Population structure and phylogeography of an acorn barnacle with induced defense and its gastropod predator in the Gulf of California

Using sequence variation in the mitochondrial cytochrome oxidase I locus, we estimated the population structure and phylogeography of the intertidal acorn barnacle, Chthamalus anisopoma, and its gastropod predator, Mexacanthina lugubris angelica. Both are endemic to the Gulf of California, being derived from taxa on the Pacific coast of the Baja peninsula, and both exhibit phenotypic plasticity for traits affecting their coevolutionary interactions. Consistent with expectations based on differences in dispersal, C. anisopoma populations generally lack geographic structure, while those of M. l. angelica are more strongly structured. However, the variable degree of differentiation in both species suggests that the extent of reciprocal selection and local adaptation in the species will vary geographically, a result consistent with the concept of a geographic mosaic of coevolution. The pattern of variation in C. anisopoma shows clear evidence of recent spatial expansion, possibly due to increased habitat availability following the last glacial maximum. Phylogeographic analyses suggest that M. l. angelica diversified into three distinct clades after the colonization of the Gulf. Overall, our results illustrate how dispersal potential, geological and climatic events, and recent population growth have impacted the pattern of sequence variation in the two species.     

Function of the shell spine in the predaceous rocky intertidal snail Acanthina spirata (Prosobranchia: Muricacea)

Feeding observations revealed that Acanthina spirata (Blainville, 1832) uses the shell spine in a ramming and prying motion, resulting in the fracturing and/or forcing open of opercular plates in the barnacles Balanus glandula (Darwin, 1854) and Chthamalus fissus (Darwin, 1854). Attacking barnacles by using the shell spine may represent a second widespread feeding mechanism (in addition to drilling) in muricacean gastropods. Specialization of the shell spine for attacking barnacles is advantageous over drilling within the context of an optimal foraging theory. Rockey intertidal field and laboratory experiments at Palos Verdes and Los Angeles, California, respectively, in 1981–1982 revealed, that snails with a shell spine have lower handling times and feed at a greater rate than spineless snails which drill their prey. Spine penetration of prey as opposed to drilling takes considerably less time than a tidal cycle. This is expected to increase the success rate for completion of feeding, since during tidal flux snails risk being dislodged. Plasticity in attack mechanisms allows A. spirata with broken spines to penetrate prey by drilling while undergoing spine repair. Differences exist in spine-feeding by A. spirata on B. glandula and C. fissus. The attack process takes more than twice as long when snails attack B. glandula versus C. fissus. However, there is no difference in the mean number of spine thrusts required to penetrate the opercular plates of the two species. When feeding on the larger barnacle B. glandula, A. spirata ingests significantly greater dry weight per unit handling time than with C. fissus.     

Phenotypic variation in shell form in the intertidal acorn barnacle Chthamalus montagui: distribution,response to predators and life history trade-offs

The acorn barnacle Chthamalus montagui can present strong variation in shell morphology, ranging from flat conic to a highly bent form, caused by a substantial overgrowth of the rostrum plate. Shell shape distribution was investigated between January and May 2004 from geographical to microhabitat spatial scales along the western coast of Britain. Populations studied in the north (Scotland and Isle of Man) showed a higher degree of shell variation compared to those in the south (Wales and south-west England). In the north, C. montagui living at lower tidal levels and in proximity to the predatory dogwhelk, Nucella lapillus, were more bent in profile. Laboratory experiments were conducted to examine behavioural responses, and vulnerability of bent and conic barnacles to predation by N. lapillus. Dogwhelks did not attack one morphotype more than the other, but only 15 % of attacks on bent forms were successful compared to 75 % in conic forms. Dogwhelk effluent reduced the time spent feeding by C. montagui (11 %), but there was no significant difference between conic and bent forms. Examination of barnacle morphology indicated a trade-off in investment in shell structure and feeding appendages associated with being bent, but none with egg or somatic tissue mass. These results are consistent with C. montagui showing an induced defence comparable to that found in its congeners Chthamalus anisopoma and Chthamalus fissus on the Pacific coast of North America, but further work to demonstrate inducibility is required.     

Sibling species in interstitial flatworms: a case study using<Emphasis Type="Italic"> Monocelis lineata</Emphasis> (Proseriata: Monocelididae)

The genetic relationships between morphologically indistinguishable marine and brackish-water populations of Monocelis lineata (O.F. Müller, 1774) (Proseriata: Monocelididae) were analysed by means of allozyme electrophoresis. Fifteen samples of M. lineata (13 from the Mediterranean and two from the Atlantic) from coastal marine and brackish-water habitats were examined for variation at 18 loci. Eleven loci were polymorphic in at least one population of M. lineata. Low levels of within-population genetic variability were found, with average observed and expected heterozygosity values ranging from H_o=0.015±0.015 to 0.113±0.044, and from H_e=0.028±0.028 to 0.138±0.054, respectively. The occurrence of a number of private alleles indicated a marked genetic divergence among populations of M. lineata, with Rogers genetic distances ranging from D_R=0.003 to 0.676 and a highly significant F_ST value (0.918±0.012, P<0.001). UPGMA (unweighted pair-group method using arithmetic average) cluster analysis and multidimensional scaling showed a clear genetic divergence between marine and brackish-water populations. Moreover, Atlantic and Mediterranean populations were sharply separated. Our results suggest that M. lineata is a complex of sibling species.Communicated by R. Cattaneo-Vietti, Genova     

Genetic evidence for the cryptic species pair, <Emphasis Type="Italic">Lottia digitalis </Emphasis>and <Emphasis Type="Italic">Lottia austrodigitalis</Emphasis> and microhabitat partitioning in sympatry

It has been proposed that the common West Coast limpet, Lottia digitalis, is actually the northern counterpart of a cryptic species duo including, Lottia austrodigitalis. Allele frequency differences between southern and northern populations at two polymorphic enzyme loci provided the basis for this claim. Due to lack of further evidence, L. austrodigitalis is still largely unrecognized in the literature. Seven additional enzyme loci were examined from populations in proposed zones of allopatry and sympatry to determine the existence of L. austrodigitalis as a sibling species to L. digitalis. Significant allele frequency differences were found at five enzyme loci between populations in Laguna Beach, southern California, and Bodega Bay, northern California; strongly supporting the existence of separate species. Both species exhibit two microhabitat morphotypes, a gooseneck barnacle morph in the mid-intertidal zone and a rock morph in the high-intertidal zone. In sympatry, L. austrodigitalis was more abundant higher in the intertidal on rocks, whereas L. digitalis was more abundant lower in the intertidal on barnacles. This finding supports earlier claims of microhabitat partitioning in this sibling species pair. In addition to this finding, the transition zone between the species was found to have shifted substantially northward in only two decades, from Monterey Peninsula, CA to near Pigeon Point, CA, where L. digitalis previously dominated.     

Population and species diversity fluctuations in a rocky intertidal community relative to severe aerial exposure and sediment burial

From a series of 10 quarterly assessment between October 1975 and May 1978 (inclusive), fluctuations in abundance were determined for macroinvertebrates and macrophytes of a rocky intertidal community on Santa Cruz Island, California, USA. During afternoon low tides in late fall and winter of the first 2 yr of study, organisms of the upper and middle intertidal zones were subjected to prolonged aerial exposure. Many species there tolerated this exposure, but die-backs occurred for a barnacle (Chthamalus fissus/C. dalli) and several algae (Endocladia muricata, Pelvetia fastigiata f. gracilis, Corallina officinalis var. chilensis, Corallina vancouveriensis, Cylindrocarpus rugosus and Codium fragile). These die-backs were succeeded by blooms of Ulva californica and Porphyra perforata. In the upper and middle intertidal zones, the major cover organisms that could tolerate prolonged aerial exposure were disproportionately prevalent and appeared to be maintained by the periodic repression of species intolerant to such exposure. In February 1978, heavy rainfall caused sediment inundation of the middle and lower intertidal zones. This event was followed by declines in abundance of a barnacle (Tetraclita rubescens) and several algae (Pelvetia fastigiata f. gracilis and corallina spp.). Shannon-Wiener H species diversity fluctuated from a high in October to a low the following May during both 1975–1976 and 1976–1977 in conjunction with the period of increased daytime aerial exposure in late fall and winter. A further decline in diversity following sediment inundation in February 1978 contributed to a long-term trend of declining H species diversity (3.06 in October 1975 to 1.87 in May 1978). We hypothesize that predictable late fall to winter aerial exposure stresses, in combination with a random physical disturbance (sediment burial), exceeded an optimal intermediate level of disturbance predicted for maximal species diversity.     

Effects of settlement density on spatial arrangement in four intertidal barnacles

Balanus amphitrite was studied in an estuary (Halifax River) in central Florida from October to November 1990, while three other barnacle species were studied on the central coast (Monterey Bay) of California from April 1988 to July 1989. Mean nearest-neighbor distances indicated that in the majority of cases the spatial arrangement of settlers was random for three different balanomorph barnacles-B. amphitrite, B. glandula, and Chthamalus dalli. In Pollicipes polymerus, a lepidomorph species, strong aggregation among settlers was almost always observed. In the three balanomorph species there was no apparent relationship between settler density and the degree of aggregation. In P. polymerus there was a significant positive correlation between settler density and the degree of aggregation. Morphological differences between balanomorph and lepidomorph barnacles may influence the evolution of settlement behavior.     

Genetic population structure of the recently introduced Asian clam,Potamocorbula amurensis,in San Francisco Bay

The genetic population structure of the recently introduced Asian clam, Potamocorbula amurensis, in San Francisco Bay was described using starch gel electrophoresis at eight presumptive loci. Specimens were taken from five environmentally distinct sites located throughout the bay. The population maintains a high degree of genetic variation, with a mean heterozygosity of 0.295, a mean polymorphism of 0.75, and an average of 3.70 alleles per locus. The population is genetically homogeneous, as evidenced from genetic distance values and F-statistics. However, heterogeneity of populations was indicated from a contingency chi-square test. Significant deviations from Hardy-Weinberg equilibrium and heterozygote deficiencies were found at the Lap-1 locus for all populations and at the Lap-2 locus for a single population. High levels of variability could represent a universal characteristic of invading species, the levels of variability in the source population(s), and/or the dynamics of the introduction. Lack of differentiation between subpopulations may be due to the immaturity of the San Francisco Bay population, the general purpose phenotype genetic strategy of the species, high rates of gene flow in the population, and/or the selective neutrality of the loci investigated.     

Geographical subdivision,demographic history and gene flow in two sympatric species of intertidal snails, <Emphasis Type="Italic">Nerita scabricosta</Emphasis> and <Emphasis Type="Italic">Nerita funiculata</Emphasis>, from the tropical eastern Pacific

The patchy distribution of rocky intertidal communities in the tropical eastern Pacific (TEP) may impose severe constraints on the genetic connectivity among populations of marine invertebrates associated with this habitat. In this study, we analyzed a portion of the mitochondrial cytochrome c oxidase subunit I (COI) gene in two sympatric species of marine snails, Nerita scabricosta and Nerita funiculata, common inhabitants of the rocky intertidal from the Gulf of California (Sea of Cortez) and outer Pacific coast of the southern Baja California (Baja) peninsula to northern South America, to assess genetic connectivity among populations of each species. One of our aims was to determine whether the morphological, behavioral, and ecological differences observed among populations of both species throughout their range in the TEP corresponded to population genetic differences. In addition, we were interested in elucidating the demographic history of both species. We found no evidence of genetic structure throughout the Gulf of California and outer coast of the Baja peninsula region for either species. Comparisons between Gulf of California/Baja and Panama populations, however, showed significant genetic differentiation for N. scabricosta, but not for N. funiculata. The genetic differences between Mexican and Panamanian populations of N. scabricosta were consistent with previously reported ecological and behavioral differences for this species between these two distant regions. However, previously reported size differences between northern and central/southern Gulf of California individuals of N. scabricosta do not correspond with our findings of genetic connectivity among these populations. Results from neutrality tests (Tajima’s D and Fu’s F _S), the mismatch distribution, and Bayesian skyline analyses suggested that both species have experienced dramatic population expansions dating to the Pleistocene.     

Cryptic isolation of Gulf of California shovelnose guitarfish evidenced by mitochondrial DNA

The shovelnose guitarfish Rhinobatos productus is an evolutionarily, ecologically, and economically important ray, with a continuous distribution from San Francisco, California (USA), to Mazatlan, Sinaloa, and in the Gulf of California (Mexico). Regional studies have revealed morphometric differences between shovelnose from the Gulf of California and the Pacific coast of Baja California, which may result from phenotypic plasticity in the presence of high levels of gene flow or from a degree of genetic differentiation in the presence of cryptic isolation within a continuous distribution. We used PCR-RFLP of the mitochondrial control region to assess the degree of genetic differentiation between Gulf of California and Pacific shovelnose guitarfish. We found very high levels of molecular diversity (averages: h=0.77, =1.19%), which may be associated with historically large and stable populations, as well as very significant levels of genetic differentiation between gulf and Pacific samples (²=64, P<0.0001; _ST=0.63, P<0.0001, mean nucleotide divergence d=2.47%). We found a deep phylogeographic break between haplotypes from the gulf and the Pacific, which may suggest the existence of cryptic species but clearly indicates more than one evolutionarily significant unit of R. productus. Our results show a pattern of genetic structure and levels of differentiation consistent with the geological history of the region. Furthermore, these findings have wide-ranging implications for the management and conservation of cartilaginous fish in Mexico, as they reveal the existence of biological diversity that will go unnoticed without the genetic scrutiny of intraspecific variation and that is highly relevant for much needed management and conservation efforts.Communicated by P.W. Sammarco, Chauvin     

Allozyme variation in populations of the dog-whelkNucella lapillus (Prosobranchia: Muricacea) from the South West peninsula of England

Four populations of the predatory gastropodNucella lapillus were sampled at sites around the South West Peninsula of England in 1986, and analysed for allozyme variation at 18 enzyme loci. Two of these loci, Gpd-1 andHk-1, exhibited sex-specific phenotypes. An absolute locus association was observed between two other loci,Mdh-1 andEst-3. This association was only found at one site (Prawle), and it is suggested that the presence of chromosomal polymorphisms could explain this finding. As a measure of overall similarity, Nei's genetic identity statistic,I, was calculated; the mean for all populations was 0.989, with values ranging from 0.981 to 0.997. Although similar on this gross level, considerable interpopulation variation was evident. Observed mean heterozygosity (per locus) ranged from 0.043 to 0.104 (mean 0.074). Populations differed also in the loci at which significant heterozygote deficits were seen (of the seven deficits recorded only those at thePep-1 locus were consistent across sites) and in the presence of rare alleles undetected elsewhere. The variation observed showed no correlation to shell morphology or geographical distance and confirmed the conclusion that species of the genusNucella show considerable disjunct variation.     

Does displacement of spawning time occur in the sibling species Cerastoderma edule and C. lamarcki?

The spawning cycles of the sibling species Cerastoderma edule (L.) and C. lamarcki (Reeve) were studied in allopatric and sympatric Danish populations from 1978–1980. The results do not support earlier findings of reproductive character displacement in sympatric populations of the two species. New records of hybrid formation and intermediate forms are presented and discussed.     

A genetic analysis of the pea crabs (Decapoda: Pinnotheridae) of New Zealand

Seven populations of the pea crabPinnotheres atrinicola Page were sampled from around the North Island of New Zealand from February to October 1987, and individuals were scored at 23 presumptive enzymatic loci. For a brachyuran crab,P. atrinicola revealed high levels of polymorphism and heterozygosity. Of the loci scored, phosphoglucose isomerase (Gpi) and phosphoglucomutase (Pgm) were distinguished by high variability ( =0.602 and 0.526, respectively). A clinal variation in electromorph frequency was evident at several loci, and atGpi in particular. Statistical analyses revealed that, despite relatively small genetic distance separation, a high degree of structuring was present between the geographic populations. The degree of population subdivision observed in this study is atypical of brachyuran crabs. It is suggested that the genetic differentiation observed between pea crab populations is maintained by life-history attributes and current movements which restrict gene flow between populations and, to some extent, by random genetic drift.Publication No. 41 from the Evolutionary Genetics Laboratory, University of Auckland     

Spatio-temporal patterns in the genetic structure of recently settled blue mussels (<Emphasis Type="Italic">Mytilus</Emphasis> spp.) across a hybrid zone

Previous studies of a hybrid zone between the mussels Mytilus edulis Linnaeus and M. galloprovincialis Lamarck have not resolved the relative importance of the genetic composition of settling larval cohorts versus post-settlement selection in determining the distribution of the parental species and their hybrids. In the present study, recently settled mussels (spat) were collected from 20 sites in southwest England throughout the summer and fall (May–October) in 1998 and 1999. This study investigated the spatio-temporal patterns of settlement and genetics of mussel spat by genetically identifying M. edulis, M. galloprovincialis and their hybrids using the diagnostic PCR marker Glu-5. Settlement was observed earlier in populations of M. edulis than in populations of M. galloprovincialis. Settlement occurred in hybrid populations at times intermediate to and overlapping with both of the parental populations. Temporal genetic variation within years was rare at most sites, while there was some variation between the two years. Spatial genetic variation, however, was common among spat settling within the hybrid populations and matched that observed in small, sub-adults at the same sites. No consistent directional changes in allele frequency were observed over the course of several weeks after settlement. These data suggest that the observed spatial variation in the adult populations is the result of spatial variation in settling larval cohorts and not of either temporal genetic variation or of selection soon after settlement.Communicated by J.P. Grassle, New Brunswick     

Genetic consequences of long larval life in the starfish Linckia laevigata (Echinodermata: Asteroidea) on the Great Barrier Reef

Gene flow between populations of the asteroid Linckia laevigata (Linnaeus) was investigated by examining over 1000 individuals collected from ten reefs throughout the Great Barrier Reef (GBR), Australia, for genetic variation at seven polymorphic enzyme loci. Despite geographic separations in excess of 1000 km, Nei's unbiased genetic distance (0 to 0.003) and standardised genetic variation between populations (F _ST) values (mean 0.0011) were small and not significant. Genetic homogeneity among L. laevigata populations is consistent with the long-distance dispersal capability of its 28 d planktonic larval phase, and is greater than that observed for other asteroid species, including another high-dispersal species, Acanthaster planci, which has a 14 d larval phase. Variation within populations was also higher than previously recorded for asteroids (mean heterozygosity=0.384; number of alleles per locus ranged from 5.1 to 6.0 in each population). Among asteroids, dispersal ability is positively correlated with gene flow and levels of variation, and negatively correlated with levels of differentiation.     

Genetic affinities of the bivalve Macoma balthica from the Pacific coast of North America: evidence for recent introduction and historical distribution

The tellinid bivalve Macoma balthica (L.) has an extensive geographic range that reaches from temperate to arctic coastal waters in the North Atlantic and North Pacific oceans. Recent studies have indicated that eastern and western North Atlantic populations are morphologically and genetically different from one another, and that they may have diverged as sibling species. To determine the genetic relationship between M. balthica from the Pacific and Atlantic coasts of North America, populations from each coast were examined at 11 enzyme loci using standard starch gel electrophoresis. Allele frequency data indicate that M. balthica populations from San Francisco Bay, California appear more closely related to western North Atlantic populations than to populations from Oregon. We suggest that San Francisco Bay populations were introduced relatively recently from western North Atlantic populations. The Oregon populations are probably a natural extension of northern populations that occur along Northern Asia and in the eastern North Atlantic.     

Allozyme variation in global populations of striped mullet, Mugil cephalus (Pisces: Mugilidae)

The striped mullet, Mugil cephalus Linnaeus, 1758, is one of the few species of marine shore fish with a worldwide circumtropical distribution. Because of this distribution and the dependency of M. cephalus on coastal waters during various phases of its life cycle, as well as nearshore living habits, questions have been raised regarding levels of genetic divergence and gene flow among transoceanic populations. To cast more light on this, allozyme variation at 27 presumptive gene loci was investigated in ten globally diverse populations. The observed heterozygosity ranged from 0.018 (Hawaii) to 0.081 (Florida), averaging 0.050. The proportion of polymorphic loci showed a similar trend. Several populations were characterised by fixed allelic differences. Estimated gene diversities were very high, the allele frequency variation among populations was found to be 68%; genetic distances reached 0.242, with an average of 0.117. Estimated rates of gene flow were high among Mediterranean populations (Nm = 7.26), and between Mediterranean and East Atlantic populations (Nm= 2.86), but extremely low between non-contiguous populations within the Indian, Pacific and Atlantic Oceans, where Nm ranged from 0.03 to 0.05. Received: 7 April 1997 / Accepted: 4 February 1998     

Conservation genetics of <Emphasis Type="Italic">Lumnitzera littorea</Emphasis> (Combretaceae), an endangered mangrove,from the Indo-West Pacific

Mangrove forests, with their ecological significance and economic benefits, are vital inter-tidal wetland ecosystems. Lumnitzera littorea (Combreataceae) is a non-viviparous mangrove distributed in tropical Asia and North Australia. Due to natural and human impacts, populations of this species have been isolated, fragmented, and highly disturbed. In China, L. littorea is an endangered species, restricted to small regions of Hainan Island. The genetic composition of five populations of this species from the Indo-West Pacific (South China, Malay Peninsula, Sri Lanka, North Australia) was assessed using inter simple sequence repeat (ISSR) makers. At the species level, expected mean heterozygosity (He) was 0.240 with 75.6% of loci polymorphic (P). However, genetic variation was much lower at the population level (P = 37.1%, He = 0.118). A high coefficient of gene differentiation (Gst = 0.515) and low level of gene flow (Nm = 0.470) indicated significant genetic differentiation among populations. AMOVA also indicated that more than half the total variation (58.4%) was partitioned among populations. The high degree of differentiation observed among populations emphasizes the need for appropriate conservation measures that incorporate additional populations into protected areas, and achieve the restoration of separate, degraded populations.     

Genetic structure of<Emphasis Type="Italic"> Linckia laevigata</Emphasis> and<Emphasis Type="Italic"> Tridacna crocea</Emphasis> populations in the Palawan shelf and shoal reefs

Allozyme variation of 10 populations of Linckia laevigata at 8 polymorphic loci and 13 populations of Tridacna crocea at 6 polymorphic loci were analyzed to compare genetic variability and genetic affinities among reefs in Palawan, Philippines. Two to five populations were sampled from each of four regions: the shelf reefs in (1) northern Palawan and (2) southern Palawan and the offshore reefs in (3) the Kalayaan island group (KIG) in the South China Sea and (4) the Tubbataha shoals in the Sulu Sea. Heterozygosity was highest in populations of L. laevigata from the south shelf of Palawan and populations of T. crocea from the Tubbataha shoals of the Sulu Sea. The lowest heterozygosity estimates were from the reefs of the KIG in the South China Sea, for both species. Overall F _ST values for both species were significant, with an estimated average number of effective migrants per generation (N _EM) of 4.85 (~5 individuals) for L. laevigata and 3.54 (~4 individuals) for T. crocea. Within-region comparisons showed N_EM ranging from 6.29 to 92.34 for L. laevigata and from 3.40 to 6.30 for T. crocea. The higher gene flow among L. laevigata populations relative to T. crocea is consistent with the greater dispersal potential of the former species. Finer scale genetic structuring was evident in T. crocea populations. For both species, the Tubbataha reefs in the Sulu Sea have higher genetic affinity with the populations from the southern shelf of Palawan, while the reefs in the KIG had higher affinity with the northern Palawan shelf reefs. The north and south shelf populations have the least genetic affinity. Genetic patchiness among reefs within regions suggests the importance of small-scale physical factors that affect recruitment success in structuring populations in small island and shoal reef systems in Palawan.     

Population genetics of the family ostreidae. II. Interspecific studies of the genera Crassostrea and Saccostrea

The estimated levels of genetic variation are reported for 6 Crassostrea and 3 Saccostrea species. The estimates are based on examination of 25 to 34 genetic loci. The average heterozygosities ranged from 6 to 22% for the Crassostrea species and from 17 to 19% for the Saccostrea species. A new sibling species (S. manilai) from the Philippines has been identified by means of protein electrophoresis. The genetic similarity and distance between species has been computed for each genus. Also, a pairwise comparison of loci and a dendrogram of the phylogenetic relationship of species has been constructed from the two genera. Some of the taxonomic levels during oyster speciation have been computed from the data of the electrophoretic study of the two lineages. The possibilities of oyster superspecies (e. g. C. gigas, C. virginica and S. cucullata) are discussed based on our population genetic study.