconstruction, and proportional evolution analysis divergence times and topologies were derived from the literature for: Amphibia (Evans et al. 2004; Benton and Donoghue

2007), Mammalia (Springer et al. 2004), Reptilia (Rest et al. 2003), Squamata (Rest et al. 2003; Vidal and

Hedges 2005; Wiens et al. 2006; Kumazawa 2007), Serpentes (Lawson et al. 2005; Lee et al. 2007; Vidal

et al. 2007), Testudines (Fujita et al. 2004; Near et al. 2005; Fritz and Bininda-Emonds 2007) and Aves

(Ericson et al. 2006; Brown et al. 2007).

Uncertain divergence times were estimated as half the span from the last common ancestor to the first descendant node. A polytomy within Aves was resolved to zero-length branches. Due to the constrained values of genome size within Aves, this polytomy is unlikely to adversely affect our results or conclusions. Phylogenetic trees were created in Mesquite v2.01 (Maddison and Maddison 2007) using the StratAdd (Faure et al. 2006) package to date nodes according to the geologic timescale

(Gradstein et al. 2004).

Comparative Methods

Hypothesis Testing. Statistical hypotheses are tested using Bayes factors. For two nested models this is twice the difference between the harmonic means from the last iteration of the Markov chains (Raftery 1996). A Bayes Factor greater than 3 is taken as positive evidence, greater than 5 as strong evidence, and over 10 are taken as very strong evidence (Raftery 1996).

Some tests for correlation are reported as p-values, which are determined by calculating the fraction of the posterior distribution that crosses zero. For likelihood ratio tests, significance was calculated for 2 x the likelihood ratio assuming a chi squared distribution and degrees of freedom equal to the difference in parameters of the models.

Regression Model and Inference. Genome size and cell size measurements were logarithmically transformed to normalize for the wide range in data values. The 12 extant taxa discussed above were added to a previous dataset (Organ et al. 2007) and the program BayesTraits

( http://www.evolution.rdg.ac.uk/BayesTraits.html

) was used to explore correlations (Pagel 1997; Pagel

1999) among character states using a Bayesian framework and tree #1 (see below; extinct taxa pruned).

BayesTraits uses a phylogenetic generalized least squares approach that corrects for the nonindependence of the species caused by shared evolutionary history. The derivation of this procedure can be found in (Organ et al. 2007).

Branch length scaling parameters were estimated simultaneously during the regression of genome size on osteocyte size in living tetrapods to better fit the data to the model. The MCMC had

5010000 iterations with a burn-in of 1000 and a rate deviation of 2. Uninformative priors were used for the alpha and beta parameters. With a Bayes factor of 20.5, there is very strong evidence for the correlation between genome size on osteocyte size. The results were explored in JMP 6.03

(SAS_Institute 2006) and are summarized in Supplementary Table 2.

Table 2: Summary of Posterior Regression Models of Genome Size on Osteocyte Size.

Alpha Beta r 2 Kappa Delta Lambda Acceptance n mean stdev

95% CI

50091

-0.81

0.42

0.0036

50091

0.35

0.07

0.0007

50091

0.43

0.06

0.0005

50091

1.95

0.92

0.0081

50091

1.19

0.68

0.006

50091

0.62

0.19

0.0016

50091

0.21

0.04

0.0004

Organ and Shedlock, Page 4

We then used BayesTraits to generate phylogenetically informed posterior distributions of genome size inferences that take into account uncertainty in the regression model parameters and aspects of the phylogenetic tree. These estimations included cell size data (Supplementary Table 1) and phylogenetic information (from tree #1, see below). BayesTraits settings and scaling parameters were the same as the regression analysis discussed above. The results are listed in Supplementary Table 4 below.

Tree #3 below was used in these test with the following scaling parameters

= 0.00,

= 0.50, and

= 1.00 (Pagel 1999).

Table 3: Genome Size Inferences for Pterosaurs and Basal Archosauromorphs. Descriptive statistics from the posterior distributions of haploid genome size for seven extinct species of basal archosauromorphs and four pterosaurs.

Taxon

Champsosaurid indet.

C-Val mean

4.07

C-Val stdev

1.28

Rutiodon sp.

Desmatosuchus haploceros

Typothorax meadei

Postosuchus kirkpatricki

2.12

3.22

3.19

2

0.21

0.33

0.32

0.2

Leidyosuchus sp.

Dimorphodon macronyx

Rhamphorhynchus muensteri

Pterodactylus sp.

3.43

1.94

1.93

2.12

0.66

0.23

0.25

0.25

Pteranodon sp. 2.01 0.35

Phylogenetic t-Test using Multiple Regression: Dummy variables were used to divide species into groups. For example, we divided the taxa into groups A, B, and C, and it is A and B that we are interested in. Two dummy variables were then coded, the first assigns 1's to A's and 0's to B’s and C’s.

The second dummy variable assigns 1's to C’s and 0's to A’s and B’s. B's are assigned 0's for both dummy variables. A continuous multiple regression model was then generated using MCMC in

BayesTraits in which the two dummy variables (independent variables) predict a third dependent variable, say, genome size. Significance of

(the proportion of the posterior distribution that crosses

0) indicates that A and B differ when the data are normalized for phylogeny. Tree #3 below was used in these tests with the following scaling parameters

= 0.00,

= 0.50, and

= 1.00 (Pagel 1999).

Node Values: Ancestral genome size was estimated by inserting 0-branch length dummy nodes and using the random walk (Model A) analysis in BayesTraits. We used the MCMC mode to generate posterior distributions of the trait values (genome size). Node values are presented in Figure 2 of the main text.

Proportional Rates of Evolution. The PDAP package (Midford et al. 2005) for Mesquite was used to estimated node values and the amount of change in immediate descendants (standardized contrasts) in 130 tetrapods, including the inferred genome size for the basal archosaurs, pterosaurs, and non-avian dinosaurs. An ordinary least square model was then fit to the natural log transformed node values and standardized contrasts.

Organ and Shedlock, Page 5

Body Size Data

The following data were used to detect the influence of population dynamics and neutral evolutionary patterns were conducted by evaluating (as discussed above for differences in character states) the evidence for differences in body size as a proxy for population size (Lynch 2006; Lynch 2007b; Lynch

2007a) vs. genome size change as discussed in the primary text. Tree #2 below was used in analyzing body mass and genome size with the following scaling parameters

= 0.42,

= 0.28, and

= 1.00

(Pagel 1999).

Table 4: Body Size and Genome Size Data for Tetrapods. Body size data were obtained from the references listed in the table and references contained therein. Genome sizes were downloaded from www.genomesize.com

.

Taxa References Body

Size

(ln g)

Genome

Size

(ln pg)

Agama agama, Agama atra, Agama

impalearis (GS), Agama impalearis (BS)

Alligator mississippiensis

4

10.93

0.48 (Nagy et al. 1999)

0.91 (Lewis and Gatten 1985)

Ambystoma maculatum 1.45 3.5 (Vinogradov and Anatskaya 2006)

3.09

2.35

0.97 (Alonso et al. 2004)

0.74 (Alonso et al. 2004)

Anguis fragilis

Anolis aeneus, Anolis auratus, Anolis carolinensis, Anolis cf. nitens, Anolis

equestris, Anolis sagraei (GS), Anolis

auratus (BS)

Anoura caudifera, Anoura geoffroyi

Apalone spinifera (=Trionyx spiniferus; GS)

Trionyx ferox (BS)

Ardea herodias

Artibeus glaucus, Artibeus jamaicensis,

Artibeus lituratus (GS), Artibeus jamaicensis

(BS)

Bison bison

Boa constrictor

Bombina bombina

Bos taurus

Bradypus variegatus

Bufo bufo

Canis familiaris

Canis latrans

Canis lupus

Chalcides chalcides

Chamaeleo ceylanicus, Chamaeleo dilepis,

Chamaeleo hoehnelli, Chamaeleo jacksoni

(GS), Chamaeleo lateralis (BS)

Chelonia mydas

Chelydra serpentina

Coluber constrictor, Coluber najadum,

Coluber nummifer, Coluber ravergieri,

Coluber schmidti, Coluber viridiflavus (GS),

2.44

8.09

7.53

3.81

13.71

8.4

1.39

13.68

8.24

3.93

10.2

9.21

10.53

1.86

2.39

11.65

8.15

4.88

0.99 (Nagy et al. 1999)

0.99 (Vinogradov and Anatskaya 2006)

0.38 (Bennett and Harvey 1987)

0.97 (White and Seymour 2003)

1.59 (Garland 1983)

0.84 (Alonso et al. 2004)

2.44 (Vinogradov and Anatskaya 2006)

1.28 (Owen-Smith 1992)

1.44 (White and Seymour 2003)

1.9 (Vinogradov and Anatskaya 2006)

1.14 (Vinogradov 1995)

1.04 (White and Seymour 2003)

1.03 (Nagy et al. 1999)

0.46 (Alonso et al. 2004)

0.9 (Alonso et al. 2004)

0.97 (Alonso et al. 2004)

0.97 (Guppy and Withers 1999)

0.65 (Nagy et al. 1999)

Organ and Shedlock, Page 6

Taxa

Coluber constrictor (BS)

Corvus brachyrhynchos

Crocodylus niloticus, Crocodylus siamensis

(GS), Crocodylus acutus (BS)

Dasypus hybridus, Dasypus kappleri,

Dasypus novemcinctus, Dasypus pilosus,

Dasypus sabanicola, Dasypus

septemcinctus (BS), Dasypus novemcinctus

(BS)

Delphinapterus leucas

Dendroica dominica

Desmodus rotundus

Desmognathus fuscus

Didelphis virginiana

Dromaius novaehollandiae

Eptesicus furinalis

Equus caballus

Erinaceus europaeus

Eumops perotis

Falco peregrinus

Felis catus

Felis lynx

Gallus gallus

Gekko gecko

Gopherus agassizii

Gorilla gorilla

Hemidactylus leightoni (GS), Hemidactylus

mabouia (BS)

Homo sapiens

Hyla savignyi

Iguana iguana

Kinixys belliana

Kinosternon subrubrum (GS), Kinosternon

avescens (BS)

Lacerta viridis

Larus atricilla

Loxodonta africana

Macropus rufus

Myotis myotis (GS), Myotis lucifugus (BS)

Natrix natrix

Ornithorhynchus anatinus

Oryctolagus cuniculus

Panthera tigris

Body

Size

(ln g)

Genome

Size

(ln pg)

References

5.95

11.81

9.01

0.22 (Bennett and Harvey 1987)

1.17 (Alonso et al. 2004)

1.63 (White and Seymour 2003)

14.22

2.28

3.38

0.69

7.82

10.57

2.34

12.9

6.62

4.03

4.76

8.01

10.52

7.9

4

7.66

12.21

0.92

11.16

3.56

6.76

6.54

5.19

3.38

5.62

15.61

10.39

1.65

4.31

6.54

7.6

11.83

1.19 (O'Corry-Crowe 2002)

0.34 (Bennett and Harvey 1987)

0.98 (White and Seymour 2003)

2.79 (Vinogradov and Anatskaya 2006)

1.42 (White and Seymour 2003)

0.43 (Bennett and Harvey 1987)

0.85 (White and Seymour 2003)

1.17 (White and Seymour 2003)

1.3 (White and Seymour 2003)

0.94 (White and Seymour 2003)

0.36 (Bennett and Harvey 1987)

1.13 (Vinogradov 1995)

1.12 (White and Seymour 2003)

0.22 (Bennett and Harvey 1987)

0.94 (Alonso et al. 2004)

1.07 (Nagy et al. 1999)

1.35 (Vinogradov and Anatskaya 2006)

0.74 (Alonso et al. 2004)

1.25 (Vinogradov 1995)

1.28 (Vinogradov and Anatskaya 2006)

1.06 (Nagy et al. 1999)

1.09 (Guppy and Withers 1999)

1 (Guppy and Withers 1999)

0.68 (Bennett and Dawson 1976)

0.37 (Bennett and Harvey 1987)

1.45 (Garland 1983)

1.14 (White and Seymour 2003)

0.76 (Nagy et al. 1999)

1.06 (Alonso et al. 2004)

1.12 (White and Seymour 2003)

1.16 (White and Seymour 2003)

1 (White and Seymour 2003)

Organ and Shedlock, Page 7

Taxa

Pelobates fuscus

Phalacrocorax auritus

Plethodon cinereus

Podarcis sicula (GS), Podarcis lilfordi (BS)

Procavia capensis

Python reticulatus

Rana pipiens

Rattus norvegicus

Regulus calendula

Sauromalus obesus

Sceloporus magister, Sceloporus

occidentalis(GS), Sceloporus graciosus (BS)

Setifer setosus

Sorex araneus

Spheniscus demersus

Struthio camelus

Sus scrofa

Tachyglossus aculeatus

Tarsius syrichta

Tonatia bidens, Tonatia evotis (GS), Tonatia

bidens (BS)

Trachemys scripta

Triturus cristatus

Trogonophis wiegmanni

Tursiops truncatus

Tyto alba

Ursus arctos (GS), Ursus horribilis (BS)

Varanus komodoensis

Varanus salvator

Vipera aspis

Xenopus laevis

6.55

1.39

1.87

13.38

6.21

12.61

10.72

7.85

4.23

4.01

6.27

2.09

8.06

11.39

11.23

7.91

4.73

3.21

Body

Size

(ln g)

2.77

7.19

1.36

2

7.78

8.72

3.56

5.47

1.7

5.12

1.6

Genome

Size

(ln pg)

References

1.53 (Vinogradov and Anatskaya 2006)

0.36 (Bennett and Harvey 1987)

3.36 (Gatten et al. 1992)

0.7 (Nagy et al. 1999)

1.4 (White and Seymour 2003)

0.47 (Vinogradov and Anatskaya 2006)

1.91 (Gatten et al. 1992)

1.21 (Vinogradov 1995)

0.29 (Bennett and Harvey 1987)

0.98 (Nagy et al. 1999)

0.94 (Nagy et al. 1999)

1.62 (White and Seymour 2003)

1.07 (White and Seymour 2003)

0.49 (Nagy et al. 1999)

0.77 (Nagy et al. 1999)

1.15 (Vinogradov 1995)

1.06 (Nagy et al. 1999)

1.66 (White and Seymour 2003)

0.85 (White and Seymour 2003)

0.87 (Montes et al. 2007)

3.12 (Vinogradov and Anatskaya 2006)

0.5 (Alonso et al. 2004)

1.15 (Reidenberg and Laitman 2002)

0.49 (Vinogradov and Anatskaya 2006)

1.01 (Garland 1983)

0.66 (Nagy et al. 1999)

0.72 (Nagy et al. 1999)

1.07 (Alonso et al. 2004)

1.19 (Gatten et al. 1992)

Organ and Shedlock, Page 8

Phylogenetic Trees

Tree 1: Phylogenetic tree used to generate regression models of genome size and osteocyte lacunae size (extant taxa only) and make posterior predictions.

Organ and Shedlock, Page 9

Tree 2: Phylogenetic tree used to generate regression models of body mass and genome size.

Organ and Shedlock, Page 10

Tree 3: Phylogenetic tree used to estimate ancestral states and to test for proportional evolution.

Organ and Shedlock, Page 11

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