Molecular phylogeny and morphological evolution of laqueoid brachiopods

14 Pages·2001·5.7 MB·English

by  Michiko Saito

Paleontological Research, vol. 5, no. 2, pp. 87-100, June 29, 2001
(0 by the Palaeontological Society of Japan
Molecular phylogeny and morphological evolution
of laqueoid brachiopods
MICHIKO SAITO1 and KAZUYOSHI ENDO2
'JSPS Research Fellow in the Department ofEarth and Planetary Science,
University of Tokyo, Tokyo, 113-0033, Japan (e-mail: [email protected])
2Department ofEarth and Planetary Science, University of Tokyo, Tokyo, 113 0033, Japan
(e-maihendo©eps.s.u-tokyo.ac.jp)
Received 4 September 2000; Revised manuscript accepted 10 March 2001
Abstract. One of the virtues of molecular phylogeny for paleontology is that it can provide inde-
pendent and often reliable sets ofdata from living relativesto test various evolutionary hypotheses
inferred from fossil forms. In this study, we present results of a molecular phylogenetic analysis
of 12 species of 7 genera belonging to the Laqueoidea, which is the most prolific ofthe brachiopod
superfamilies in the seasaround Japan. Ontoa phylogenetictree based on partial sequences(1218
bp) of the mitochondrial coxl gene, we superimposed various external and internal morphologic
characters of both juveniles and adults forthetaxa examined. The resulting patterns indicated that
several lineages experienced paedomorphic evolution in termsofthe brachidial (loop) morphology,
and that, contrary to some traditional views, certain adult features, such as the bilateral loop, pos-
session of a cardinal process, and a rectimarginate commissure, had homoplasious distributions.
Examination of the character distributions also revealed, however, that anterior nonbifurcation of
the septal pillar at the axial phase is a synapomorphyfora majorclade recognized in the molecular
analysis. Those results suggest that early loop ontogeny, information about which is still fragmen-
tary, would be useful in assessing relationships among laqueoid brachiopods, including certain
Mesozoic genera.
Key words: Brachiopoda, cytochrome c oxidase (coxl) gene, Laqueoidea, loop ontogeny,
I
mitochondrial DNA, molecular phylogeny, Recent
Introduction Although molecular trees are only working hypotheses of
the true evolutionary relationships of living species, they are
The Laqueoidea is one of the larger terebratulide brachio- useful in providing a basis fordiscussion of the likely history
pod superfamilies, being well represented in both present- of a character of interest. In studies of morphological char-
day waters and Cenozoic strata of Japan. The members of acter states, predictions can be made about the probable di-
this superfamily, as well as other superfamilies within the rection of morphological character state transformations and
order Terebratulida, are characterized by the possession of combinations of characters in basal versus derived species,
calcareous internal skeleton known as the loop which con- and therefore wecan reassess the morphological characters
tinually undergoes considerable morphological change dur- that support the relationships. Because only morphological
ing growth before attaining the full adult stage. Due to its characters can be used to establish the phylogenetic affini-
complexity and diversity, loop morphology has been the ties ofancient fossil taxa, the success ofa morphological ap-
parmiomnegtoloalqufeooridthebraincfheiroepnocdesoafndphyfloorgetnheeticclasrseilfaitciatoinosnhiposf cphraoraacchtefrorstfaotsesielvsolcuatinonbeareinccornesaisdeedregdreianttlhyeilfigphattotferanns ionf-
long-looped brachiopods generally at various taxonomic dependently estimated phylogeny.
levels (Hatai, 1936, 1940; Muir-Wood et al., 1965; Previous brachiopod molecular systematics have been
MacKinnon, 1993). However, the assumption that loop mor- based on immunological comparisons of shell macromole-
phology reflects phylogeny has not been fully tested, norhas cules (Collins et al., 1988; Curry et al., 1991; Endo et al.,
it been possible to discuss loop evolution without the risk of 1994) and on nucleotide sequence comparisons of nuclear
circulararguments. Ideally phylogenies should be based on 18S ribosomal ribonucleic acids (rRNA) and mitochondrial
characters that are completely independent of the loop. One 12S rRNA (Cohen and Gawthrop, 1996, 1997; Cohen era/.,
such would be molecular characteristics. 1998a, 1998b). The novel overall patterns of loop evolution
88 Michiko Saito and Kazuyoshi Endo
that the immunological data indicated were largely unsup- Table1. Specimensusedinthisstudyandtheirsamplinglocali-
ported by the results of 18S rRNA sequence comparisons ties. Accession numbers refer to the DDBJ nucleotide sequence
(Cohen and Gawthrop, 1997; Cohen etal., 1998b). Besides, database.
titiwonasshidpisffaicmulotnugsicnlgostehleyirmemlautneodloggeincearla.daEtvaetno wrietsholtvheer1el8aS- Species Locality Acncuemsbseiron
rRNA data, which offered direct measurements of molecular
similarity and thus are more reliable, detailed relationships Ingroup
among the long-looped terebratulide brachiopods remained (Laqueoidea)
unclear because the tempo of the 18S rRNA sequence evo- Laqueusrubellus 1 Sagami Bay AB026501
lution was considered too slow to provide adequate varia- L. rubellus2 Sagami Bay
tions among these forms (Cohen era/., 1997). L. rubellus3 Sagami Bay
Both the nucleotide and amino acid sequences of the L blanfordi Otsuchi, Tohoku AB026502
mitochondrial cytochrome c oxidase subunit (coxl) gene
turned outto provide a potentially useful frameIworkforshal- L quadratus 1 SWofOshima AB026505
lower phylogenies, especiallyofthe relationships among the L. quadratus2 SWofOshima
long-looped laqueoid brachiopods (Saito et al., 2000). In L californicus Monterey Bay, AB026503
this paper, we report the phylogenetic relationships of California, USA
laqueoid brachiopods inferred from the cox7 sequences and L c. vancouveriensis Monterey Bay, AB026504
discussevolutionary processes ofthe loopand ofothermor- California, USA
phologiccharacters in laqueoid brachiopods, including some Pictothyrispicta 1 off Mishima AB026506
possibly basal Mesozoic fossils. Pictothyrispicta2 Sagami Bay
Monica nipponica Izu Islands, AB026509
Material and methods W
ofTakase
Brachiopod samples and molecular phylogenetic analy- Frenulina sanguinolenta 1 Vava'u, Tonga AB026510
sis.—Twenty-seven specimens representing a total of 16 F. sanguinolenta2 Vava'u, Tonga
species of terebratulide brachiopods including 11 laqueoid Shimodaiapterygiota 1 Off Shimoda AB026511
species were available forthis study (Table 1). S. pterygiota2 OffShimoda
Full details of DNA extraction, amplification and sequenc- Terebrataliacoreanica 1 Otsuchi, Tohoku AB026508
ing methods are described in Saito et al. (2000). In brief, T. coreanica2 Wakkanai, Hokkaido
wceoxrle osbetqauienendcebsyt(h1e21di8rebctpsoerqu4e0n6ciangmionfoDNacAidasmpilnifliecnagttiho)n Coptothyrisgrayi1 Otsuchi, Tohoku AB026507
products synthesized by PCR. Amino acid sequences were C. grayi2 Wakkanai, Hokkaido
deduced by reference to the genetic code of brachiopod Outgroup
mitochondrial DNA (Saito etal., 2000). Phylogenetic analy- (long-looped forms)
sis by maximum-parsimony (MP) was performed with PAUP
version 3.1 (Swofford, 1993), using the exhaustive search Ecnomiosasp. 1 Izu Islands AB026512
algorithm and equalweighting forall substitutions. Toevalu- Ecnomiosasp. 2 Izu Islands
ate the robustness of the internal branches, 500 bootstrap Campagessp. SW ofYonejima AB026513
replications were executed. Analysis by neighbor-joining Outgroup
(NJ; Saitou and Nei, 1997) and maximum-likelihood (ML) (short-looped forms)
were performed with Molphy version 2.3 (Adachi and Terebratulina crossei Otsuchi, Tohoku AB026514
Hasegawa, 1996a) using the mtREV24-F model (Adachi Terebratulinapacifica offOshima AB026515
and Hasegawa, 1996b) for amino acid data and HKY85 Gryphusdavidsoni S ofOshima AB026516
model fornucleotidedata (Hasegawa era/., 1985), usingthe
"Local Rearrangement Search" option. For each internal
branch, a local bootstrap probability (LBP) was estimated by position nucleotide sequences were used as data sets.
the RELL method (Kishino et al., 1990) with 1000 replica- Because little variation was detected in the amino acid se-
tions. TreeView version 1.4 (Page, 1996) was used to draw quences and the 1st and 2nd codon positions of nucleotide
trees. sequences, analyses of five Laqueus species were per-
Because of the low intraspecific nucleotide sequence formed separately with full lengt—hs of the nucleotide data.
variations in the examined individuals (less than 2%), and Morphological observations. Observation of juvenile
the lack of any amino acid difference within each species, loop morphologies of two laqueoid species, Jolonica
one individual was selected to represent the species in the nipponica and Terebratalia coreanica, was carried out on a
phylogenetic analysis. These representative nucleotide se- Hitachi S-2400S Scanning Electron Microscope using the
quences will appear in the DDBJ nucleotide sequence data- methods described by Saito (1996).
base with the Accession Numbers AB026501 -AB026516
shown in Table 1.
For analysis of deeper relationships within the
Laqueoidea, both the amino acid and the 1st and 2nd codon
Molecular phylogeny of laqueoid brachiopods 89
Results they are generally positioned close to one anotherin the four
cladograms. Tree 4 shows early branching of Shimodaia
Laqueoid relationships within the 6 genera.
Of the terebratulides analyzed, Ecnomiosa sp. and The NJ analysis consistently supported Tree 1 (Figure 2).
Campages sp. clustered basal to the laqueoids and The ML analysis supported Tree 1 or Tree 2, however, the
monophyly of laqueiods were strongly supported (100% log-likelihood differences among Trees 1 to 3 are very small
LBP. Figure 1). Therefore, we used Ecnomiosa sp. and when amino acid sequences are used. The LBP support for
Campages sp. as the outgroups for the analyses of all the branch including Terebratalia or Coptothyris is low (19
laqueoids sampled and within the species of Laqueus.
Analyses were also made for an ingroup comprising the 6
genera of Laqueoidea using Laqueus rubellus as outgroup. Tree 1
Laqueus
Analyses based on different tree-building methods (NJ, .
ML, and MP) and different data sets converged to indicate Shimodaia
four possible topologies for the relationships among .
laqueoid genera (Trees 1 to 4; Figure 2). The results of the - Frenulina
molecularphylogenetic analysisare summarized in Figure 3.
All resulting trees clearly indicated the basal placement of . Pictothyris
Laqueus in the Laqueoidea. The local bootstrap support of Jolonica
this node is high in all analysis (99-100%). Among the re-
maining six genera (Terebratalia, Coptothyris, Shimodaia, - Terebratalia
Frenulina, Pictothyris and Jolonica), the close relationship Coptothyris
between Jolonica and Pictothyris is consistently supported
by high bootstrap values (82-99%). Three of the four trees Tree 2
(Trees 1 to 3) show very similar topologies: the close asso- Laqueus
ciation of Shimodaia-Frenulina-Pictothyris-Jolonica, with
Terebratalia
Terebratalia and Coptothyris left outside. The positions of
Terebratalia and Coptothyris differ slightly in each tree but Coptothyris
Shimodaia
Frenulina
Pictothyris
Jolonica
ooica
Tree 3
Laqueus
Coptothyris
Terebratalia
Shimodaia
Frenulina
Pictothyris
^quadrat"5
Jolonica
*%&&»
Tree 4
4P
Laqueus
w
Shimodaia
\\ Terebratalia
Coptothyris
Ecnomiosa sp.
Campages sp. Frenulina
Pictothyris
0.1 substitutions/site
Jolonica
Figure 1. NJ tree based on amino acid sequences. The
number at each internal node of the tree indicates the percent- Figure 2. Four possible topologies for the relationships
age of node occurrence in 500 bootstrap replicates. among laqueoid genera.
—
90 Michiko Saito and Kazuyoshi Endo
ML
TreeID. Treetopology MP aa 1st+2nd
aa 1st+2nd InL BP InL BP
Tree 1 ((Laq,((((Pic,Jol),Fre),Shi),(Tra,Cop))),Ecn,Cam) 228 349 -2418.64±109.10(ML) 0.2887 -2855.96±101.53(ML) 0.4484
Tree2 ((Laq,(((((Pic,Jol),Fre),Shi),Cop),Tra)),Ecn,Cam) 230 351 -2419.42±108.87(-0.8) 0.2626 -2863.78±102.18(-7.8) 0.0369
Tree3 ((Laq,(((((Pic,Jol),Fre),Shi),Tra),Cop)),Ecn,Cam) 228 349 -2419.54±109.61(-0.9) 0.2410 -2859.35±101.83(-3.4) 0.2996
Tree4 ((Laq,((((Pic,Jol),Fre),(Tra,Cop)),Shi)),Ecn,Cam) 226(MP) 348(MP) -2423.61±109.48(-5.0) 0.2077 -2860.59±101.85(-4.6) 0.2151
ML
TreeID. Treetopology MP aa 1st+2nd
aa 1st+2nd InL BP InL BP
Tree 1 (Laq,((((Pic,Jol),Fre),Shi),(Tra,Cop))) 125 206 -1852.65±77.85(-5.5) 0.0715 -2183.02±75.88(-3.9) 0.0891
Tree2 (Laq,(((((Pic,Jol),Fre),Shi),Cop),Tra)) 124 206 -1847.14±77.19(ML) 0.6903 -2179.14±75.71(ML) 0.4130
Tree3 (Laq,(((((Pic,Jol),Fre),Shi),Tra),Cop)) 124 206 -1852.30±78.06(-5.2) 0.1245 -2182.64±75.92(-3.5) 0.1915
Tree4 (Laq,((((Pic,Jol),Fre),(Tra,Cop)),Shi)) 123(MP) 205(MP) -1861.79±79.67(-14.6) 0.1137 -2182.97±76.15(-3.8) 0.3064
Figure 3. Summaryofphylogeneticanalysisshowing thetotal maximum parsimonytreelength,the log-likelihood (±stan-
darderrors)andthebootstrapprobabilitiesforeachoftheplausibletrees. Speciesnameabbreviations: Laq=Laqueusrubellus,
Pic = Pictothyrispicta, Jol = Jolonica nipponica, Fre = Frenulinasanguinolenta, Shi = Shimodaiapterygiota, Tra = Terebratalia
coreanica, Cop= Coptothyrisgrayi, Ecn= Ecnomiosasp., Cam= Campagessp. UpperBox: relationshipsof7laqueoidgenera
with Ecnomiosa sp. and Campages sp. as outgroup. Lower Box: relationships of 6 laqueoid genera (Shimodaia, Frenulina,
Jolonica, Pictothyris, Coptothyris, Terebratalia) with Laqueusrubellusasoutgroup. aa: amino acid data. 1st+ 2nd: nucleotide
data of 1st and 2nd codon positions.
66%) in all analyses. The node ofthe Shimodaia-Frenulina- Ecnomiosasp.
LPiBcPtosth(y7r0i-s-1J0o0l%o)n.ica clade is supported by moderate to high -C—ampagessp.
The MP analysis consistentlysupported Tree 4 (Figure2). Laqueus rubellus
~
However, the tree length differences amongst the fourtrees -100- j L
— blanfordi
aIrnedeoxnl(yRlo)nfeoroarlltfwoourstteoppsol(oFgiigeusrewa3)s. aBlessoidreelsa,titvheleyRleotwen(tRilo=n -100- ™—1 L quadratus
0.446-0.663), indicating that support for Tree 4 in MP —L californicus
-100-
analysis is not strong. When 500 bootstrap replicates were 1 Lc.vancouveriensis
performed, the resulting consensus trees showed either un-
resolved trichotomy or the clustering of Shimodaia- Figure 4. NJtreeofcoxlnucleotidesequencesforthere-
Frenulina-Pictothyris-Jolonica with a low BP value (51 - lationships within the genus Laqueus. The same topologywas
56%). It is known that the MP analysis is more susceptible obtained byothermethodsofanalysis (MPand ML). The num-
to 'unequal rate effects' than the NJ or ML analysis, and can bers in the tree represent LBP values.
lead to a wrong tree when the nucleotide substitution rates
greatly vary among different branches (Saitou and Imanishi, same tree topology.
1989). The observed branch length variation among the
ingroup taxa (Figure 1) suggests that the tree indicated by Character state distributions among laqueoid brachio-
the MP analysis may not be reliable. pods
These results lead to the conclusion that any one of Tree Molecular analyses of coxl sequences, as described
1, 2, or3 represents the best estimate ofthe true phylogeny, above, provide apreliminaryframeworkfortheelucidation of
but the available coxl data being inadequate to make afinal phylogenetic relationships among some laqueoid brachio-
determination from among them. More data are needed to pods. Onto this molecular framework, we superimposed
resolve the positions of Terebratalia and Coptothyris. Thus, some morphological characters of those brachiopods, such
the strict consensus tree of Trees 1 to 3 is proposed as a as shell traits (outline, commissure shape and coloration),
basis for reconstruction of laqueoid evolution. adult loop morphology, cardinalia at the annular phase of
Figure 4 gives the ML tree of 5 species of the genus loopontogeny, andtypeoftheseptal pillarattheaxial phase
Laqueus. Two coherent groups were assessed; (1) the (Figure 5). Details ofthe selected morphological characters
Japanese group (L. rubellus, L. blanfordi, L. quadratus) and for each species are summarized in Table 2. Loop
(2) the North American group (L. californicus, L. c. ontogenetic series of laqueoid species are shown in Figure
vancouveriensis). Each cluster was supported by a high 6. Figure 7 illustrates hitherto undescribed early loopstages
LBP value (100%). The NJ and MP analyses yielded the of Terebratalia coreanica and Jolonica nipponica.
Molecular phylogeny of laqueoid brachiopods 91
Table 2. Comparisons of selected morphological characters of 7 species of the Laqueoidea.
maximum adult loop axial/annular cardinal deltidial ornament
Species size (cm) pattern septal pillar cardinalia process plates inadult andcoloration
Laqueus 3.5 bilateral bifurcate innerand outer hinge plates, inner rest- absent conjunct yellowish red with stripes
mbellus ing on the medianseptum
Pictothyhspicta 3.5 latero- nonbifurcate no innerhinge plates, the cardinalia are present conjunct irregulardivaricating stripesof
vertical divergent white upon red background
Jolonica 2.5 bilacunar nonbifurcate divided hinge plates, with high crural- present conjunct rose-red; some have interven-
nipponica bases, hinge-socketsdeep ingbandsoflightyellowmottling.
Frenulina 1.5 bilateral nonbifurcate thecardinaliabeardisjunct, innerhinge- present disjunct in yellowish brown with short ir-
sanguinolents plates elevated well above the valve small conjunct regularred stripes marginally
floor in large
Shimodaia 0.7 incomplete nonbifurcate steeplydipping innerhinge plateswhich absent disjunct red-mottled, with intervening
pterygiota annular convergeon a low medianseptum bandsofwhite mottling.
Terebratalia 5.9 trabecular bifurcate callus between the socket-ridges joined present conjunct red with layersofwhite,
coreamca toseptum ratherdull
Coptothyris 5.0 teloform bifurcate callusdepositbetweenthesocket-ridges present disjunct dull redwith radial ribs
grayi with which septum unites
Shellshape andcoloration.— Externally, laqueoid species which converge on a low median septum to form a sessile
exhibit great variability in shell size and shape. In this study, septalium, comparable to that occurring in young L. rubellus
it became apparent thatthe onlyexternal shell characterthat and Laqueussp. (Saito, 1996; MacKinnon etal., 1997). This
supported phylogenetic relationshipswasthe pattern of shell resemblance may also have resulted from parallel evolution.
—
coloration (Figure 5; top and second row). All the species in Juvenile loop morphology. At the axial phase of early
the clade of Shimodala-Frenulina-Plctothyris-Jolonica ex- loop development, when the median septum has a pair of
hibit irregular red stripes or mottling patterns, while shells of flanges on its posterior part, the anterior part of the median
others are radially striped (in L. rubellusand T. coreanica) or septum bifurcates only in the basal species in the molecular
have uniform coloration (in C. grayi, L blanfordi, L. phylogenetic tree, namely, L. rubellus, C. grayi and T.
quadratus, L. californicus and L c. vancouveriensis). Other coreanica (Figure 5; fifth row). In all other species that form
external characters, such as the type ofthe commissure and a clade, i.e., F. sanguinolenta, P. picta, J. nipponica and S.
completeness of deltidial plates, did not show any system- pterygiota, the septal pillar remain nonbifurcate until the an-
atic distribution on the molecular phylogenetic tree. nular phase (Figure 5; fifth row; boxed; Saito, 1996;
Adult loop morphology.—The adult loop pattern is often MacKinnon etal., 1997). Although the adult loop patterns
thought to represent phylogenetic affinity among laqueoid may be misleading, early bifurcation of the septal pillar may
genera, and has been used as a key character to divide the be a useful character in assessing relationships among
superfamily into families and subfamilies. For example, laqueoid genera.
Laqueus and Frenulina have often been included in the
same subfamily (Kingeninae in Richardson, 1975; Discussion
Laqueinae in Smirnova, 1984) based on their possession of
a bilateral adult loop. A close relationship between Laqueoid classification
Pictothyhsand Laqueushas also been maintained based on Taxonomic assignments of the seven laqueoid genera in-
similarity of external characters, as well as adult loop pat- vestigated in this paper (Laqueus, Terebratalia, Coptothyris,
terns; the adult laterovertical loop of Pictothyhs has been Shimodaia, Frenulina, Jolonica and Pictothyhs) have been
considered to be at a stage one step more advanced than controversial for a long time. Opinions as to which genera
that of Laqueus (see Thomson, 1927; Hatai, 1940; should be included in the family Laqueidaevarieddepending
Smirnova, 1984). on the features that each author conjectured important. For
However, the results of the molecular study suggest that example, Richardson (1973, 1975) considered the families
these interpretations, based on adult loop morphology, are Kingenidae, Macandreviidae and Laqueidae as synony-
not reliable. The three genera possessing a bilateral, or mous, and proposed uniting them in the family Laqueidae,
laterovertical, adult loop (Figure 5; third row; boxed) did not based on resorption patterns in loop development and the
form a clade, supporting the conclusion that a bilateral loop presence of dental plates. In this view, the seven ingroup
appeared independently in the lineage leading to Laqueus genera compared in our molecular study are included in the
and Frenulina. family Laqueidae. Smirnova (1984) defined the Laqueidae
—
Cardinalia. The cardinal process is prominent in most as those with a loop of the late frenuliniform stage (i.e.
laqueoids; however, species belonging to the genera bilacunar loop) or of more advanced stages, in which the
Laqueusand Shimodaia lack it. The molecularphylogenetic connections between the ascending and descending
tree indicates that the cardinal process may have been lost branches remain joined to the septum at all stage. In so
at least twice independently (Figure 5; fourth row). S. doing, she included a numberof lower Cretaceous genera in
pterygiota possesses steeply dipping inner hinge plates the Laqueidae (Zittellina, Zeuschneria, Tulipina, Waconella),
92 Michiko Saito and Kazuyoshi Endo
Laqueus Shimodaia Frenulina Pictothyris Jolonica Coptothyris Terebratalia
m
Figure 5. Morphological charactersoflaqueoidspeciessuperimposedonthe molecularphylogenetictree. Thetreetopologyrep-
resents the consensus oftheTrees 1, 2, and 3 (cf. Figure 3). Vertical lengths ofthe branchesare arbitrary. Morphological characters
(from toptobottom): anteriorviewoftheshells;dorsalviewoftheshells; adultlooppattern; cardinaliaintheannularphase; septal pillar
at the axial phase. The drawings are not strictly to scale. The rectimarginate commisure of Laqueusand Pictothyris (top row; boxed)
which was previously considered to be evidence uniting these genera, appeared separately in the molecular phylogenetic tree. In the
shell external features, the red-white dot coloration (second row; boxed) supports a close relationship between Shimodaia, Frenulina,
Pictothyrisand Jolonica. Characterssuchasthe adultbilateral orlatero-vertical loop pattern (third row; boxed), andtheabsenceofcar-
dinalprocess(fourth row; boxed),donotreflectphylogeny. Thenon-bifurcationoftheseptalpillarintheaxialphase(bottom row; boxed)
supports the Shimodaia-Frenulina-Jolonica-Pictothyrisclade.
Molecular phylogeny of laqueoid brachiopods 93
but excluded certain genera such as Terebratalia and play a bilacunar loop, a loop with two pairs of connecting
Coptothyris, which exhibited a trabecular or teloform adult bands (lateral and mediovertical), although the width of the
loop pattern. Zezina (1984) elevated the subfamily bands are different from that in the bilateral loop such asthat
Terebrataliinae (Richardson, 1975) to family status, and dis- found in Laqueus. The adult loop phases of both Shimodaia
tinguished it from the Laqueidae that accommodated such and Jolonica are comparable with juvenile loop phases in
genera as Laqueus, Frenulina, Aldingia, Jolonica, Pictothy- other laqueid members, and based on the molecular
ris, Compsohaand Ecnomiosa. More recently, in summariz- cladograms (Figure 5), it is more parsimonious to consider
ing the biogeography ofarticulated brachiopods, Richardson the abbreviated ontogenies of Shimodaiaand Jolonicaas in-
(1997) included 13 living genera in the family Laqueidae dependent synapomorphies.
{Coptothyris, Jolonica, Pictothyris, Terebratalia, Laqueus, Williams and Hurst (1977) pointed out that the most sig-
Tythothyris, Simplicithyris, Frenulina, Ecnomiosa, Compso- nificant trend within the post-Paleozoic long-looped
ha, Aldingia, and two otherundiscussed genera), butshe did terebratulides is the neotenous elimination of later stages of
not provide explicit criteria for this classification. loop ontogeny and a simultaneous simplification of the
Concerning the familial groupings of the seven Recent lophophore. Our results indicate that such complex evolu-
genera, the following two points can be drawn from the re- tionary processes have indeed been at work in laqueoids.
sults of our coxl study. Firstly, in the rooted monophyletic Bifurcation.— As reported by Richardson (1975) and Saito
cluster of laqueoids that included Terebratalia and (1996), the loopontogeniesof laqueoid species appearto be
Coptothyris, Laqueus branched off first, followed by a roughly the same until the bilacunarphase. However, at the
trichotomous cluster comprised of Terebratalia Coptothyris earlier axial phase, characterized by the development of
,
and the subcluster of Shimodaia, Frenulina, Jolonica, and septal flanges, two types of septal pillar can be recognized;
Pictothyris (Figure 5). Therefore, if Terebratalia and in one form of septal pillar the anterior edge becomes bifur-
Copthothyris are excluded from the Laqueidae and included cate whereas in the other form of septal pillar the anterior
in the Terebrataliidae, then Laqueus and the remaining four edge is nonbifurcate (Saito, 1996; Figure 6). In Laqueussp.
genera (Shimodaia, Frenulina, Jolonica, and Pictothyris) (Figures. 8.1, 8.2), T. coreanica (Figure 8.3) and C. gray!
should be accommodated in at least two separate families. (Figure 8.4), the septal pillar is anteriorly bifurcate. On the
A grouping including Laqueus, Shimodaia, Frenulina, other hand, Pictothyris sp. (Figure 8.5), Jolonica nipponica
Jolonica, and Pictothyristo the exclusion of Terebrataliaand (Figure 8.6), F. sanguinolenta (Figure 8.7) and Shimodaia
Copthothyris would be paraphyletic at best. pterygiota (Figure 8.8) all exhibit a nonbifurcate septal pillar
Secondly, in analyses of all the available terebratulide and retain remains of projections until the annular phase
forms including other than laqueoids, Ecnomiosa branched (Figure. 9.5-9.8).
off outside not only of the laqueoids, but also of the The results of molecular phylogeny indicate paraphyly for
terebratelloids of the Southern Hemisphere (Saito et al., in those with the bifurcate septal pillar (Figure 5). Thus, bifur-
press). Thus, on molecular grounds, the view of including cation is considered as the ancestral state and
Ecnomiosa in the family Laqueidae (Richardson, 1997) is nonbifurcation a synapomorphy. Two Mesozoic laqueoid
not supported. MacKinnon and Gaspard (1996) reported genera (Gemmarcula and Trigonosemus) show the anterior
that the descending branches of Ecnomiosa grow only from bifurcation of the septal pillar at the annular phase (Elliott
the crura unlike otherlong-looped brachiopods, justifying our 1947; Cooper 1955; Steinich 1965). This observation ac-
conclusion based on loop ontogeny. cords well with our contention that anterior bifurcation of the
Inclusion of Terebratalia and Coptothyris and exclusion of septal pillar is an ancestral character (Figure 5).
Ecnomiosa imply that the adult loop morphology alone can- Evolution of Bilateral Loop.— As discussed earlier, the
not be used as the prime character to define the coxl results indicated that species with a bilateral adult loop
Laqueoidea. Instead, presence of a pair of flanges on the did not form a monophyletic cluster (Figure 5). Two interpre-
septal pillar at the axial stage of loop ontogeny (Figure 8; tations are possible for the evolution of the bilateral loop;
Saito, 1996) and also the presence of dental plates in the one is that parallel evolution occurred, i.e., the bilateral loop
ventral valve appear to be more explicit and better-suited evolved twice independently, and the other is that the bilat-
character states to define this superfamily, and are to be in- eral loop is a plesiomorphic character.
corporated as such in the diagnosis ofthe Laqueoidea in the The formerinterpretation tends to be supported bythe fact
forthcoming revised Treatise (MacKinnon, pers. comm., that the two Cretaceous laqueoid genera, Gemmarcula and
2000). Trigonosemus, possess a trabecular loop. But the latter in-
terpretation becomes equally possible if anothergenus such
Processes of loop evolution as Waconellafrom the LowerCretaceous that has a bilateral
Paedomorphosis.— It is evident from comparison of the loop in the adult phase is taken into consideration.
ontogenetic sequences of the loop morphology (Figure 6) Waconella has been considered as one of the members of
with phylogenetic relationships (Figure 5), that the ancestral group from which Laqueus is derived, because
paedomorphic loop evolution occurred at least twice among of the possession of the same type of adult loop, cardinalia
laqueoids, in the lineages that produced Shimodaia and and shell shape, as well as the close geographical distribu-
Jolonica. As discussed in MacKinnon etal. (1997), adult in- tion with other laqueoid genera (Owen, 1970; Smirnova,
dividuals of Shimodaia have an incomplete annular loop, the 1984). Since a deep diversification between Laqueus and
brachidial ring being incomplete due to resorption ofthevery other laqueoid genera is inferred from the coxl analysis, this
narrow transverse band. Adult individuals of Jolonica dis- connection between Waconella and Laqueus seems quite
94 Michiko Saito and Kazuyoshi Endo
anterior
bifurcation
ofthe septum
bilateral
Figure 6.
Molecular phylogeny of laqueoid brachiopods 95
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96 Michiko Saito and Kazuyoshi Endo
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