Resurrection of Nucella ostrina (Gould, 1852), lectotype designation for N-emarginata (Deshayes, 1839), and molecular genetic evidence of Pleistocene speciation

9 Pages·2003·6.3 MB·English

by  P B Marko

THE VELIGER
© CMS. Inc.. 2003
The Veliger46(l):77-85 (January 7, 2003)
Resurrection of Nucella ostrina (Gould, 1852), Lectotype Designation for
N. emarginata (Deshayes, 1839), and Molecular Genetic Evidence of
Pleistocene Speciation
PETER MARKO'
B.
Molecular Systematics Laboratory, Natural History Museum of Los Angeles County, 900 Exposition Boulevard,
Los Angeles, California 90007, USA
RICHARD PALMER
A.
Department of Biological Sciences, University of Alberta, Edmonton, AB T6G 2E9, Canada
AND
Bamfield Marine Station, Bamfield, BC VOR IBO, Canada
GEERAT VERMEIJ
J.
Department of Geology, University of California, Davis, California 95616, USA
Abstract. Previous work demonstrating concordant patterns of reproductive isolation, fixed genetic differences, and
morphological differentiation indicates the existence of morphologically cryptic "northern" and "southern" species
within the nominal taxon Nucella emarginata. The southern species, which retains the name Nucella emarginata (De-
shayes, 1839), is characterized by four to five rows of spiral sculpture on the body whorl of the shell in the form of
regularly spaced knobs plus an adapical tooth or callus on the columella. The type locality for N. emarginata is San
Miguel Island, California. The northern species, N. ostrina (Gould. 1852) is characterized by five to six cords of
continuous spiral sculpture, a taller and more slender spire, and usually a more flared aperture than N. emarginata. The
type locality for A^. ostrina is Tillamook Bay, Oregon. Because Deshayes' original description of A^. emarginata was
based on four specimens (syntypes), we have re-figured and designated one ofthese syntypes as a lectotype. A lectotype
for A^. ostrina was assigned previously (Johnson, 1964). A new analysis of previously published mitochondrial DNA
sequences and molecular clock calibration dates from the fossil record also indicates a late Pleistocene divergence for
A^. ostrina and N. emarginata. A late Pleistocene divergence time, and the subtle nature ofmorphological differentiation
between these two species, together provide an important counter-example to the prevailing view that little speciation
occurred during the Pleistocene along rocky Californian shores, a period characterized by rapid and frequent environ-
mental change.
INTRODUCTION Because patterns ofgeographic variation in shell form are
particularly pronounced in Nucella. this genus provides
Accurate discrimination of biological species is essential
an unusually challenging group for characterizing the re-
for describing patterns of organismal diversity, a funda-
lationship between morphological form and reproductive
mental first step toward understanding the processes that
isolation.
Tgehnoerrpaete&diSvoelresi-tCyavaat,th1e99s4p;ecKileasutlaeuvelet(aKl.n,ow1l9t9o9n)., I1n99t3h;e A combination of data from genetic markers and mor-
ocenebrine gastropod genus Nucella Roding, 1798, per- phological characters, as well as direct evidence of repro-
vasive geographic variation in shell form within nominal ductive isolation, together indicate the existence of two
species has led to an extensive history oftaxonomic con- biological species within the nominal taxon A', emarginata
fusion at the species level (see Palmer et al., 1990). Cur- (Deshayes, 1839). First, Palmer et al. (1990) demonstrated
rently, four nominal species ofNucella on the west coast a fixed genetic difference at an allozyme locus (Isocitrate
ofNorth America are widely recognized in the literature. dehydrogenase-2, EC 1.1.1.42) between "northern" and
"southern" populations of A^. emarginata. Second, this
' Current address: Department ofMarine Sciences, 12-7 Ven- fixed allelic difference was also shown to be concordant
ableHall, CB#3300, UniversityofNorthCarolinaatChapelHill, with subtle morphological differences inboth shell andegg
Chapel Hill, North Carolina 27599, USA. capsule morphology (Palmer et al., 1990). Third, con-
Page 78 The Veliger, Vol. 46, No. 1
trolled laboratory crosses between northern and southern tochrome c oxidase I (COl) sequences from 50 individ-
populations failed to produce any offspring (Palmer et al., uals (Genbank accession numbers for mtDNA haplo-
1990). Lastly, a geographically broader survey of both al- types: AFO76536-AFO76560). We calculated maximum
lozyme loci and mitochondrial DNA (mtDNA) sequences likelihood sequence divergences among all COl haplo-
(cytochrome c oxidase 1) furtherrevealed that genetic and types with PAUP* 4.0 (Swofford, 2001) using the HKY
morphological differentiation between northern and south- model of nucleotide substitution (Hasegawa et al., 1985)
ern morphological forms of A', emarginata are consistent coupled with gamma-distributed rate heterogeneity
throughout a broad region of sympatry in central Califor- among nucleotide sites (Yang, 1994). Actual nucleotide
nia, between San Francisco and Point Conception (Marko, frequencies were assumed to equal the observed frequen-
1998). The combination of morphological, reproductive, cies, and the transition to transversion ratio (t) and the
and genetic differences now provides conclusive evidence shape parameter (a) for rate heterogeneity among sites
oftwo biological species within A^. emarginata: a northern were each inferredusing aNeighbor-joining treetopology
species found between Yakutat, Alaska and Point Concep- based on Jukes-Cantor genetic distances (Jukes & Cantor,
tion, California, and a southern species distributed from 1969). A log-likelihood ratio test (see Felsenstein, 1988;
San Francisco, California to Punta Eugenia, Baja Califor- Huelsenbeck & Crandall, 1997) was used to determine if
nia Sur (see Palmer et al., 1990; Marko, 1998). Nucella COl satisfied the criterion of substitution rate
The northern species was provisionally recognized as constancy, an assumption that must be valid in order to
Nucella ostrina (Gould, 1852) in an earlier paper (see infer divergence times from molecular sequences. In all
Marko, 1998). Here, we present formal systematic de- analyses, trees were rooted with haplotypes from the con-
scriptions for these two sibling species plus designate a geners A'^. canaliculata and A^. lima (Genbank accession
lectotype for A^. emarginata (a lectotype for N. ostrina numbers AF076561-AF076565).
was previously chosen by Johnson, 1964). Given only Using the procedure described by Nei & Li (1979), we
subtle morphological differences between these two spe- calculated the net sequence divergence at third positions
cies, we also investigate these species' time of diver- between species as p^e(„«> = Pab - 0-5 (Pa + Pb)' where
gence, based on analyses of previously published mito- Pa and pg are the mean sequence divergences among in-
chondrial DNA sequences (from Marko, 1998). We then dividuals within species A and B, respectively, and p^B
discuss the relevance of the timing of this speciation is the mean sequence divergence among individuals be-
event toward understanding spatial and temporal patterns tween species (also see Avise & Walker, 1998; Edwards
of morphological and species diversity in molluscan fau- & Beerli, 2000). Net nucleotide divergence more accu-
nas of the cool-temperate Eastern Pacific. rately estimates the time elapsed since population split-
ting because uncorrected gene divergences between spe-
MATERIALS and METHODS cies will always predate speciation (Nei & Li, 1979; Av-
ise & Walker, 1998; Avise, 2000; Edwards & Beerli,
Both Gould's and Deshayes' specimens were examined 2000). To determine the rate at which COl diverges, we
for comparison to the morphological differences that are used the split between A^. canaliculata and the N. emar-
associated with genetic differences and reproductive iso- ginatalN. ostrina clade as a calibration point, which is
lation between Nucella emarginata and N. ostrina (Palm- known from the fossil record to have occurred between
eret al., 1990; Marko, 1998). Shells from PBM'spersonal 5-10 Ma ago (Collins et al., 1996). The rates inferred
collection were examined and photographed to present a from this fossil calibration were then applied to the net
sampling of geographic variation in shell form within COl divergence between N. ostrina and N. emarginata
both species. Rather than attempting to document the en- to infer their time of separation.
tire range of variation in both species, and considering
that the basic morphological differences were recently SYSTEMATICS
figured elsewhere (Palmer et al., 1990), we instead fo-
cused on specimens that exhibit relatively subtle differ- Family Muricidae Rafinesque, 1815
ences in shell morphology. Material fromtheNatural His-
Subfamily Ocenebrinae Cossmann, 1903
tory Museum, London (NHM), Museum National
d'Histoire Naturelle, Paris (MNHN), The United States Genus Nucella Roding, 1798
National Museum of Natural History (USNM), the Nat-
ural History Museum of Los Angeles County (LACM), Nucella emarginata (Deshayes, 1839)
and the Zoological Institute of the Russian Academy of
Sciences (ZIRAS) were also examined. (Figures lA-D, 2M-T)
To determine whether limited morphological differen- —
tiation between these species reflects recent speciation, Purp1u8r4a1:epmia.r2g5i.na—tRaeevDee,sh1a8y4e5s:,3,1p8i3.9:10,3f6i0g.. 46D.e—sChoaoykees,,
we inferred the time of divergence for N. ostrina and A^. 1915: 203.
emarginata using previously published (Marko, 1998) cy- Tliais emarginata Vanatta, 1910: 38.
p. B. Marko et al., 2003 Page 79
Figure 1. A-D. Lectotype ofNucella einarginata (Deshayes, 1839). Shell length: 25 mm. E-G. Lectotype ofTV. ostriua (Gould. 1852).
Shell length: 20 mm. A and E. Apertural views: B and E Abapertural views. C and G. Apical views. D. Callus or tooth on the adapial
end ofthe aperture ofN. emarginata lectotype. Scale bar = 2 mm (F only).
Thais {Nucella) emarginata Dall, 1915: 569, pi. 75, figs. 2- Description: Shell ovate, body whorl typically large, and
3.—Oldroyd, 1927; 44, pi. 36, figs. 2-3. — spire both short and broadly conical. Color yellowish to
Nucel1l9a78e:ma4r6g,ifniag.ta2A4b-b4ot.t—,Pa1l9m1eA:r1et82a,lf,ig.1919900:9.325,McfLige.a3n., brown, some banded. Whorls convex. When shell sculp-
ture is well developed, spiral sculpturing consists ofreg-
Type material examined: Purpura einargiuata, MNHN ularly spaced knobs at the distal margins of the spiral
MNHN
syntypes. Purpura nipestris, syntypes. cords (Palmer et al., 1990: fig. 3). Body whorl with four
to five rows of major spiral cords; some specimens with
Designation of lectotype: Deshayes' descriptions were
based onfourdifferent specimens. We have thereforedes- minorcords between majorcords. Penultimate whorl with
two cords. Columella curved, flattened; color light brown
ignated the specimen in Figure 1 as the lectotype. to white. Aperture large, outer lip sometimes wavy (de-
Type locality: Purpura emarginata, San Miguel Island, pending on extent of external sculpturing), five teeth re-
California, USA. Purpura rupestris, no type locality re- cessed from margin. Typically with a tooth or callus on
corded. the adapical end of the aperture of the shell (Figures lA,
Page 80 The Veliger, Vol. 46, No. 1
p. B. Marko et al., 2003 Page 81
D). Egg capsules cylindrical with relatively short necks, populations found from San Francisco south. In some
distal flared margin. Shells and egg capsules ofA', eniar- populations where sculpture is weakly developed, such as
ginata are figured extensively elsewhere; for examples in the vicinity of Point Conception, California (e.g., Fig-
see Palmer et al. (1990). ures 2R, T), the early (juvenile) whorls ofthe shell often
exhibit the characteristic uniformly spaced knobs. One of
Geographic range: On rocky shores in the middle to
us (GJV) noticed that a small tooth or callus on the adap-
high intertidal between Punta Eugenia, Baja California,
ical end of the columella also characterizes the southern
Mexico and Fort Point, near San Francisco, California,
species (Figure ID). The presence of the adapical tooth
USA. Although a single specimen from Punta Eugenia,
BajaCalifornia Surhas been collected (LACM 51-43.16), can be subtle in thin-shelled specimens (e.g.. Figure 20).
but is often well developed in shells from wave-protected
N. emarginata appears to be rare south of Punta Cabras,
Baja California, Mexico. In 1993 and 1994, PBM found environments (e.g.. Figures 2M, Q). Due to its position
on the inner surface ofthe columella, the presence ofthe
A^. emarginata to be abundant (approximately five to 10 adapical tooth is often readily diagnosed by sliding a
individuals/m-) at Punta Descanso, PuntaMesquite, Punta
blunt probe overthe posteriorendofthe columella. Based
Banda, Punta Santo Tomas, and Punta Cabras. However,
7 km to the south ofPunta Cabras, only eight individuals on the correspondence between the moiphological char-
were found at Ejido Erendira; only four individuals were a(c1t9e9r0s,) trehteaisnosutthheernnasmpeecNi.esermeacrogginniaztead. by Palmer et al.
collected farther south at Punta Baja. These observations
Deshayes' syntypes were said by their collector, M.
catortrheespLoAndCMto:aonplatytetrwnofooufnd13inBatjhae Ccaollilefcotrinoinaslhotosusaerde Chiron, to have been collected in New Zealand (Deshay-
es, 1839). Dall (1915) later revised the type locality as
from south ofPunta Cabras (including the Punta Eugenia
San Miguel Island "where the typical form is abundant"
individual), totaling eight specimens. Nucella emarginata
(Dall, 1915:570). One of us (PBM) examined museum
is patchily distributed but abundant in southern California specimens from San Miguel Island (LACM 67-38.33,
wherever suitable rocky substrate is found. Between Point
60602, 60571, 60576) finding a mixture ofboth N. emar-
Conception, California and San Francisco, California, N.
ginata and N. ostrina morphologies. Although both spe-
etemraerygiBnaayt,aSiasnfoLuunids oBnalyy, iMnoermrboayBamye,ntHsalsfucMhooasnMBoany-, cies are likely present on San Miguel Island, we see no
reason to change the type locality given the apparent
and at Fort Point, just inside San Francisco Bay (see
LACM abundance of snails at this location possessing the char-
Palmer et al., 1990; Marko, 1998). material from
Tomales Bay. just north of San Francisco, includes two acteristic shell features of A', emarginata.
Dall (1915) suggested that Purpura lagenaria Duclos,
individuals that possess spiral knobs and an apertural
1832 (not of Lamarck, 1822) and Purpura rupestris Va-
gtoiontaht,aseuxgtgeensdtsinbgeytohantdtShaengFeroagnrcaipshcioc. PraBngMecoofllAe^c.teedmaerx-- leemnacrigeinnnaetsa,.1T8h46e,smyingthyptesbeofjuPn.iorrupsey.sntorinsym(sMNoHfNP)urpwuerrae
tensively in Tomales Bay between 1991-1997, but found
recently identified as Lepsithais lacunosus (Bruguiere,
no individuals with the uniquely derived morphological 1789), from New Zealand (B. Marshall, personal com-
features ofN. emarginata.
munication). However, the whereabouts of Purpura la-
Remarks: Purpura emarginata was first described by genaria Lamarck, 1822. figured by Duclos 1832, is un-
Deshayes (1839) but no figures were published in the known. This specimen may be in the Natural History Mu-
original description. A drawing was published 2 years seum of Clermont-Ferrand (France), which houses the
later (Deshayes 1841), but this figure captures little detail Duclos collection, but this collection is currently unavail-
of the shell. We therefore re-examined Deshayes' syn- able for study (P. Bouchet, personal communication).
types (Figure 1) and found that they possess the charac- Nevertheless, the specimen figured by Duclos (Duclos,
teristic knobby sculpture on the body whorl of the shells 1832: pi. 11, fig. 11) clearly possesses a curved siphonal
that is characteristic of the southern species described by canal. Therefore, iffrom the eastern Pacific, P. lagenaria
Palmer et al. (1990). Vanatta (1910:38) remarked that the is most likely not a member of the genus Nucella, and
name N. emarginata Deshayes refers to a "short-spired may instead be a specimen of Acanthiinicella Cooke,
rather rough surfaced form," likely referring to the typi- 1918.
cally short-spired shell and rough, knobby sculpture of Several authors (Reeve, 1845; Tryon, 1880; Vanatta,
Figure 2. Morphological geographic variation (apertural and apical views, respectively) among Nucella ostrina
(A-N) and N. emarginata (M-T). A, B. Sitka, Alaska (USNM 88842). C. D. Tatoosh Island. Washington. E, F.
Cape Arago, Oregon. G, H. ShelterCove, California. I. J. Ocean Beach, San Francisco, California. K, L. Soberanes
Point. California. M. N. Half Moon Bay. California. O, P. Pacific Grove, California. Q. R. San Luis Obispo.
California. S. T. Laguna Beach, California. Scale bar = 10 mm.
A
Page 82 The Veliger, Vol. 46, No. 1
Table 1
Comparison of morphological differences between Niicella ostrina and N. emarginata.
Shell character N. ostrina N. emarginata
Spire Taller and more slender Shorter and broader
Aperture Typically flared Narrow, with a callus or tooth on the
abapical surface
External sculpture Typically 5-6 continuous spiral cords Evenly spaced spiral knobs
Egg capsules Vase-shaped, with a longer neck Cylindrical, with a shorter neck, flared
distally
1910; Dall. 1915) regarded Purpura conradi Nuttall as a minorcords between majorcords. Penultimatewhorl with
junior synonym ofA^. emarginata. Purpura conradi, how- two cords. Columella curved, flattened; color dark purple
ever, was never described, known only from an unpub- to white. Apertural teeth not common. Egg capsules vase-
lished manuscript plus several specimens deposited in the shaped, generally more slender than in N. emarginata.
NHM
by Nuttall (see Reeve, 1845; Tryon, 1880). There-
fore, it is not an available name and we do not include it Comparison: See Table 1.
in our synonymy. Reeve, Vanatta, andTryon all remarked Geographic range: From Yakutat, Alaska, (Vermeij et
that the spiral cords ofthe P. conradi specimens are dis- al., 1990) to Point Conception, California (Marko, 1998),
continuous, giving the shell a rough, knobby exterior. but specimens also known from San Miguel Island, Cal-
Two ofus (PBM and GJV) have also examined the same ifornia (see above). Between San Francisco and Point
shells (NHM 1855.3.14.34) and concurthat they are spec- Conception, N. ostrina is found predominantly on wave-
imens ofN. emarginata. exposed shores and seldom occurs in calm water envi-
ronments.
Nucella ostrina (Gould, 1852)
Remarks: Nucella ostrina Gould (1852) is the oldest
(Figures lE-G, 2A-L) available name that has been applied to populations cor-
Purpura ostrina Gould, 1852: 244.—Gould, 1857: pi. 18, responding to the northern species. Although the N. os-
figs. 310a, b.—Johnson, 1964: 120, pi. 9, fig. 12—. trina lectotype has weak external shell sculpture, the spi-
Thais emarginata variety projecta Dall, 1915: 571. Dall, ral cords on the apex ofthis relatively tall shell are clearly
1921: 112 (refers to a figure in Dall, 1915, that is not continuous, the aperture is large, and the specimen lacks
T. emarginata van projecta). an adapical tooth on the columella. The only other taxon
Nucella ostrina Abbott, 1974: 182, fig. 1910 (in synonymy that potentially has priority over A', ostrina is Purpura
with N. emarginata).
lapillus var. anomala Middendorff, 1849, a species that
Type material examined: Purpura ostrina Gould 1852, resembles N. ostrina but which was synonymized withA^.
lectotype. Museum of Comparative Zoology, Harvard emarginata by Dall (1915). However, one of us (ARP)
University (MCZ 19275). Tliais emarginata variety ;7ro- recently examined the anomala holotype, recognizing it
jecta Dall 1915, holotype. United States National Muse- as simply a highly aberrant specimen of N. lapillus col-
um of Natural History (USNM 88842). Purpura lapillus lected in the North Atlantic.
variety anomala Middendorff 1849, holotype. Zoological Dall (1915) also published a detailed drawing ofa sin-
Institute of the Russian Academy of Sciences (ZIRAS gle specimen from Lituya Bay, Alaska (USNM 220975)
20633). that possesses spiral knobs and an adapical apertural
tooth. We have collectedextensively throughout southeast
Type locality: Purpura ostrina, Killimook [Tillamook
Alaska and have found no specimens that remotely re-
Bay], Oregon, USA. Thais emarginata variety projecta,
semble the southern species in these respects. In fact,
Sitka, Alaska, USA. Purpura lapillus variety anomala,
Alaskan specimens are typically unusually high spired
Lapland Russia (Barents Sea).
and very thin shelled, such as Dall's (1915) T. emarginata
Description: Very similar to A', emarginata. Shell ovate, var. projecta (Figures 2A, B, USNM 88842) from nearby
body whorl large, and spire both short and broadly con- Sitka, Alaska. Collections ofN. ostrina (LACM 15-11.
ical. Color white to dark purple, some banded. Base color and 75-77.5) from the vicinity of Lituya Bay all lack an
and banding variation extensive, greater than in N. emar- adapical tooth and are also high-spired shells with well
ginata. Whorls convex. When shell sculpture is well de- developed spiral cords, similar to T. emargiriata var.pro-
veloped, spiral sculpturing consists of continuous spiral jecta (Figures 2A, B). Although some specimens of N.
cords (Palmer et al., 1990:fig. 3). Body whorl with five ostrina do exhibit weakly nodulose or bumpy sculpture,
to six rows of major spiral cords; most specimens with the specimen figured by Dall from Lituya Bay is unlike
p. B. Marko et al., 2003 Page 83
any specimen we know of from north of San Francisco. emarginata and N. ostrina therefore provides an impor-
We therefore beheve that the southeastern Alaska locahty tant counter-example to the conclusion that little specia-
assigned to the single specimen from Lituya Bay is also tion occurred during the Pleistocene along rocky Califor-
in error. nian shores. Instead, for Nucella, the Pleistocene may
have been a period of limited morphological differentia-
RESULTS tion between species.
A likelihood ratio test indicates that a constant rate of Inferred divergence times based on molecularsequence
nucleotide substitution can be rejected across all COl nu- data have important caveats, even if sequences evolve at
a constant rate. Poor calibrations, due to inconsistencies
cleotide sites forNiicella emargiiiata andA^. ostrina (2Aln
= 48.0, df = 28, P < 0.025). However, third position einrrtohreifnosmsiollerceucolradr,colfotcekn ianntarloydsuecse(tLheee,gre1a9t9e9s;t sYooudrecre o&f
substitutions, most of which do not result in amino acid
= Yang, 2000). For example, Nucella canaliculata and the
changes, satisfy the rate constancy assumption (2Aln
24.8, df = 28, P > 0.5). Therefore, we restricted our N. emarginatalN. ostrina clade likely diverged earlier
than the fossil record indicates because actual splits al-
estimates of divergence times to third codon positions.
Using a divergence of 5—10 Ma for Nucella canaliculata rweacyosrd.preAdnateeatrhlieerapdpievaerragnecneceofofnetwhetacxaaliibnrattihoenfotsasxial
fraaontrdeCtoOhfelthA^ti.hridredmpoapsroigstiiintoainotnadsli.Nv.eGrigovseetnnrcientahoaftclN3au.dce1,e-l6lw.ae6%oospbtetrrianian1eadMnada wwhoiuclhd riensutlutrninwaosumladllyeirelidnfearnreedarrlaiteerotfiCmeOo1fdisveepragreantcieo,n
A^. emarginata differ by 1.1% at third positions, we infer ftoorceNn.eedmiavregrigneantcaeafnodrA^N..osotsrtinrai.naHoawnedveNr., aemparreg-Pilneaitsa-
A', emarginata and A'^. ostrina diverged 167,000-355,000 would entail a time of divergence for the calibration in
years.
excess of 40 Ma. Although we cannot reject an earlier
DISCUSSION time of divergence for our calibration taxa, an Eocene
divergence for A', canaliculata and the A^. ostrinalN.
The existence and identification of cryptic species has emarginata lineage (a crown clade within Nucella see
important implications for characterizing spatial and tem- Collins et al., 1996) is highly improbable given that the
poral patterns of species diversity and therefore for de- genus Nucella only first appears in the fossil record dur-
veloping hypotheses about the relative timing ofenviron- ing the latest Oligocene or earliest Miocene (Collins et
mental changes and speciation (Mayr, 1942; Levinton & al., 1996).
Simon. 1980; Michaux. 1989; Jackson & Cheetham, A second source of error we consider is that the
1990; Knowlton, 1993; Budd et al., 1994; Klautau et al.. amount of sequence divergence between our calibration
1999; Marko & Jackson. 2001). For example, because of lineages may be significantly underestimated. Although
the high frequency and relatively rapid pace of changes assuming an explicit model of nucleotide substitution
in climate, sea level, and coastal geomorphology along takes multiple substitutions at single nucleotide sites into
the Califomian coast during the Pleistocene, rates ofspe- account, error in the estimates of molecular divergence
ciation have been hypothesized to be relatively high dur- (i.e., branch lengths between taxa) may also result in poor
ing this period of time because such environmental estimates ofdivergence rates. Because the divergences of
changes are believed to cause disruptions in gene flow interest here are relatively recent (5 to 10 Ma), the prob-
between populations of intertidal marine organisms (Go- lem of saturation of nucleotide positions with multiple
likov, 1973; Valentine & Jablonski, 1983; Vermeij, 1989; substitutions is probably not an important factor: uncor-
Reid, 1990; Collins et al., 1996). rected mitochondrial third positions only begin to ap-
Direct comparisons ofmolluscan diversity between the proach saturation in Nucella after 5 to 10 million years
Pleistocene and Recent, however, do not support the hy- (Collins et al., 1996; Marko & Vermeij, 1999). Neverthe-
pothesis that speciation and extinction rates were elevated less, even if our estimates of sequence divergence are
during the last 1-2 million years: the strong similarity biased because of saturation, this bias is conservative
between Recent and Pleistocene faunas (e.g., Vedder & with respect to our conclusions: larger sequence diver-
Norris, 1963; Marincovich, 1976; Valentine, 1989) is in- gences between the taxa used to calibrate our molecular
terpreted as evidence that the effects of speciation and clock would result in larger rates ofsequence divergence,
extinction were likely negligible along rocky shores of which in turn would yield an even more recent range of
the Califomian coast during the last 1-2 Ma (Valentine divergence times for A^. emarginata and A^. ostrina.
& Jablonski, 1993; Lindberg & Lipps, 1996; Roy et al., The inherent difficulty in distinguishing biological spe-
1996). However, if many evolutionarily distinct species, cies based on morphology alone in Nucella suggests that
such as A^. emarginata and N. ostrina, have been lumped the process of speciation (i.e., the evolution ofreproduc-
into artificially cosmopolitan nominal species, rates of tive isolation) is notnecessarily accompanied by dramatic
speciation and extinction in the fossil record are likely morphological differentiation when compared to patterns
underestimated. A late Pleistocene separation for N. of geographic variation within species (also see Palmer,
Page 84 The Veliger, Vol. 46, No. 1
1985b). Therefore, interpretations of tiie fossil record of Deshayes, G. P. 1841. G. Poupre: Purpura. Magasin deZoologie
Nucella that employ the assumption that speciation may (Guerin), pi. 25.
be recognized by significant morphological changes (e.g., DucLOS, M. 1832. DescriptiondequekquesespeciesdePourpres,
servantde typeasix sectionsetabliesdanscegenre.Annales
KeiT, 1995) must be considered in light of the subtle dif-
des Sciences Naturelles 26:103-112.
ferences in shell form between the two most recently di- Edwards, S. V. & P. Beerll 2000. Gene divergence, population
verged species, N. emarginata and A^. ostrina. Although divergence, and the variance in coalescence time in phylo-
the extent of intraspecific variation in shell morphology geographic studies. Evolution 54:1839-1854.
in Nucella is somewhat unusual, making the recognition Felsenstein, J. 1988. Phylogenies from molecularsequences: in-
of biological species particularly difficult, the existence ference and reliability. Annual Review ofGenetics 22:521-
of cryptic species in rocky shore gastropods is not an 565.
uncommon phenomenon. For example, other prominent GoLiKOV, A. N. 1973. Species and speciation in poikilothermic
animals. Marine Biology 12:257-268.
ftohsisniali(zfaobrlmeertlayxaasssuicghneads tLoitAtcoarinntah,inLao,ttisae,eaMnadrkMoex&acVaenr-- Goul1d2,.AM.olAl.us1c8a52&. USnhietlelsd.SGtaotuelsdEx&plLoirnicnoglnE:xpBeodsittoino.n.5V1o0lpupm.e
meij, 1999) all harbor morphologically similar but genet- Gould, A. A. 1857. United States Exploring Expedition. Mol-
ically distinct species on the Pacific coast ofNorth Amer- lusca & Shells, Atlas. Gould & Lincoln: Boston.
ica (Murphy, 1978; Mastro et al., 1982; Marko & Ver- Hasegawa, M.. H. Kishino&T. Yano. 1985. Datingthe human-
meij, 1999). As a consequence, species identifications ape splitting by a molecular clock of mitochondrial DNA.
based purely on moiphological grounds must always be Journal of Molecular Evolution 22:160-174.
assessed in this context. Huelmsaetniboencka,ndJ.hPy.po&theKs.isA.teCsrtianngdaulslin.g 1m9a97x.imPhuymlolgiekenlyiheosotdi.-
Acknowledgments. Part ofthe research presentedherewas sup- Annual Review ofEcology and Systematics 28:437-466.
ported by the Graduate Group in Population Biology (UC Davis) Jackson, J. B. C. & A. H. Cheetham. 1990. Evolutionary sig-
and a National Science Foundation Dissertation Improvement nificanceofmorphospecies: atestwithcheilostomebryozoa.
Grant to PBM. We thank D. Geiger, J. McLean, V. Heros, and Science 248:579-583.
A. Moran for numerous comments and suggestions. We thank L. Johnson, R. I. 1964. The Recent MolluscaofAugustuaAddison
Groves (LACM), V, Heros (MNHN). T. Nici<ens (USNM), R Gould. United States National Museum Bulletin 239. Smith-
Mordan (NHM). and A. Baldinger (MCZ) for access to collec- sonian Institution: Washington. 182 pp.
tions and specimen loans. Jukes, T. H. & C. R. Cantor. 1969. Evolution of protein mol-
ecules. Pp. 21-132 in H. N. Munro (ed.). Mammalian Pro-
LITERATURE CITED tein Metabolism. Academic Press: New York.
Kerr, R. A. 1995. Did Darwin get it all right? Science 267:
Abbott, R. T. 1974. American Seashells. 2nd ed. Van Nostrand 1421-1422.
Reinhold Company; New York. 662 pp. Klautau, M., C. a. M. Russo, C. Lazowski, N. Boury-Es-
AviSE, J. C. 2000. Phylogeography: the History and Formation NAULT, J. p. Thorpe & A. M. Sole-Cava. 1999. Does cos-
of Species. Harvard University Press: Cambridge, Massa- mopolitanism result from overconservative systematics? A
chusetts. 447 pp. case study using the marine sponge Clioiulrilla niicula. Evo-
AviSE, J. C. & D. Walker. 1998. Pleistocene phylogeographic lution 53:1414-1422.
effectson avian populations and the speciation process. Pro- Knowlton, N. 1993. Sibling species in the sea. Annual Review
ceedings of the Royal Society, London Biological Sciences ofEcology and Systematics 24:189-216.
BuDD2,65A:.45R7,-K4.63G.. Johnson & D. C. Potts. 1994. Recognizing Lamarck, J. B. 1822. Histoire Naturelle des Animaux sans Ver-
tebres. Verdiere: Paris.
morphospecies in colonial reef corals: I. Landmark-based Lee, M. S. Y 1999. Molecular clock calibrations and metazoan
Collimnest,hoTd.s.M.P,alKe.obFiroalzoegry,2A0.:4R8.4-P5a0l5m.er, G. J. Vermeu & W. d39i1v.ergence dates. Journal of Molecular Evolution 49:385-
M. Brown 1996. Evolutionary history of northern hemi- Levinton, j. S. & C. M. Simon. 1980. A critique of the punc-
sphere Nucella (Gastropoda, Muricidae): molecules, ecolo-
tuated equilibria model and implications forthe detection of
Cookgey,, aA.ndHf.oss1i9ls1.5.EvTohleutigoenog5r0a:p2hi2c8a7l-2d3i0s4t.ribution of Purpura speciation in the fossil record. Systematic Zoology 29:130-
142.
Mlaaplialcluoslo(gL.i)c.alParStocIi:eItnyPoaflaLeoarncdtoicnw1a1te:r1s9.2-P2r0o9c.eedingsofthe Lindberg, D. R. & J. H. LiPPS. 1996. Reading the chronicle of
Dall,genWu.sHN.uce19l1l5a.inNhoatbeistiongntthheensopretchiweesstofcotahsetomfolAlmuesrciacnasaunbd- Jqaubaltoenrsnkair,yDt.emHp.erEartewirnoc&kyJs.hHo.reLfiapupnsas.(edPsp..).1E6v1o-l1u8t2ioinnaDr.y
adjacent regions. Proceedings ofthe United States National Paleobiology. University of Chicago Press: Chicago.
Museum 49:557-572. Marincovich, L. 1976. Late Pleistocene molluscan faunas from
Dall, W. H. 1921. Summary of the marine shell-bearing mol- upper terraces ofthe palos Verdes Hills, California. Natural
lusks of the northwest coast of America, from San Diego, History Museum of Los Angeles County Contributions in
California, to the Polar Sea, mostly contained in the collec- Sciences 281:1-28.
tion ofthe United StatesNational Museum, withillustrations Marko, P. B. 1998. Historical allopatry and the biogeography of
ofhitherto unfigured species. Smithsonian Institution United speciation in the prosobranch snail genusNucella. Evolution
States National Museum Bulletin, 112:1-217. 52:757-774.
Deshayes, G. p. 1839. Nouvellcs especes de mollusques. Revue Marko, R B. & J. B. C. Jackson. 2001. Patterns ofmorpholog-
Zoologique, par la Societe Cuvierienne pp. 356-361. ical diversity among Recent and fossil tropical American
p. B. Marko et al., 2003 Page 85
W
geminate bivalves in the family Arcidae. Journal of Pale- Roy, K.,J. Valentine, D. Jablonski & S. M. Kidwell. 1996.
ontology 75:590-606. Scales of climatic variability and time averaging in Pleis-
Marko, P. B. & G. J. Vermeij. 1999. Molecular phylogenetics tocene biotas: implications for ecology and evolution.
andtheevolutionoflabral spinesamongeasternPacificoce- Trends in Ecology and Evolution 11:458-463.
nebrine gastropods. Molecular Phylogenetics & Evolution Swofford, D. L. 2001. PAUP*: Phylogenetic Analysis Using
13:275-288. Parsimony (*and Other Methods). Version 4. Sinauer As-
Mastro, E., V. Chow & D. Hedgecock. 1982. Littohna scutu- sociates: Sunderland.
lata and Littohnaplena: sibling species status oftwo pros- Thorpe, JP. & A. M. Sole-Cava. 1994. The use of allozyme
obranchgastropodspeciesconfirmedbyelectrophoresis.The electrophoresis in invertebrate systematics. ZoologicaScrip-
Veliger 24:239-246. ta 23:3-18.
Mayr,E. 1942. Systematics andthe OriginofSpecies.Columbia Tryon, G. W. 1880. Manual of Conchology, Volume 2 (Muri-
University Press: New York. 334 pp. cinae, Purpurinae). Academy of Natural Sciences: Philadel-
McLevainse,dJe.d.H.,Nat1u9r7a8.l MHaisrtionreySMheulslesuomfSoofutLhoesrnAnCgaellifeosrnCioau.ntRye,- Valenphtiian.e,28J9. Wpp.. 1989. How good was the fossil record? Clues
Science Series 24:1-104. from the Californian Pleistocene. Paleobiology 15:83-94.
MiCHAUX, B. 1989. Morphological variation of species through Valentine, J. W. & D. Jablonski. 1983. Speciation in the shal-
MiDDtEiNmDeO.RBFiFo,logAi.caTl.Jo1u8r4n9a.loBfeitthreaLgeinnzeuaneiSnoecrieMtayl3a8c:o2z3o9o-l2o5g6i.a l2o0w1-s2e2a6: iGneRn.erWa.lSpiamtst,erJn.sH.anPdribcieo&geoPgrEa.pSh.icWhcaolnlteroyls(.edsP.p)..
NMeuir,psPRshMipeosyet.s.,cesirBi&esiPc.sboaulGWroon.g.fg..-ilc1HK2ai9.al4m7i8p7LsB.eieutp.rlCpllo(.ei1lAtc9icih7smn9eeal.nle1ai5AMd5kaa:atau1eshd9)tee3rmmo-dadi2iti0esig6cic.odtavealelrirsmeWdoissdpbse.eylnnosefvclo.her:catfasrttoesupnidh:byoliriSnent-gg. ValenCEAEinvtcocooimaRllpnd.uooeetgs,Eimii.ocitJnac.iR,loiWPcnTrkCaielolmsem&sefm:vsuaarNnD&ni.iedattwDiJiS.aeopYnbsaSolc:craoehtkn:l.HsmuikTtsaihet.neroyri(E1ec9mtda9isel3.mr).eg.aenFsSnodcpsacelsecGeiiselo.eofsgcPaorpDma.iBmpviuhe3onris4sicp1ith-tiePy3ere4seri9:,-n
spectives. University ofChicago Press: Chicago.
cgeeneedtiincgsvaorifattihoen Nianttieornmasl oAfcraedstermicytioonfeSncdioennuccelseasUeSs.APr76o:- Vanatta, E. G. 1910. Purpura crispata and saxicola. The Nau-
tilus 24:37-38.
5269-5273. Vedder, J. G. & R. M. NoRRis. 1963. Geology ofSan Nicholas
Oldroyd, L S. 1927. The marine shells of the West Coast of Island, California. U.S. Geological Survey Professional Pa-
North America. Stanford University PublicationsGeological
per 369:1-65.
Series 2:230-236. Vermeij, G. J. 1978. Biogeography and Adaptation. Harvard
Palmer, A. R. 1985b. Quantum changes in gastropod shell mor- University Press: Cambridge. Massachusetts 416 pp.
Palmpehro,loA.gyR.n,eeS.dDn.otGraeyflreoctns&pecDi.atiSo.n.WoEovdorluutfifo.n 13999:06.99R-e7p0r5o.- Vermeciaju,sesG.ofJ.ex1t9i8n9c.tioGne:ogtrhaephcaisceroefstrtihceticoonldasnoartghueirdneotcoeatnhse
ductive,morphological, andgeneticevidencefortwocryptic during the Neogene. Paleobiology 15:335-356.
species ofnortheastern PacificNucella. The Veliger33:325- Vermeij, G. J., A. R. Palmer & D. R. Lindberg. 1990. Range
338. limits and dispersal of molluscs in the Aleutian islands,
Reeve, L. A. 1845. Conchologia Iconica: or, Illustratuions ofthe Alaska. The Veliger 33:346-54.
Shells ofMolluscous Animals. Volume 3. Monographofthe Yang, Z. 1994. Maximum likelihood phylogenetic estimation
Genus Purpura. London, Reeve, Brothers, King, William from DNA sequences with variable rates oversites: approx-
Street, Strand. imate methods. Journal ofMolecularEvolution 39:306-314.
Reid, D. G. 1990. Trans-Arctic migration and speciationinduced YoDER, A. D., & Z. Yang. 2000. Estimation ofprimate specia-
by climatic change: the biogeography ofLittorina (Mollus- tion dates using local molecular clocks. Molecular Biology
ca: Gastropoda). Bulletin ofMarine Science 47:35-49. & Evolution 17:1081-1090.