phyletic patterns of early development in gastropod molluscs

Phyletic patterns of early development in gastropod molluscs

David R. Lindberga,� and Robert P. Guralnickb

aDepartment of Integrative Biology and Museum of Paleontology, University of California at Berkeley, Berkeley, CA 94720,

USAbColorado University Museum and EPO Biology, University of Colorado at Boulder, Boulder, CO 80309, USA�Author for correspondence (e-mail: [email protected])

SUMMARY Cell lineage data for 30 exemplar gastropodtaxa representing all major subclades and the outgroupPolyplacophora were examined for phylogenetic signal usingcladistic analysis. Most cell lineages show phyletic trends ofacceleration or retardation relative to the outgroup and morebasal ingroup taxa, and when coded this variation is phylo-genetically informative. PAUP analyses of a cell lineage dataset under three sets of character ordering assumptionsproduced similar tree topologies. The topologies of the strictconsensus trees for both ordered and Dollo (near irreversibilityof character transformations) character assumptions weresimilar, whereas the unordered character assumption re-covers the least phyletic information. The cell lineage clado-grams are also in agreement with the fossil record of the timingand sequence of gastropod subclade origination. A long

branch lies between the Patellogastropoda1Vetigastropodagrade and the Neritopsina1Apogastropoda clade. Thegeological timing of this long branch is correlated with thefirst large-scale terrestrially derived eutrophication of thenear-shore marine habitat, and one possible explanationfor this branch may be a developmental shift associated withthe evolution of feeding larvae in response to the moreproductive conditions in the near-shore water column.Although character transformations are highly ordered inthis data set, developmental rate characters (like all othermorphological and molecular characters) are also subjectto homoplasy. Finally, this study further supports thehypothesis that early development of gastropod molluscshas conserved a strong phyletic signal for about half a billionyears.

INTRODUCTION

‘‘Among these groups the cleavage pattern and the fate of the various

blastomeres are so nearly identical that a common ancestry is

scarcely to be doubted.’’

Hyman (1951:10)

Hyman’s (1951) use of ontogenetic criteria to suggest

phylogenetic relationships among spiralian taxa occurred

toward the end of a 70-year hiatus that resulted, in part, from

a backlash to Haeckel’s (1866) overly optimistic statement

that ontogeny recapitulated phylogeny. It was another 25

years until Gould’s (1977) influential review of the history and

potential evolutionary and ecological relationships between

ontogeny and phylogeny helped to jump start the modern

research enterprise in evolutionary development. Gould’s

timing could not have been better, because molecular

biologists were also beginning to examine and understand

gene activity during development across broad expanses of

the tree of life (e.g., Davidson 1976). Because of these and

other events, the words ‘‘development’’ and ‘‘evolution’’ were

once again spoken in juxtaposition.

Molluscs have long provided data regarding the conserved

nature of developmental pathways both within and between

spiralian taxa. Using cell lineage data from gastropod

exemplars, Verdonk and van den Biggelaar (1983), Freeman

and Lundelius (1992), Haszprunar (1993), van den Biggelaar

(1993), van den Biggelaar (1996a), van den Biggelaar and

Haszprunar (1996), Lindberg and Ponder (1996), and

Guralnick and Lindberg (2001) all contended that cleavage

patterns in early gastropod development show a strong

phyletic signal.

The overall trend that has been noted is one of increasing

acceleration of 4d cell lineage formation accompanied by

retardation of trochoblast formation in the ‘‘higher’’ taxa. For

example, in the outgroup Polyplacophora (chitons) 4d

mesentoblast formation occurs when the embryo is composed

of about 73 cells (Heath 1899), whereas in stem gastropod

taxa (e.g., Patellogastropoda and Vetigastropoda) mesento-

blast formation is slightly sooner, occurring at about the 63

cell stage (van den Biggelaar 1996a), and in the ‘‘higher’’

crown group taxa (Caenogastropoda and Heterobranchia),

mesentoblast formation now occurs at the 24 cell stage

(Verdonk and van den Biggelaar 1983; van den Biggelaar

1996a). This acceleration relative to cell number is due to an

EVOLUTION & DEVELOPMENT 5:5, 494–507 (2003)

& BLACKWELL PUBLISHING, INC.494

earlier onset of 3D macromere division relative to the

divisions of the first, second, and third quartet of (Verdonk

and van den Biggelaar 1983).

Most of these previous studies only focused on two cell

characters: the formation of the 3D macromere and the 4d

mesentoblast. This limited character set likely results from the

heavy weighting of these charactersFboth play a critical role

in the determination of the developmental fates of a large

number of blastomeres (Damen and Dictus 1994a, 1994b;

Collier 1997). In addition to a limited character set, the

placement of these characters in a phylogenetic framework

has often been ambiguous with the characters mapped onto

paraphyletic taxa such as Archaeogastropoda and Mesogas-

tropoda (e.g., Freeman and Lundelius 1992; Haszprunar

1993) or used to construct what often amounts to a single

character phylogenies (e.g., van den Biggelaar and Haszpru-

nar 1996; Lindberg and Ponder 1996).

Here we again focus on the Gastropoda, but compared

with the studies above our data set (a) represents a substantial

increase in taxon sampling, (b) uses characters from all

available cell lineages, and (c) uses an explicit methodology

(maximum parsimony) to estimate relationships. The trees

provided by this initial analyses are evaluated and then used

to (a) estimate the extent of phyletic information present in

early gastropod development relative to morphological data

sets, (b) examine evolutionary patterns in the early develop-

ment of gastropod molluscs, (c) examine their correspondence

with trees based on mesentoblast formation, and (d) examine

scenarios for the timing and evolution of gastropod life

history characters.

MATERIALS AND METHODS

Character analysisCell lineage characters were identified from the sequence of

formation of molluscan cell lineages as shown in Fig. 1. As

documented above, molluscan (and especially gastropod) cell

lineages have been extensively studied and provide a broad set of

remarkable morphological markers across the taxon (Appendix).

These markers are defined by cell cleavage number and can be

visualized on a cell lineage tree (Fig. 1a). Although specification of

cell lineages can be either invariant or variable (Davidson 1990),

invariant cell lineage specification is more common in spiralian taxa

such as the Mollusca and Annelida, whereas variable cell lineage

specification is more often found in taxa with radial cleavage

(Valentine 1997). Wray (1994) used this variability in cell lineage

Fig. 1. Cell lineage trees. (a) Conklin’s (1897) notation for the designation of cell lineages. For brevity only six cell division cycles are shownhere and for only the A macromere. Identical representations exist for the B, C, and D macromeres as well. Although this node-based viewof a strictly bifurcating tree accurately reflects the number of cell divisions at which a given lineage is formed, cell lineage data in this formatare not useful for comparative studies between taxa because of its invariance. (b) Cell lineage trees can be scaled by the number of cellspresent in the embryo at the time of appearance of a given cell lineage, and the relative timing of the appearance of each lineage definedrelative to cell number. For example, although both the 2A and 1a1 cell lineages (represented by 2Q and 1q1 in b) arise at their respectivefourth cell divisions (a), 2A forms when eight cells are present, whereas the 1a1 cell lineage does not appear until the 24 cell stage.

Ontogeny and phylogeny of gastropodmolluscs 495Lindberg and Guralnick

specification to document cell lineage evolution in the radially

cleaving Echinodermata. However, for more invariant taxa such as

molluscs, early cleavage division typically equals specification

(Collier 1997; Dictus and Damen 1997) and some other parameter

must be used to calibrate cell lineage formation between taxa.

Although lacking variation in specification, the relative timing

of cell lineage originations does vary (Fig. 1b), and variation in

number of cells present in the embryo relative to the sequence of

cell linage formation has been used to compare patterns of

development in several spiralian taxa. For example, van den

Biggelaar (1963) documented heterochronic changes in the

retardation of the formation of the larval trochoblasts and the

acceleration of formation of the 4d mesentoblast and mapped these

trends on a gastropod phylogeny. Freeman and Lundelius (1992)

examined the evolution of the ‘‘small d’’ cell lineage in several

spiralian clades and also demonstrated acceleration in d quadrant

formation in the Gastropoda by mapping cell lineage formation on

an evolutionary tree. van den Biggelaar and Haszprunar (1996)

tested the hypothesis that cleavage patterns in the Gastropoda were

informative as to ‘‘taxonomic and evolutionary ranking’’ and

focused on the relative timing of the formation of the 3D

macromere and the 4d mesentoblast. Haszprunar (1993), Lindberg

and Ponder (1996), and Ponder and Lindberg (1997) also mapped

or coded embryo cell number at mesentoblast formation into

gastropod phylogenetic analyses and scenarios.

Outside of the Mollusca, van den Biggelaar et al. (1997) used

cleavage patterns, cell lineages, and cell specification patterns to

suggest relationships within the Spiralia, and Boyer and Henry

(1998) discussed evolutionary modifications of the spiralian

developmental program. More recently, Guralnick and Lindberg

(2001) substantially increased taxon and character sampling as

compared with earlier studies and used maximum parsimony and

neighbor joining to examine the extent of phyletic information

present in the early development of the Spiralia.

Cell lineage data used here are modified from Guralnick and

Lindberg (2001) (Appendix). The Guralnick and Lindberg (2001)

data set consists of cell numbers for the time of formation of 54

individual cells for 67 spiralian taxa, including 35 molluscs (5

Bivalvia, 27 Gastropoda, 2 Polyplacophora, and 1 Scaphopoda). In

Guralnick and Lindberg (2001) the 67 exemplars were used as

operational taxonomic units (OTUs); in this study the data set has

been restricted to gastropod taxa and molluscan outgroup

exemplars. These data were augmented by unpublished cell lineage

data provided by van den Biggelaar (personal communication,

2002) and then compartmentalized into composite OTUs that

represented the major gastropod subclades (see below).

Generally, analogous cells in different ‘‘quartets’’ form at

approximately the same time, and treating each cell from a

particular quartet as a single character would provide misleading

measures of support. Thus, when the variation in the relative

timing of cell divisions within quartets was minimal (about two to

four cells) and likely to lead to redundant characters, a median

value for the entire quartet was calculated. For example, the value

of 1q1 would equal the median of 1a111b111c111d1 (Fig. 1a) with

‘‘q’’ designating micromere quartets and ‘‘Q’’ designating macro-

mere quartets (Fig. 1b). This was done for 52 of the lineages

producing 13 characters. For cell lineages 4d and 4d1 individual

lineage values were used (Fig. 1b). The 1q cell lineage was found to

be invariant across taxa and was excluded, leaving 14 characters in

our analysis (Fig. 1b, Appendix).

Data for 14 cell lineages were available for most of the 32

molluscan OTUs (2 outgroup and 30 ingroup examplars). These

OTUs were grouped into nine major molluscan subclades (one

outgroup and eight ingroups) to allow clade level comparisons with

current hypotheses of gastropod relationships and previously

published analyses of gastropod cell lineage evolution. These

subclades have consistently been found to be monophyletic in most

morphological (Haszprunar 1988; Ponder and Lindberg 1997;

Sasaki 1998) and molecular studies (Tillier et al. 1992; Rosenberg et

al. 1997; Winnepenninckx et al. 1998) over the last 15 years. Cell

numbers for the OTUs were calculated as median values for all

quartets or individual lineages within each subclade. In three cases

only single exemplars exist for a subcladeFPatellogastropoda,

Neritopsina, and Valvatoidea. All data were log transformed to

reduce variance before gap coding. Character states were gap

coded by graphing the distribution of values within each character

and examining for gaps and trend changes by eye. Obvious isolated

groupings and breaks in trends were recognized and assigned

discrete character states as follows:

� Characters 1–6: The ‘‘trochoblasts’’ contribute to the formation

of the prototroch and its supporting cells (Dictus and Damen

1997). van den Biggelaar (1993) showed retardation in this

lineage in gastropods. However, the Patellogastropoda appear to

be an exception and show acceleration of this cell lineage

compared with the outgroup Polyplacophora and the Vetigas-

tropoda.

1Fmedian number of cells present at formation of 1q1 cell

lineage (4th division): 1650, 2151.


lineage (5th division): 2450, 2851, 3252, and 38–4053.


lineage (6th division): 44–5450 and 68–9951.


lineage (6th division): 36–4950, 55–7251.


lineage (5th division): 3250, 44–4951, and 6052.


lineage (6th division): 6050, 8051, and 123–13252.

� Characters 7–9: This cell lineage produces prototroch and

posttrochal ectoderm; the first stomatoblast contributes to the

formation of the foot and shell gland (Dictus and Damen 1997).

7Fmedian number of cells present at formation of 2q cell

lineage (4th division): 1650 and 1251.


lineage (5th division): 3250, 2451.


lineage (6th division): 6050, 5251, 4452, 4153, 37–

3854, and 3255.

� Characters 10–11: This cell lineage produces ectomesoderm and

posttrochal ectoderm (Dictus and Damen 1997).

496 EVOLUTION & DEVELOPMENT Vol. 5, No. 5, September^October 2003

10Fmedian number of cells present at formation of 3q cell

lineage (5th division): 2050, 23–2451, and 3252.


lineage (6th division): 5450, 6051, 4852, 40–4153, and

3654.

� Characters 12–14: The 4Q cell lineage produces endoderm and

the 4d lineage (the mesentoblast) endoderm and endomeosderm

(Dictus and Damen 1997). These characters have often been

treated as heterochronies associated with the acceleration of

development in more ‘‘derived’’ taxa (van den Biggelaar 1993;

van den Biggelaar and Haszprunar 1996).

12Fmedian number of cells present at formation of 4Q cell

lineage (6th division): 8550, 63–6451, 48–4952, and 42–

4453.

13Fmedian number of cells present at formation of 4d cell

lineage (6th division): 64–7350, 41–4851, and 25–3252.

14Fmedian number of cells present at formation of 4d1 cell

lineage (7th division): 90–13050 and 39–4951.

AnalysesThe data matrix was subjected to exhaustive searches using PAUP�

version 4.0b10 (Swofford 1998) under maximum parsimony with

the Polyplacophora serving as the outgroup (Wingstrand 1985). All

characters were equally weighted, were assumed to show acceler-

ated character transformation (there were no changes in character

transformations with either accelerated or delayed character

transformation assumptions), and character state ordering was

varied in different maximum parsimony analyses between un-

ordered, ordered, and Dollo criteria. Strict consensus trees were

calculated for the trees produced under each of these three criteria.

Bremer support values for each tree were calculated using the clade

decay option in MacClade 4.0 (Maddison and Maddison 1992).

Tree statistics for these analyses are presented in Table 1.

The data matrix was also used to evaluate five previously

reported trees (Fig. 2). The Ponder and Lindberg (1997) (P&L)

treeFbased on an analysis of 40 taxa and 117 morphological

charactersFand five phylogenetic trees constructed by van den

Biggelaar and Haszprunar (1996) (vdB&H 18–21) using cell

number at the time of formation of the mesentoblast and the

presence/absence of the polar lobe as characters. We entered the

P&L and vdB&H trees as topological constraints and the analyses

rerun as described above, including varying the assumption sets for

character state transformations. Comparisons among constraint

and maximum parsimony trees were made using overall branch

lengths and quartet dissimilarity measures (Day 1986; Component,

version 2.0, Page 1993) (Tables 1 and 2).

Table 1. Tree statistics

Character Type and MP and Constraint Trees Steps No. of Trees CI1 RI RCI

Gastropod subclades

MP unordered 32 11 0.524 N/A N/A

MP ordered 34 7 0.714 N/A N/A

MP Dollo 34 3 0.714 N/A N/A

Tree comparisons

Ponder and Lindberg (1997)

MP unordered 33 1 0.879 0.809 0.711

MP ordered 35 1 0.824 0.833 0.691

MP Dollo 36 1 0.806 0.863 0.695

van den Biggelaar and Haszprunar (1996, Fig. 18)

MP unordered 35 1 0.829 0.714 0.592

MP ordered 39 1 0.737 0.722 0.530

MP Dollo 41 1 0.707 0.765 0.541


MP unordered 35 1 0.800 0.714 0.592

MP ordered 39 1 0.744 0.722 0.537

MP Dollo 42 1 0.691 0.745 0.515


MP unordered 34 1 0.828 0.762 0.650

MP ordered 37 1 0.784 0.778 0.610

MP Dollo 40 1 0.725 0.784 0.569


MP unordered 33 1 0.879 0.809 0.711

MP ordered 36 1 0.806 0.806 0.649

MP Dollo 37 1 0.784 0.843 0.661

Shaded rows indicate most parsimonious (MP) constraint trees; note ties for MP ordered and Dollo assumption sets. CI, ; RCI, ; RI.1CI for strict consensus trees5Rohlf’s CI(1).


RESULTS

Results of the PAUP� analyses under three sets of character

type assumptions are presented in Fig. 3 and Table 1. Trees

were between 32 and 34 steps in length, and the number of

most parsimonious trees ranged from 11 trees under

unordered criteria to 7 trees under ordered and 3 trees under

the Dollo assumption. Zero length branches were present for

four OTUsFVetigastropoda, Neritopsina, Sorbeoconcha,

and Pulmonata (Fig. 3). In all strict consensus trees

(unordered, ordered, and Dollo), the stem taxa Patellogas-

tropoda and Vetigastropoda followed the outgroup Poly-

placophora. In the ordered and Dollo trees the Neritopsina

followed these stem groups and preceded the crown group

Apogastropoda; the strongest Bremer support marked the

stem between the vetigastropods and the Neritopsina (Fig. 3).

Fig. 2. Published trees compared with the cell lineage developmental data set by maximum parsimony criteria. P&L cladogram andphylogram from Ponder and Lindberg (1997). vdB&H cladograms from van den Biggelaar and Haszprunar (1996); number refers to theirfigure number. Branch lengths for cell lineage developmental data analysis shown for P&L tree are similar to branch lengths in vdB&H treesas well.


Polytomies were present in the apogastropods under all three

criteria. Longer branches and weaker Bremer support

separated the vetigastropods from the polyplacophorans

and Patellogastropoda in all three trees (Fig. 3).

The number of characters used in this analysis depended

on taxon sampling, and our sampling is based on published

studies of early cell division patterns. After character analysis

the number of characters in different cell lineages and cell

division groups varied between one and six and one and

seven, respectively (Table 3). However, different cell lineages

and cell division groups were broadly distributed over the

trees as informative characters (Fig. 4), and there was no

significant difference between the characters expected and

observed frequencies on the trees grouped by either cell

lineage or cell division criteria (Table 3).

Our next analysis focused on comparing the most

parsimonious trees from our analysis with the previously

published gastropod trees. The P&L tree and four vdB&H

trees (Fig. 2) were entered as constraint trees and evaluated

relative to the cell lineage data set under the same three

character assumption sets. The P&L tree was found to be one

to two steps longer than the most parsimonious trees, whereas

the vdB&H trees were one to eight steps longer (Table 1). The

P&L tree was most parsimonious with the cell lineage tree run

with Dollo and unordered characters and tied with the

vdB&H21 tree when compared with cell lineage trees under

the unordered assumption. Substantially longer branches also

marked the stem between the vetigastropods and the

Neritopsina in all the constraint trees as well (e.g., P&L

phylogram in Fig. 2).

Quartet measures for comparisons among all trees (P&L,

vdB&H, most parsimonious trees) show the vdB&H figure 20

tree most similar to the P&L tree (symmetric differ-

ence50.143) (Table 2). The unordered most parsimonious

tree based on cell lineage data is equivalent to all five

constraint trees (symmetric difference50.424), whereas the

ordered and Dollo trees are most similar to the P&L tree

(symmetric difference50.217).

Table 2. Componentr quartet measures analysis of maximum parsimony and constraint trees from Table 1

Tree 1 Tree 2 SD EA DC SJA Q s d

P&L UnOrd 0.424 0.595 0 0 126 51 0

Ord 0.217 0.357 0 0 126 81 0

Dollo 0.217 0.357 0 0 126 81 0

vdB&H UnOrd

18 0.424 0.595 0 0 126 51 0

Ord 0.478 0.571 0.214 0.333 126 54 27

Dollo 0.478 0.571 0.214 0.333 126 54 27

P&L 0.317 0.317 0.317 0.317 126 86 40

vdB&H UnOrd

19 0.424 0.595 0 0 126 51 0

Ord 0.449 0.548 0.190 0.296 126 57 24

Dollo 0.449 0.548 0.190 0.296 126 57 24

P&L 0.222 0.222 0.222 0.222 126 98 28

vdB&H UnOrd

20 0.424 0.595 0 0 126 51 0

Ord 0.391 0.500 0.143 0.222 126 63 18

Dollo 0.391 0.500 0.143 0.222 126 63 18

P&L 0.143 0.143 0.143 0.143 126 108 18

vdB&H UnOrd

21 0.424 0.595 0 0 126 51 0

Ord 0.420 0.524 0.167 0.259 126 60 21

Dollo 0.420 0.524 0.167 0.259 126 60 21

P&L 0.262 0.262 0.262 0.262 126 93 33

Shaded rows indicate most similar trees; all unordered trees are equally similar. VdB&Hnn, van den Biggelaar and Haszprunar (1996), where nnrepresents the figure number; P&L, Ponder and Lindberg (1997); UnOrd, unordered; Ord, ordered; SD, symmetric difference; EA, explicitly agree; DC,do not conflict; SJA, strict joint assertions, Q, maximum possible resolved; s, resolved and same; d, resolved and different (Day, 1986).


DISCUSSION

The cell lineage data set shows congruence with current

hypotheses of higher gastropod relationships. A gastropod

clade was also present in the Guralnick and Lindberg (2001)

spiralian analysis. In their strict consensus tree of spiralian

taxa, a pair of polyplacophoran taxa were sister to all

gastropod taxa in the analysis. Within the gastropod ingroup

there were some similarities to phylogenies constructed from

morphological analyses (Haszprunar 1988; Ponder and

Lindberg 1997). The two vetigastropods were basal in their

position relative to the neritopsine taxa, but groupings within

the apogastropods were comprised of an unexpected mix of

pulmonates, caneogastropods, and opisthobranchs. Pogono-

Fig. 3. Strict consensus trees (left, cladograms; right, phylograms) for the three character assumption sets. Bremer support (clade decay)values are shown on the cladograms, and tree number randomly chosen for the phylograms is given under each tree.


phoran, polychaeate, and bivalve exemplars were also nested

within the Gastropoda. Many aspects of the topology of the

Dollo strict consensus tree in this analysis are congruent with

trees produced from both morphological (Haszprunar 1988;

Ponder and Lindberg 1997; Wagner 2001) and molecular

analyses (Tillier et al. 1992; Harasewych et al. 1997a,b;

Rosenberg et al. 1997; Winnepenninckx et al. 1998; Colgan et

al. 2000; Harasewych and McArthur 2000; Yoon and Kim

2000). The fossil record also corroborates many aspects of the

cell lineage trees, including the early divergence of the

Patellogastropoda and Vetigastropoda (Late Cambrian to

Early Ordovician, 523–488 million years ago) (Hedegaard et

al. 1997; Bandel 2000; Fryda 2001) and the subsequent

origination of the Neritopsina and Apogastropoda (Late

Sularian to Devonian, 428–374 million years ago) (Yoo 1994;

Fryda 2001; Fryda and Blodgett 2001; Wagner 2001).

It is uncommon in molluscan phylogenetics for a single

character base (the sequence of cell lineage originations) to

produce trees congruent with analyses based on multiple

character sources (Lindberg and Ponder 2001). In Ponder and

Lindberg’s (1997) morphological analysis there is not a single

character base (e.g., radulae, shell microstructure, digestive

system, sperm morphology, etc.) that will produce a tree

closely congruent with the tree based on total evidence.

Although Ponder and Lindberg discussed the acceleration of

mesentoblast formation in ‘‘higher’’ gastropod taxaFtheir

character 117 (developmental rates)Fthe character was

scored only as the absence or presence and size of the polar

lobes, a character that would be apomorphic for the

Sorbeoconcha in the current study. And although some data

at that time suggested that differential acceleration might be

occurring in different subclades (van den Biggelaar 1993), it

was insufficient to determine whether informative patterns

were present.

van den Biggelaar and Haszprunar (1996) completed

sampling within the major gastropod subclades and found

patterns in cell number at the time of formation of the 4d

mesentoblast and the presence of the polar lobe that they used

to construct possible trees. The van den Biggelaar and

Haszprunar trees have slightly poorer resolution compared

with the trees calculated here, and this undoubtedly reflects

their limited character set, which also produced some

unfamiliar groupings. For example, because the Neritopsina

lack a polar lobe but show an accelerated mesentoblast, the

van den Biggelaar and Haszprunar character set required this

taxon to (a) nest in the heterobranch lineage (vdB&H19) or

(b) originate after acceleration, but before formation of the

polar lobe in the caenogastropods as in vdB&H20. With

additional characters and the Dollo assumption, the Ner-

itopsina are resolved as the sister taxon of the Apogastropo-

da, as in some morphological analyses and molecular

analyses. However, the overall congruence between the van

den Biggelaar and Haszprunar trees is noteworthy and argues

that specification of the stem cell of the mesentoblast (3D) is

one of the most critical and conserved aspects of early

gastropod development (Freeman and Lundelius 1992; van

den Biggelaar 1993; Guralnick and Lindberg 2001).

It is clear that early development of gastropod molluscs

has conserved a strong phyletic signal for about half a billion

years. Moreover, this signal is further sharpened under

Table 3. Number and frequency of developmental characters by cell lineage and cell division

Expected Observed

Cell Line Chars Freq Chgs Freq

1q 6 0.43 11 0.33

2q 3 0.21 7 0.21

3q 2 0.14 7 0.21

4Q 1 0.07 3 0.09

4d 2 0.14 5 0.15

R5 14 1 33 1

w25 0.9996

Cell Div Chars Freq Chgs Freq

4 2 0.14 3 0.06

5 4 0.29 7 0.33

6 7 0.50 15 0.58

7 1 0.07 2 0.03

R5 14 1 33 1

w25 0.9930

Expected, number of possible characters in Fig. 1, a and b; Observed, number of character occurrences on trees (e.g., Fig. 4). Chi-square values are notsignificant.


stringent ordered and Dollo character transformation models.

Both assumptions are directional filters for character

transformation and may serve as good models for many of

the ordered characteristics of invariant development (David-

son 1990). This can be clearly seen in the Dollo-like behavior

of the phyletic trends present in the retardation and

acceleration of the descendant cell lineages of the 1q, 2q,

and 3q quartets (Fig. 5).

The role of development in phylogenetic reconstruction

was formalized by Hennig (1966). His concept of the

semaphoront recognized the potential presence and usefulness

of characters derived from different ontogenic stages, and his

ontogenic criterion was the third augmentation for determin-

ing character polarity (Hennig 1966). However, the applica-

tion of ontogenetic polarity determination has been

controversial. Although Nelson (1978) and others argued in

support of ontogenetic criteria, other workers, including Fink

(1982) and Albrecht (1985), cautioned against the use of

development in polarity determinations. However, Fink and

Albrech’s concerns were likely based on their experience with

non-spiralian taxa where specification is more variable and

are in marked contrast to the gastropods where early

development is virtually invariant and a strong phyletic signal

remains. This suggests that the applicability of the ontogenetic

criterion in polarity determinations will follow the degree of

variation seen in cell lineage specification and may be most

useful for spiralian taxa.

One of the most consistent features of the character matrix

is the presence of a long branch between the Patellogastro-

poda1Vetigastropoda grade and the Neritopsina1Apogas-

tropoda clade. There are twice the number of character

changes along this long branch as there are among the

outgroup and first two stem taxa, and the changes on this

long branch represent over 24% of the total tree length. The

changes along this branch occur in every cell lineage and three

of the four cell division groups in the data matrix. Character

transformations include retardation of the fifth and sixth

cleavages of the descendants of the 1q cell linage and

acceleration of the 2q, 3q, 4A–C, and 4d cell lineages. The

largest changes in cell number are associated with the

retardation of the 1q cell lineage that produces the head

region, prototroch, and apical tuft (Raven 1966; Render 1991;

Collier 1997; Dictus and Damen 1997), followed by the

acceleration of the 4d cell lineage that forms the endoder-

m1endomesoderm and ultimately the adult mesodermal

structures (muscles, heart, kidneys, digestive system, etc.)

(Raven 1966; Collier 1997; Render 1997; Dictus and Damen

1997).

This long branch may result from several possible factors,

including insufficient taxon sampling, extinction, or possibly a

macroevolutionary event. No early cleavage data exist for

several major deep sea and vent taxa such as the Neompha-

lidae as well as the Sequenziina and Cocculinidae, all of which

may be nested in this region of the tree (Ponder and Lindberg

1997). Extinction of large diverse gastropod clades such as the

Bellerophonta and Euomphalina (Fryda 2001; Wagner 2002)

may also have contributed.

This long branch might also represent a developmental

shift associated with life history evolution, including the

evolution of direct development, increasing complexity of

reproductive systems, and larval feeding (Wray and Raff

1989; Wray 1994). Freeman and Lundelius (1992) postulated

that acceleration of the D quadrant specification was

correlated with the evolution of direct development; Ponder

and Lindberg (1997) suggested it was not correlated with the

evolution of direct development per se but rather with

modifications originally lengthening the veliger phase.

Fig. 4. Character mapping on tree 2 of three trees from the mostparsimonious Dollo analysis, including distribution of associatedcell lineage and cell division data. See Table 1 for tree statistics.


Accelerating development to lengthen a developmental

phase seems counterintuitive in the classic context of

acceleration of development (Gould 1977). However, Ponder

and Lindberg (1997) argued that if acceleration was involved

in shortening the trochophore stage, an earlier appearance of

the gastropod veliger larva could provide a potentially longer

feeding phase in which growth and development can take

place. Substantial delays in metamorphosis were then possible

because developmental and other energetic requirements were

met by the larvae. van den Biggelaar (1993, 1996) and van den

Biggelaar and Haszprunar (1996) suggested that the retarda-

tion of the 1q cell lineage (trochoblasts) might also be

correlated with the reduction of the prototroch of the

trochophore and changing life history strategies. Thus,

observation of both acceleration (4d) and retardation (1q)

in the evolution of early gastropod development is consistent

with Ponder and Lindberg’s scenario. Moreover, it further

demonstrates that both peramorphosis and padeomorphosis

can operate simultaneously in the embryo.

The geological timing of this developmental long branch

correlates with several major changes in earth history. During

the Silurian the climate stabilized, marking an end to the

erratic fluctuations of the Ordovician. One result of these

changes was the melting of large glaciers and a substantial rise

in sea level. Coral reefs appeared, as well as several major

evolutionary events in the history of ‘‘fishes,’’ including the

radiation of jawless fish and the diversification of freshwater

and jawed fish. It is also during the Silurian that the first

evidence of a major diversification of terrestrial life is

preserved, including vascular plants and arthropods. These

features suggest increased productivity associated with the

invasion of terrestrial habitats by plants, thereby making

possible the first terrestrially derived eutrophication of the

near-shore marine realm. The evolution of armored fish and

diversification of large arthropod predators such as the

eurypterids during this period also suggest increased preda-

tion pressure (Signor and Brett 1984; Vermeij 1987). Many of

these same factors have been argued by Vermeij (1995) to be

drivers in other Phanerozoic revolutions, and the possible

correlation of the reorganization of the gastropod develop-

mental pathway with the evolution of feeding larvae may

represent another realized opportunity for innovation and

diversification under Vermeij’s model.

Both the Neritopsina and Apogastropoda clades are

plesimorpohic for feeding larvae, complex egg capsules, mixed

developmental modes, and internal fertilization, whereas

feeding larvae and most of these other associated features

are absent in the Polyplacophora, Patellogastropoda, and

Fig. 5. Patterns of retardation and acceleration in the relative timing of formation in three gastropod cell lineages. For example,polyplacophoran embryos increase by 20 cells from the time of formation of the 1q1 to the 1q112 cell lineages, whereas pulmonate embryosincrease by 56 cells between the same two events. Note homoplastic features of retardation and acceleration in the 2q to 2q11 and 3q to 3q1

categories in the Apogastropoda (arrows). In each cell lineage category the outgroup is to the left and the crown taxa to the right.


Vetigastropoda clades (Haszprunar et al. 1995; Hadfield et al.

1997; Ponder and Lindberg 1997). Although direct develop-

ment, internal fertilization, and mixed developmental modes

have been independently derived in a few taxa in each of these

stem groups, the condition is always demonstrably homo-

plastic (Ponder and Lindberg 1997).

If the long branch marks a developmental response to

selection for feeding larvae, it does not appear to have

required a Goldschmidian hopeful monster but rather a rate

change or rachet in the relative timing of the formation of

different cell lineages (a rachet-like model is supported by the

results of the Dollo character assumption set; see below). This

is because the initial trends in cell lineage formation were

already present in the nonfeeding stem taxa (Fig. 5,

Appendix). In addition, a second nonfeeding outgroupFthe

ScaphopodaFalso shows acceleration of the 4d cell lineage

and retardation of the 1q lineages (van Dongen and

Geilenkkirchen 1974). So, unless scaphopod and stem

gastropod taxa ‘‘knew’’ a feeding larvae lay approximately

80 million years in their descendants’ future, the changes in

cell lineage origination that are thought to be associated with

the origin of feeding larvae would have to be exaptations

(sensu Gould and Vrba, 1982), the coopting of a trend that

was under selection for some other reason but more recently

has been reorganized for the evolution of feeding larvae. In

addition, these changes in cell lineage origination appear to be

constrained in specific directions in different cell lineages as

demonstrated by the applicability of the Dollo criterion to

these character patterns (Fig. 5).

The number of times feeding larvae have evolved in the

Gastropoda has been ardently debated (Haszprunar et al.

1995; Ponder and Lindberg 1997; Hickman 1999). Proponents

of multiple origins consistently list ‘‘differences’’ between

feeding modes as evidence of separate derivations in three

major cladesFNeritospina, Caenogastropoda, and Hetero-

branchia. However, numerous autapomorphies can provide

no support for evolutionary interpretations, and the most

parsimonious scenario remains a single origin on the long

branch between the Patellogastropoda1Vetigastropoda grade

and the Neritopsina1Apogastropoda clade.

However, there is other evidence of parallel evolution in

the developmental data. In many of the apogastropods some

of the later developmental character states (number of cells at

the time of formation of a particular cell lineage) are similar,

although they are obtained through convergent patterns of

retardation and acceleration in their respective cell lineages.

The creation of these homoplastic characters results from

scoring cell lineage formation relative to cell number, but they

can be readily recognized by examining character distribu-

tions on the tree and by graphically inspecting the relative

contribution of different rates of cell division across cell

lineages. In our analyses the nonresolution in the Apogas-

tropoda appears to result from this form of homoplasy.

AcknowledgmentsWe acknowledge the immense contributions of Professor Jo A. M.van den Biggelaar of the University of Utrecht, whose work onmolluscan development provides the framework on which futurestudies of the evolutionary history and diversification of the Molluscawill ultimately be parsed. We thank B. K. Hall, J. A. M. van denBiggelaar, D. B. Wake, G. Wray, and an anonymous reviewer forcriticism of the manuscript; J. A. M. van den Biggelaar for providingseveral unpublished cell lineage data (see Appendix); and M. G.Kellogg, B. Mishler, R. Meier, C. Nielsen, and G. Vermeij for helpfuldiscussions. This work was supported, in part, by NSF DEB-9700728. This is contribution number 1778 from the University ofCalifornia Museum of Paleontology.

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APPENDIX

Gastropoda taxon data set collated from Guralnick and Lindberg (2001)

TaxonCell Lineage

Source

1q1

1q11

1q112

1q121

1q22

1q222

2q 2q1

2q11

3q 3q1

4Q 4d 4d1

Outgroup

Polyplacophora 16 24 54 36 32 60 16 32 60 24 54 85 73 113

Acanthochitona 16 24 44 36 32 56 16 32 56 24 44 84 73 ? van den Biggelaar, 1996b

Ischnochiton 16 24 63 36 32 63 16 32 63 24 63 85 73 113 Heath, 1899

Ingroup

Patella 16 32 44 41 32 60 16 32 52 32 60 63 64 ? van den Biggelaar, 1977

Vetigastropoda 16 32 53 44 32 61 13 24 45 23 48 62 64 90

Gibbula 16 32 55 43 32 63 12 24 44 20 48 55 64 89 Robert, 1902

Haliotis 16 32 52 48 32 60 16 24 48 24 48 63 64 91 van den Biggelaar, 1993 &

personal communication

Tricolia 16 32 52 40 32 60 12 24 44 24 48 64 64 ? van den Biggelaar, personal

communication

Calliostoma 16 32 52 44 32 60 12 24 44 24 48 64 64 ? van den Biggelaar, personal

communication

Theodoxus 16 28 ? 49 ? ? 12 24 41 24 41 49 41 49 Blochmann, 1881

Architaenoglossa 16 40 ? ? 44 ? 12 24 38 20 40 48 48 ?

Ampullaria 16 44 ? ? 44 ? 12 24 36 20 36 48 48 ? van den Biggelaar and

Haszprunar, 1996

Viviparius 16 36 ? ? ? ? 12 24 40 20 44 47 48 ? van den Biggelaar and

Haszprunar, 1996

Valvata 16 40 ? ? ? ? 12 24 32 20 40 44 41 ? van den Biggelaar and

Haszprunar, 1996

Opisthobranchia 21 39 99 73 62 132 12 22 40 22 34 43 30 41

Aplysia 24 52 ? ? ? ? 12 18 38 24 37 41 37 41 Carazzi, 1905

Umbrella 24 44 121 91 67 ? 12 24 38 16 29 47 25 38 Heymons, 1893

Tethys 16 28 ? 65 58 ? 12 24 65 24 37 41 37 41 Viguier, 1898

Fiona 24 40 76 63 60 132 12 24 32 24 36 44 25 45 Casteel, 1904

Elysia 16 29 ? ? ? ? 12 20 29 24 29 ? 25 ? Pelseneer, 1911

Pulmonata 16 37 102 68 52 123 12 24 33 22 38 43 32 44

Physa 16 41 123 72 67 123 12 24 29 24 41 44 29 52 Wierzejski, 1905

Lymnaea 16 36 ? ? ? ? 12 24 29 21 41 46 25 24 van den Biggelaar and

Haszprunar, 1996

Biomphalaria 16 45 91 76 55 ? 12 24 32 24 40 40 25 41 Camey and Verdonk, 1970

(continued )


Planorbis 16 39 91 55 49 ? 12 24 32 24 46 49 34 49 Holmes, 1900a

Argolimax 16 32 ? ? 44 ? 12 24 40 20 28 36 36 46 Carrick, 1939

Limax 16 30 ? ? 44 ? 12 24 36 20 32 40 40 49 Kofoid, 1905

Sorbeoconcha 16 29 74 58 55 87 12 24 35 23 39 51 30 39

Hydrobia 16 28 ? ? ? ? 12 24 24 24 42 45 37 42 van den Biggelaar,

pers. comm.

Littorina 16 28 68 68 48 80 12 24 36 24 40 44 28 36 Delsman, 1914

Bithynia 16 28 65 55 41 49 12 24 41 24 44 81 41 46 Dam, 1986

Crepidula 16 29 88 55 100 100 12 24 38 20 34 52 25 30 Conklin, 1897

Serpulorbis 16 29 ? ? ? ? 12 24 ? 24 ? ? 29 ? Holmes, 1900b

Pterotrachea 16 32 ? ? 32 ? 12 20 ? 24 ? ? 33 ? Fol, 1896

Argobuccinum 16 28 ? ? ? ? 12 24 ? 20 ? ? 29 ? Philpott, 1925

Busycon 16 29 ? 55 55 ? 12 24 38 24 34 55 25 48 Conklin, 1907

Nassarius 16 28 ? ? ? ? 12 24 ? 20 ? 31 28 30 Grachtrup, 1991

Ilyanassa 16 28 ? ? ? ? 12 24 31 24 ? ? 28 ? Clement, 1952

Numeric values indicate embryo cell number at formation of each cell lineage by taxon. Composite OTUs (operational taxonomic units) are shown inbold. The 1q cell lineage is invariant (8 cells) and is not included here. ?5missing data.

Major gastropod subclade data set derived from above

Character number = 1 2 3 4 5 6 7 8 9 10 11 12 13 14

Cell lineage = 1q1 1q11 1q112 1q121 1q22 1q222 2q 2q1 2q11 3q 3q1 4Q 4d 4d1

Polyplacophora 16 24 54 36 32 60 16 32 60 24 54 85 73 113

Patellogastropoda 16 32 44 41 32 60 16 32 52 32 60 63 64 ?

Vetigastropoda 16 32 52 44 32 60 12 24 44 24 48 64 64 90

Neritopsina 16 28 ? 49 ? ? 12 24 41 24 41 49 41 49

Architaenoglossa 16 40 ? ? 44 ? 12 24 38 20 40 48 48 ?

Valvatoidea 16 40 ? ? ? ? 12 24 32 20 40 44 41 ?

Opisthobranchia 21 40 99 65 60 132 12 24 38 24 36 43 25 41

Pulmonata 16 38 91 72 49 123 12 24 32 23 41 42 32 48

Sorbeoconcha 16 28 68 55 48 80 12 24 37 24 40 49 29 39

NEXUS data set for PAUP� analyses

Character number = 12345 67890 1234

Polyplacophora 00000 00001 0000

Patellogastropoda 02000 00012 110?

Vetigastropoda 02000 01121 2100

Neritopsina 01?0? ?1131 3211

Architaenoglossa 03??1 ?1140 321?

Valvatoidea 03??? ?1150 331?

Opisthobranchia 13112 21141 4321

Pulmonata 03111 21151 3321

Sorbeoconcha 01111 11141 3221

Gastropoda taxon data set collated from Guralnick and Lindberg (2001) (continued )

TaxonCell Lineage

Source

1q1 1q11 1q112 1q121 1q22 1q222 2q 2q1 2q11 3q 3q1 4Q 4d 4d1


phyletic patterns of early development in gastropod molluscs

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