The Journal of Heredity 2002:93(6)
© 2002 The American Genetic Association 93:432-438
Brief Communication |
Disparity in Population Differentiation of Sex-Linked and Autosomal Variation in Sibling Species of the Jaera albifrons (Isopoda) Complex
From the Department of Evolutionary Biology, University of Copenhagen, Universitetsparken 15, DK-2100 Copenhagen Ø, Denmark.
Address correspondence to Hans R. Siegismund at the address above, or e-mail: HSiegismund{at}ZI.KU.DK.
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Abstract |
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The genetic variation at four enzyme loci is described for 22 populations of three Jaera species—J. albifrons, J. ischiosetosa, and J. praehirsuta—in the J. albifrons complex (Crustacea, Isopoda) in Denmark. The variation at three of the loci is similar, with the allele frequency spectra close to each other in all three species. An evolutionary tree based on the variation at these three loci revealed that the populations from the different species are completely intermixed in the tree. This was supported by hierarchical F-statistics where the between-species component was zero. At a fourth locus, Gpi (glucose phosphate isomerase), the species differ substantially. This locus is sex linked in J. ischiosetosa, but in the two other species, J. albifrons and J. praehirsuta, it is either found on autosomes or is sex linked with a high recombination rate between the locus and the centromere. An evolutionary tree for this locus partitions the populations into separate groups and a hierarchical F-statistic has a between-species component of about 50%. The results are attributed to introgression with a higher rate for autosomes than for sex chromosomes.
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Introduction |
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The sibling species in the Jaera albifrons complex are common members of the shallow-water fauna on the coast of the North Atlantic. In total, there are five species: J. albifrons Leach, J. ischiosetosa Forsman, J. praehirsuta Forsman, J. forsmanii Bouquet, and J. posthirsuta Forsman (Solignac 1981). The species are closely related but can be distinguished by the secondary sexual characters of the males (the setation on the pereopods) (Naylor 1972). Females are morphologically very similar, making it practically impossible to distinguish individuals to species. The species were initially described as races by Forsman (1944, 1949), but were elevated to species level by Bocquet (1953), who considered them as members of the superspecies J. marina and gave them trinomial names. The trinomial naming system has been abandoned in favor of the usual binomial naming convention (Naylor 1972). The distribution ranges commonly overlap, either as narrow contact zones (Bocquet 1953) or as broader sympatric distributions of the species (Jones and Naylor 1971; Naylor and Haathela 1966, 1967). The species are closely related, which is reflected in a geographically widespread hybridization among them (Carvalho 1989; Solignac 1981).
In Jaera, like many other isopods with chromosomal sex determination, females are heterogametic (ZW) whereas males are homogametic (ZZ) (Shuster and Levy 1999). Staiger and Bocquet (1954) showed that females in Jaera have two W chromosomes; that is, they are ZW1W2. Siegismund and Christensen (1992) found that the enzyme locus for glucose phosphate isomerase (Gpi) is sex linked in Danish populations of J. ischiosetosa, where it is carried on the Z as well as on one of the W chromosomes. In two other Danish Jaera species, this locus is found on autosomes. In J. ischiosetosa, the Gpi locus has probably been carried on an autosome that has fused with the Z chromosome. One arm of the neo-Z chromosome consists of the previous autosome. Therefore males carry their two copies of the Gpi locus on each of their neo-Z chromosomes, whereas females carry a copy on the neo-Z and on the neo-W chromosome. The present study focuses on how the sibling species in the J. albifrons complex are differentiated at this sex-linked locus and at three autosomal loci at the intra- and interspecific level.
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Materials and Methods |
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Sampling
The animals were collected at 21 locations in Denmark in 1988 and 1989 (Figure 1). The shortest distance between two locations was about 3 km for locations 4 and 10. Location 4 was at the shore north to a cove, whereas location 10 was at the inner part of the cove. Sampling took place by collecting stones at the shore at a depth of up to 0.5 m and removing animals on the underside with a brush. At the sampling stations, a stretch of up to 500 m was covered. The animals were brought alive to the laboratory, where the specific status of males was determined with the key in Naylor (1972). Each individual was placed in 5–10 µl of buffer in a tube and stored at -80°C.
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Electrophoresis
Enzyme electrophoresis was carried out on 5% acrylamide gels with two buffer systems: a histidine buffer at pH 6 (tray: 0.01 M histidine monohydrochloride; gel: tray buffer diluted once) and a tris/citrate buffer at pH 7 (tray: 0.45 M tris, 0.13 M citrate; gel: tray buffer diluted 9:500). Both gels were run at 20 V/cm for 1.5 h.
A preliminary survey with about 25 enzymes resulted in 11 usable systems covering 12 loci. Of these, eight were monomorphic for the same alleles in a comparison of the J. albifrons population from location 2 with the J. ischiosetosa population from location 7, and these have not been used.
The gels were sliced into two and stained for the following enzymes: glucose phosphate isomerase (E.C. 5.3.1.11), phosphoglucose mutase (E.C. 2.7.5.1) (the histidine gels), mannose phosphate isomerase (E.C. 5.3.1.8), and malate dehydrogenase (E.C. 1.1.1.37) (the tris/citrate gels). The recipes were slightly modified versions of those in Harris and Hopkinson (1976). The staining for malate dehydrogenase revealed two stained zones, interpreted as the variation coded by two different loci. The locus coding for the fastest moving allozyme revealed a locus that was polymorphic in all populations. This locus is named Mdh in the present work. The other locus showed almost no variation. Alleles were named by their relative mobility to the most common allele, which was given the value 100.
Statistical Analysis
The variation at the four loci Gpi, Mdh, Mpi, and Pgm in J. albifrons and J. praehirsuta agree with the expected genotypic distributions for loci on autosomal chromosomes in diploid organisms. The same is the case for the Mdh, Mpi, and Pgm loci in J. ischiosetosa, whereas the Gpi locus in this species is sex linked (Siegismund and Christensen 1992). Guo and Thompson's (1992) Monte Carlo permutation test was used to compare the genotypic distributions at the autosomal loci to Hardy–Weinberg expectations. One thousand permutations were used in each test. For each permutation, the probability of the permutated genotypic distribution was estimated. The significance level was found as the frequency of permutated values equal to or larger than the observed value.
The Gpi locus in J. ischiosetosa is sex linked and is carried on the Z and one of the W sex chromosomes. This makes the estimation of allele frequencies difficult. In a population with variation on both sex chromosomes, one does not know which sex chromosome carries a specific allele in a heterozygote of the heterogametic sex. Therefore the allele frequencies were estimated and the data were analyzed with the procedures of Siegismund and Christensen (1992). Let zi and wi be the frequency of allele i at the Gpi locus on the Z and W chromosome, respectively. With random union of gametes, the expected genotypic proportions in males are
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In J. albifrons and J. praehirsuta, the variation at the Gpi locus was analyzed by testing for homogeneity of the genotypic distributions between sexes (Fisher's exact test in the procedure FREQ of SAS [1990]) and then testing for Hardy–Weinberg proportions of the sums in the same way as described above. The Bonferroni procedure was used to estimate tablewide levels of significance (Holm 1979).
The population structure for the two species with more than two populations (J. albifrons and J. ischiosetosa) was described with Wright's F-statistics according to Weir and Cockerham (1984). Deviations from Hardy–Weinberg proportions within populations were measured by the component FIS. The differentiation between populations within species (FSP) and the differentiation between species (FPT) was quantified by partitioning the total genetic differentiation (FIT) into three hierarchies, FIS, FSP, and FPT. The four F-statistics are related through
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The phylogenetic relationships among the populations were described with a tree estimated under the assumption that the populations solely diverge from each other because of genetic drift (Felsenstein 1973, 1981). The tree was estimated with the program CONTML from the package PHYLIP, version 3.5 (Felsenstein 1993).
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Results |
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It was rare to find a completely allopatric population of any of the Jaera species. Of the 21 sampled locations, only four contained a single species (of males) (Table 1). At the remaining 17 locations, two or three species were found to be sympatric. (No attempt was made to keep animals collected from a single stone separate, thus any segregation of the species on a smaller scale could not be detected.) Sympatric populations of all three species were rare and were only observed at three locations. In the sympatric populations, usually one species dominated, whereas the other species constituted less than 10% of the individuals, except for two cases, locations 11 and 21. Usually the frequency of the rarer species was on the order of a few percent.
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Genotypic Distributions
The data will be presented in two parts: first, for the variation at the Gpi locus, which differs in inheritance among the species, and second, for the loci where the observed variation agrees with the expected distributions for autosomally inherited variation in all species. Data from females are only included for the Gpi locus and are only used to illustrate the sex linkage of this locus. Since it has not been possible to determine the specific status of females, this has possibly included some bias in the genotypic proportions among them. At a single location, 11, this is expected to have a relatively large effect, since the frequencies of the two species found at this location—judged from the males (Table 1)—are 70% and 30%, respectively. At the other locations, the bias is probably much lower. One of the purposes of the present work was to study the divergence between the species. Therefore the population structure and the phylogenetic trees will be described with variations in males only.
At the Gpi locus, three common alleles (112, 107, 100) were found in both J. albifrons and J. praehirsuta (Table 2). Seventeen individuals with alleles that were rare in all Jaera species were excluded in J. albifrons. The frequencies of these alleles were less than 0.01. Males and females did not differ in this respect.
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Except for location 1, tests for homogeneity of genotypic distributions among sexes were accepted at the 5% significance level. Applying the Bonferroni correction renders the significant value for location 1 nonsignificant on a tablewide level. No test for homogeneity among sexes was carried out for population 11, since the sample from this location mostly consisted of J. ischiosetosa (Table 1).
Except for the sample from location 1, the genotypic distributions at the Gpi locus agreed with expected Hardy–Weinberg proportions at an autosomal locus. The genotypic distribution at location 1 was significant because of an excess of heterozygotes, with the largest contribution from females.
Table 3 presents the genotypic distribution at the Gpi locus for both sexes in J. ischiosetosa. Only the genotypes for the two common alleles (112, 100) are included. Individuals carrying rare alleles have been excluded; they consisted of 24 females and 7 males. Most of the excluded females (18) and males (6) carried allele 107, which was common in the two other species. (The exclusion of these individuals might distort the estimation of allele frequencies, but only in a minor way, since the rare alleles had frequencies of less than 0.01.)
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The Gpi locus is carried by the Z and one of the W chromosomes in J. ischiosetosa. This results in genotypic distributions with a high frequency of heterozygotes in females when the Z and the W chromosomes carry alleles with different frequencies. In the most extreme case where the two sex chromosomes are fixed for different alleles, all females are heterozygotes, whereas all males are homozygotes; an example was found in the sample from location 7 (Table 3). Males are expected to show Hardy–Weinberg proportions when the Z chromosome is polymorphic. This was observed at several of the sampling locations (Table 3). Two of the tests for random union of gametes were significant at the 5% level (Table 3). The reason for the significance in the sample from location 11 was probably that J. albifrons and J. ischiosetosa were sympatric with rather high frequencies. Thus the females consisted of a large fraction of J. albifrons individuals, which might have caused the significance. In the sample from location 8, the hypothesis of random union of gametes was rejected at the 0.035 level, which was nonsignificant on a tablewide level. The genotypic distributions in J. ischiosetosa agreed with those expected under the assumption of random union of gametes.
Siegismund and Christensen (1992) formulated an additional hypothesis that puts a further restriction on the data: the Z and W chromosomes carry alleles with the same frequencies. Not unexpectedly, this hypothesis was rejected in all populations since the genotypic distributions were very different in females and males (data not shown).
The genotypic distributions at the other three loci (Mdh, Mpi, and Pgm) agreed with the expectation for autosomal loci in all species. There was no suggestion of different genotypic distributions among sexes, except at locations with sympatric species in high frequencies (data not shown). To avoid problems with mixtures of females from different species, only males were included. The variation of the common alleles at the three loci (Mdh, Mpi, and Pgm) is presented in Table 4. Individuals carrying other alleles than those in these tables have been excluded. These alleles were always rare (with frequencies less than 0.01) and the number of omitted individuals was always very low for a single locality.
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All loci in the three species agreed with Hardy–Weinberg expectations. Of the 66 tests, two were significant at the 5% level, which was close to the expected number, and none was significant on a tablewide level. There was neither the suggestion of excess nor deficiency of heterozygotes at any locus of the three species. Only at the Mpi locus was there a slight suggestion of a deficiency of heterozygotes. Of 22 fixation indexes, 5 were negative and 17 positive. This number and more extreme numbers are only expected with a frequency of 0.017. The overall impression is that the genotypic distributions agree with Hardy–Weinberg proportions and that the samples can be described by the allele frequencies.
Population Structure
The variation at the autosomal loci was similar in the three Jaera species. At the Mdh locus, all three species had the same allele (100) as the most frequent allele and the other two alleles were in the same frequency range. The same pattern was observed at the Mpi locus. Nineteen of the populations had the same allele (100) as the most frequent. The variation at the Pgm locus was more irregular, but the same two alleles (100, 95) were the most frequent in all populations.
The genetic relatedness among the populations based on the variation at the autosomal loci is shown in Figure 2. There is no suggestion of a partitioning of the tree into three species groups. Rather, the geographical position of a population seems to have a certain influence on its placement in the tree. For example, populations that geographically are close or next to each other are often found close to each other in the tree (Figure 2). The influence of geography on the placement of populations in the tree was not supported by a Mantel test (Mantel 1967), where matrices of geographical distances and Nei's genetic distances were compared with a permutation test (P =.08).
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The hierarchical F-statistics confirm the pattern observed in the tree. (This analysis is based on the two species where several populations have been sampled, i.e., J. albifrons and J. ischiosetosa). The average level of differentiation among populations within species, FSP, is similar in both species, with an average of 0.091 (Table 5). There is no suggestion of segregation among the species. The average FPT value is slightly negative, indicating a lack of genetic differentiation among them.
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The variation at the Gpi locus differs among the three species. Besides the difference in inheritance, there seems to be larger differences in allele frequencies among the species than observed at the autosomal loci. Three common alleles were found in both J. albifrons and J. praehirsuta (Table 2), whereas only two common alleles were found in J. ischiosetosa (Table 3). For the analysis of the F-statistics and the estimation of the phylogenetic tree among the populations, the individuals of J. ischiosetosa carrying the rare allele found in the other two species was included (it had a frequency of 0.003). The differences in frequencies among the species are so large that the populations are partitioned in the tree (Figure 3), with J. ischiosetosa being separated from the other two species. This observation is supported by the hierarchical F-statistics (Table 5). The within-species component, FSP, is somewhat higher in J. ischiosetosa compared to J. albifrons, but the average level (0.141) is of the same order as observed at the autosomal loci. The between-species component, FPT = 0.510, is larger than the within-species component and substantially larger than that observed at the autosomal loci.
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Discussion |
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The genotypic variation at the four polymorphic loci in the three Jaera species agreed with the expected distributions for random union of gametes in all local populations. This result differs from the study of Piertney and Carvalho (1994, 1997) on the population structure of members of the J. albifrons complex in Wales. They reported consistent deviations from Hardy–Weinberg proportions, with an excess of homozygotes for local populations. This was explained by relatively high levels of inbreeding in small isolated populations under rocks. Piertney and Carvalho (1994, 1997) attributed this to the direct development of the Jaera species, where the females carry eggs in brood pouches until they hatch, and to the limited dispersal ability of adults. Localized inbreeding was supported by the finding of high levels of genetic relatedness in local populations using DNA fingerprinting (Piertney and Carvalho 1995).
Piertney and Carvalho (1994, 1997) also found great differentiation on a microgeographic scale. Populations separated by less than 5 m differed significantly in allele frequencies. If the Danish populations had been subdivided on a similar scale, this would probably have produced significant departures from Hardy–Weinberg proportions due to Wahlund effects, since most of the samplings took place on a stretch of several hundred meters along the coast. Gene flow on a local scale seems to be significantly higher in Danish than in Welsh populations. As suggested by Piertney and Carvalho (1994), this could be due to more homogeneous environments because of a limited tidal range in Danish waters.
Another aspect that distinguishes Danish from Welsh populations is the inheritance of the Gpi locus in J. ischiosetosa. In contrast to Danish populations, there was no suggestion that this locus was sex linked in the Welsh populations studied by Piertney and Carvalho (1997). They found significant deviations from Hardy–Weinberg expectations with a deficiency of heterozygotes. Since they included both sexes in their samples, they would probably have detected an excess of heterozygotes if this locus was inherited as sex linked and had different allele frequencies as in the Danish populations.
The most striking observation in the Danish Jaera populations was the difference in population structure of autosomal and sex-linked variation. There was no differentiation among species for autosomal variation, in contrast to the sex-linked locus, where the between-species component reached 0.51. In this respect, again, they differ from the reports on the variation found in Wales. A direct comparison of F-statistics is not possible since Piertney and Carvalho (1997) did not report hierarchical F-statistics that included between-species components, but a qualitative comparison is feasible. In Wales, the variation at the Gpi locus was similar in J. albifrons and J. ischiosetosa; both carried the same two alleles within the same frequency range. At four other loci, one of the species carried an allele not present in the other at high frequencies.
The observed pattern of differentiation of Danish Jaera populations could be explained in several ways. First, similar allele frequencies in different species could reflect responses to local selection pressures. Second, the different morphs recorded in Denmark could belong to the same species. Third, introgression between the species could result in related allele frequency arrays among them (although with different levels of introgression of autosomes and sex chromosomes).
The first explanation implies natural selection as an important factor in shaping the population structure. An increasing number of studies have demonstrated differential fitness effects of molecular variants (reviewed in Watt and Dean 2000). In particular, variation at the Gpi locus has been shown to be influenced by natural selection in several cases, for example, Colias butterflies (Watt et al. 1996), Gryllus crickets (Harrison 1977), and the isopod Asellus aquaticus (Shibab and Heath 1987a,b). The lack of differentiation among species at the three loci Mdh, Mpi, and Pgm could be imagined as a response of closely related species to similar selection pressures (Harrison 1977). This effect would be expected to result in parallel allele frequencies in geographically closely situated populations. The variation at the loci was similar in the studied species but was not parallel, as suggested by the nonsignificance of the Mantel test. Therefore natural selection does not seem to be a likely explanation.
With regard to the status of members of the J. albifrons complex, they are normally considered as distinct species (e.g., Naylor 1972) and the genetic data from the Welsh populations clearly support this (Piertney and Carvalho 1997). If the Danish populations are members of a single species, they are expected to interbreed freely within populations. Unfortunately there was only a single location (11) where two species were found with high frequencies. At this location they differ at the Gpi locus (Tables 2 and 3). At two other loci, Mpi and Pgm, the variation is homogeneous (tested with the number of observed alleles), whereas the variation at the Mdh locus differs significantly among the species (
2 = 12.04, P =.002, df = 2). This indicates that the two species do not interbreed freely in sympatric populations.
The third explanation, introgression, seems more plausible. Species within the J. albifrons complex are known to hybridize, although in a limited amount. Solignac (1981) reported a frequency of hybrids in France of 0.001–0.01, and Carvalho (1989) found hybrids with a lower incidence, less than 0.001, in Wales.
The Jaera species differ from each other by Robertsonian translocations. If the species were chromosomally similar to each other in Denmark, this could facilitate introgression. Both J. albifrons and J. ischiosetosa are polymorphic for these translocations in populations that have been studied in Europe. J. albifrons is the most variable species; the diploid number for males varies from 18 to 28, with most of the populations being monomorphic (Lécher 1967, 1968). In J. ischiosetosa, the range is lower, with the diploid number in males varying from 26 to 30 on the European continent and from 26 to 32 in Iceland (Lécher and Solignac 1972, 1975). Intraspecific crosses between populations that differ in a single fusion result in hybrids showing trivalents at the meiosis, whereas crosses between populations differing in more fusions result in meiotic abnormalities (Lécher 1967), suggesting a partial isolation between these populations. Lécher and Solignac (1975) have investigated several Danish J. ischiosetosa populations. Two populations on the east coast of Jutland and one at location 7 were polymorphic, with the diploid numbers in males ranging from 28 to 30. One population on the west coast of Jutland and one from the German Baltic coast were monomorphic with 2n = 30 (for males). Less is known about J. albifrons in Denmark. Lécher (1968) reported that a J. albifrons population from the northern part of Jutland had a diploid number of 26 in males. The same number was found in a population from the German part of the Baltic Sea. The difference in chromosome number between J. albifrons and J. ischiosetosa in Denmark is smaller than the differences between the highest and the lowest number in either of the species. This could possibly reduce hybrid breakdown as an isolating mechanism.
The introgression seems to be limited to the autosomes. The variation at the Gpi locus suggests that the exchange of sex chromosomes is low. This raises the question of whether the Gpi locus is sex linked in J. albifrons and J. praehirsuta. If it is sex linked in the two species and its position is more distal to the centromere, this could allow a sufficiently high recombination rate to keep the gene frequencies on Z and W chromosomes close to each other. The outcome would be the observed Hardy–Weinberg distributions in these species. The more proximal position of the Gpi locus in J. ischiosetosa could have arisen by an inversion that included most of the Z chromosome. This also limits the translocation of an autosome to the Z chromosome to a single event in the J. albifrons complex, where it is known that females are ZW1W2 in all four European species (Staiger and Bocquet 1954).
An inversion on the Z chromosome in J. ischiosetosa could probably reduce the crossing over of homologous parts of the sex chromosomes in hybrid males, thus keeping the Z chromosomes as separate units in the different species. Sex chromosomes often have a large effect on postzygotic isolation (Coyne and Orr 1999). In addition, in species with females being the homogametic sex, it has been found that a substantial fraction (approximately 1/3) of the phenotypic variation in sexually selected traits is caused by X-linked genes (Reinhold 1998). Therefore one could imagine that if Z chromosomes carry a major part of the loci that control the morphological and behavioral differences between the species, this could explain why the species in the J. albifrons complex have not merged into a single species.
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Acknowledgments |
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I thank Pernille Selmer Olsen for technical assistance and Bent Christensen, Marianne Philipp, and Thure P. Hauser for comments on the manuscript. This study was supported in part by grant no. 9901844 from the Danish Natural Science Research Council.
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Footnotes |
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Corresponding Editor: Sudhir Kumar
Received September 26, 2001
Accepted September 30, 2002
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References |
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Bocquet C, 1953. Recherches sur le polymorphisme naturel des Jaera marina (Fabr.) (Isopodes Asellotes). Arch Zool Exp Genet. 90:187-450.
Carvalho GR, 1989. Microgeographic genetic differentiation and dispersal capacity in the intertidal isopod Jaera albifrons Leach. In: Reproduction, genetics and distribution of marine organisms (Ryland JS and Taylor PA, eds). Fredensborg, Denmark: Olsen & Olsen; 265–271.
Carvalho GR, Piertney SB, 1997. Interspecific comparison of genetic population structure in members of the Jaera albifrons species complex. J Mar Biol Assoc UK. 77:77-93.
Coyne JA, Orr HA, 1999. The evolutionary genetics of speciation. In: Evolution of biological diversity (Magurran AN and May RM, eds). Oxford: Oxford University Press; 1–36.
Felsenstein J, 1973. Maximum-likelihood estimation of evolutionary trees from continuous characters. Am J Hum Genet. 25:471-492.[ISI][Medline]
Felsenstein J, 1981. Evolutionary trees from gene frequencies and quantitative characters: finding maximum likelihood estimates. Evolution. 35:1229-1242.[CrossRef]
Felsenstein J, 1993. PHYLIP (phylogeny inference package), version 3.5c. Seattle: University of Washington.
Forsman B, 1944. Beobachtungen über Jaera albifrons Leach an der schwedischen Westküste. Ark Zool. 35:1-33.
Forsman B, 1949. Weitere Studien über die Rassen von Jaera albifrons. Leach. Zool Bidr Uppsala. 27:449-463.
Guo SW, Thompson EA, 1992. Performing the exact test of Hardy–Weinberg proportion for multiple alleles. Biometrics. 48:361-372.[CrossRef][ISI][Medline]
Harris H, Hopkinson DA, 1976. Handbook of enzyme electrophoresis in human genetics. Amsterdam: North Holland.
Harrison RG, 1977. Parallel variation at an enzyme locus in sibling species of field crickets. Nature. 266:168-170.[CrossRef][Medline]
Holm S, 1979. A simple sequentially rejective multiple test procedure. Scand J Stat. 6:65-70.
Jones MB, Naylor E, 1971. Breeding and bionomics of the Jaera albifrons group of species (Isopoda: Asellota). J Zool. 165:183-199.
Lécher P, 1967. Cytogénétique de l'hybridation expérimentale et naturelle chez l'isopode Jaera (albifrons) syei Bocquet. Arch Zool Exp Genet. 108:633-698.
Lécher P, 1968. Polymorphisme chromosomique dans les populations baltes et scandinaves de l'isopode Jaera (albifrons) syei Bocquet. Arch Zool Exp Genet. 109:211-227.
Lécher P, Solignac M, 1972. Étude caryologique de Jaera (albifrons) ischiosetosa (Crustacés, Isopodes). I. Polymorphisme chromosomique Robertsonien dans trois populations d'Islande. Arch Zool Exp Genet. 113:439-450.
Lécher P, Solignac M, 1975. Étude caryologique de Jaera (albifrons) ischiosetosa (Crustacés, Isopodes) III. Cline chromosomique des côtes ouest-européennes. Arch Zool Exp Genet. 116:591-614.
Mantel NA, 1967. The detection of disease clustering and a generalized regression approach. Cancer Res. 27:209-220.[ISI][Medline]
Naylor E, 1972. British marine isopods. London: Academic Press.
Naylor E, Haathela I, 1966. Habitat preferences and interspersion of species within the superspecies Jaera albifrons Leach (Crustacea, Isopoda). J Anim Ecol. 35:209-216.
Naylor E, Haathela I, 1967. Quantitative ecological distribution of the Jaera albifrons group of species in the Baltic. Ophelia. 4:19-27.
Piertney SB, Carvalho GR, 1994. Microgeographic genetic differentiation in the intertidal isopod Jaera albifrons Leach. I. Spatial distribution of allozyme variation. Proc R Soc Lond B. 256:195-201.[CrossRef]
Piertney SB, Carvalho GR, 1995. Detection of high levels of genetic relatedness in rock-populations of an intertidal isopod using DNA fingerprinting. J Mar Biol Assoc UK. 75:967-976.
Piertney SB, Carvalho GR, 1997. Interspecific comparisons of genetic population structure in members of the Jaera albifrons species complex. J Mar Biol Assoc UK. 77:77-93.
Reinhold K, 1998. Sex linkage among genes controlling sexually selected traits. Behav Ecol Sociobiol. 44:1-7.
SAS,, 1990. SAS/STAT user's guide, version 6. Cary, NC: SAS Institute.
Shibab AF, Heath DJ, 1987a. Components of fitness and the Pgi polymorphism in the freshwater isopod Asellus aquaticus (L.). 1. Fecundity selection. Heredity. 58:69-73.
Shibab AF, Heath DJ, 1987b. Components of fitness and the Pgi polymorphism in the freshwater isopod Asellus aquaticus (L.). 2. Zygotic selection. Heredity. 58:289-295.
Shuster SM, Levy L, 1999. Sex-linked inheritance of a cuticular pigmentation marker in the marine isopod, Paracerceis sculpta Holmes (Crustacea: Isopoda: Sphaeromatidae). J Hered. 90:304-307.
Siegismund HR, Christensen B, 1992. A sex linked enzyme polymorphism in the marine isopod Jaera ischiosetosa. J Hered. 83:388-393.
Solignac M, 1981. Isolating mechanisms and modalities of speciation in the Jaera albifrons species complex (Crustacea, Isopoda). Syst Zool. 30:387-405.[CrossRef]
Staiger H, Bocquet C, 1954. Cytological demonstration of female heterogamety in isopods. Experientia. 10:64-69.[CrossRef][ISI][Medline]
Watt WB, Dean AM, 2000. Molecular-functional studies of adaptive variation in prokaryotes and eukaryotes. Annu Rev Genet. 34:593-622.[CrossRef][ISI][Medline]
Watt WB, Donohue K, Carter PA, 1996. Adaptation at specific loci. VI. Divergence vs. parallelism of polymorphic allozymes in molecular function and fitness-component effects among Colias species (Lepidoptera, Pieridae). Mol Biol Evol. 13:699-709.[ISI]
Weir BS, Cockerham CC, 1984. Estimating F-statistics for the analysis of population structure. Evolution. 38:1358-1370.[CrossRef][ISI]
Yeh F, Yang R-C, Boyle T, Ye Z-H, Mao JX, 1997. POPGENE, the user-friendly shareware for population genetic analysis. Edmonton: University of Alberta.
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