Comparative karyotypes of two northeastern Pacific abalone species (Haliotis fulgens Philippi and Haliotis rufescens Swainson).
KEY WORDS: chromosomes, karyotype, centromeric-index, relative-length, arm-ratio, Haliotidae
Abalones grouped within the genus Haliotis, Linnaeus 1758, comprise from 60 to 70 species described worldwide (Lindberg 1992). They are distributed in the northeast Pacific, northwest Pacific, tropical west Pacific or Indo-Pacific, southwest Pacific, and Mediterranean Sea (Lindberg 1992, Lee & Vacquier 1995).
Karyotypes in abalones have been studied only for few of those 60 to 70 described species. Those species include H. cracherodii, from the northeast Pacific (Minkler 1977) with a diploid chromosome number 2 n = 36; H. discus, H. discus hannai, H. gigantea, and H. madaka from the northwest Pacific (Arai et al. 1982, Nakamura 1986, Wang et al. 1988, Okumura et al. 1995 in Okumura et al. 1999, Miyaki et al. 1997, Miyaki et al. 1999, Okumura et al. 1999) with a 2 n = 36; H. varia, H. planata, H. diversicolor aquatilis, H. diversicolor diversicolor, H. ovina, and H. asinina from the Indo-Pacific or tropical west Pacific (Nakamura 1985, Nakamura 1986, Arai et al. 1988, Jarayabhand et al. 1998) with a 2 n = 32; and for H. tuberculata from the Mediterranean Sea (Colombera & Tagliaferri 1983, Arai & Wilkins 1986) with a 2n = 28. The knowledge of karyotypes in abalone species could provide useful information for systematics of abalone species, and also with a tool to determine the most adequate species for hybridization. Hybridization has been reported to occur among abalone species within certain geographic areas (Owen et al. 1971, Leighton & Lewis 1982, Koike et al. 1988, Hoshikawa et al. 1998), and it represents a potentially important tool for genetic improvement of abalones.
In this research, we aim to define the karyotype of two abalone species distributed in the northeast Pacific, green (or blue) abalone (Haliotis fulgens) and red abalone (Haliotis rufescens). The karyotypes for these species have not been described, but it was previously reported that both hybridize (Leighton & Lewis 1982).
MATERIALS AND METHODS
For both species, adult abalone was induced to spawn at 2 different abalone hatcheries. For red abalone, 8 cultured organisms at the commercial laboratory "BC Abalone" in Erendira, Baja California, Mexico were used, and for green abalone 8 wild adults kept at the Laboratory of Abalone Spat Production from "Cooperativa de Buzos y Pescadores" at Isla Natividad, BCS, Mexico. They were induced to spawn, eggs fertilized, and the first hatching trochophore larvae were collected for this study. For both species, only spawns that produced normal and viable larvae were used to collect samples.
Miyaki et al. (1997) procedures for treating larvae and making slides were used. In short, colchicine (0.1%) was applied to the larvae for 2 h, applying a hypotonic shock with sodium citrate (1%) immediately after for 40 min. Larvae were fixed in Carnoy solution, exchanging this solution 3 times every 15 min. Slides were made by placing 50 to 100 larvae on a clean slide, adding 2 drops of cooled acetic acid (60%), macerating with a surgical knife to obtain a cell suspension, and dropping on this cell suspension from a height of 10-15 cm Carnoy solution to expand the macerated cells on the slide. The slides were heated and allowed to dry for approximately 1 h before staining with Giemsa (10%) for 10 min.
Chromosome counts were done at 100X using an Olympus BX41 microscope. A total of 59 metaphases and 60 metaphases were counted for red abalone and for green abalone respectively.
Karyotypes and quantitative measurements of chromosomes for both species were done using the best 10 metaphases obtained from each abalone species. Each metaphase was selected from different slides to guarantee they were derived from different larvae. Each metaphase was digitalized using a Cool SNAP-Pro (Media Cybernetics) camera, and transferred to an image analyses program (Image-Pro Plus 4.5 Program). Measurements of short and long arms of each chromosome, and mean relative length (RL) of chromosomes were estimated according to Thiriot-Quievreux (1984), and centromeric indices (CI) and long and short arms relative lengths (LA, SA) based on Levan et al. (1964). Classification of chromosomes was done using centromeric index according to Levan et al. (1964), using conventional names (m for metacentric, sm for submetacentric, st for subtelocentric). Those chromosomes whose mean CI fell within the limit of different types of chromosomes were classified as intermediates between the 2 classes (i.e., m-sin & sm-st). The fundamental number was estimated as White (1973), assigning the value of 4 to all metacentric, submetacentric, and subtelocentric chromosomes, and a value of 2 to telocentric pairs.
Chromosomes comparisons between the two species were done by means of a karyo-ideogram (Spotorno 1985), plotting the relative length of the short versus the long arm with their confidence intervals (n = 10, alpha = 0.05).
From the 60 metaphases evaluated for H. fulgens, 85% had a diploid chromosome number 2 n = 36, and for the 59 metaphases in H. rufescens 61% a 2 n = 36 (Fig. 1).
[FIGURE 1 OMITTED]
The karyotype and a representative metaphase from which they were compared for each species are presented in Figure 2a (H. fulgens) & 2b (H. rufescens). For H. fulgens the relative length of the largest chromosome was 7.14 and that of the smallest chromosome was 4.45. For H. rufescens the relative length of the largest chromosome was 6.71 and that of the smallest chromosome was 4.48 (Table 1). The fundamental number for both species was 72.
[FIGURE 2 OMITTED]
Based on the karyo-idiogram, the karyotype of H. fulgens (Fig. 3) can be classified as consisting of 10 pairs of metacentric chromosomes, 3 pairs metacentric-submetacentric, 4 pairs submetacentric, and 1 pair submetacentric-subtelocentric (tending to subtelocentric because of its confidence interval). No telocentric chromosomes were observed. The karyotype of H. rufescens is different than that in H. fulgens, because it consists of 8 pairs of metacentric chromosomes, 6 pairs metacentric-submetacentric, 3 pairs submetacentric, and 1 pair submetacentric-subtelocentric. As with H. fulgens, no telocentric chromosomes were observed for H. rufescens.
[FIGURE 3 OMITTED]
The analysis by the karyo-ideogram comparing relative lengths of short and long arms, and an analysis of chromosomes differences in centromeric index between the two species indicated consistent significant (P < 0.05) differences in relative lengths of short and long arms and in centromeric index between 5 of the 18 chromosomes (4, 7, 9, 11, & 18). Other chromosomes differed in CI or in one or other of the arms lengths, but not in all three (Table 1, Fig. 3).
From the abalone species for which karyotypes have been published, the smallest diploid number has been 2 n = 28, followed by an intermediate diploid number of 2 n = 32, and the largest diploid number reported being 2 n = 36 (Table 2). The diploid number of abalone species for which chromosomal studies have been done follows a pattern associated with the geographic distribution of the species (Nakamura 1986), with a 2 n = 28 seen for the Mediterranean species H. tuberculata (also named H. lamellosa), a 2 n = 32 being present among species of the Indo-Pacific or tropical west Pacific, which includes H. varia, H. planata, H. diversicolor aquatilis, H. diversicolor diversicolor, H. asinina, and H. ovina, and the largest 2 n = 36 seen for species described for the northeast and northwest Pacific, as H. madaka, H. discus, H. gigantea, H. discus hannai, and H. cracherodii (Table 2).
Based on genetic studies, today it is believed that not all those described abalone species are different. For example, lysine cDNA sequence homology among 27 Haliotis species has indicated that some of the described abalone species around the world are, in fact, the same species (Lee & Vacquier 1995). Species that are possibly a single one and are included in Table 2 are, for the Pacific northwest H. madaka and H. discus hannai; for the Indo-Pacific H. diversicolor supertexta and H. diversicolor aquatilis; and from the Mediterranean H. tuberculata tuberculata and H. tuberculata lamellosa (or H. lamellosa). Two additional genetic studies based on isozyme analyses have also suggested that H. madaka and H. discus are the same species (Hara & Fujio 1992 in Lee & Vacquier 1995), and that H. diversicolor diversicolor is different from H. planata and H. varia (Arai et al. 1988). Differences in karyotypes seem to confirm that H. madaka, H. discus and H. discus hannai are the same species, and that H. diversicolor diversicolor is different from H. planata and H. varia (Table 2).
The diploid chromosome number, 2 n = 36 of the two species evaluated in the present study, H. rufescens and H. fulgens, is in agreement with the previously reported karyotype for only one species from the northeast Pacific, H. cracherodii (Minkler 1977), and the reported association between the diploid number with geographic distribution (Nakamura 1986). In as much as the northwest Pacific (Japan) abalone species also have a diploid number of 36, our results confirm that marked differences in karyotypes do exist between northwest and northeast Pacific abalones. Northwest Pacific abalones only have metacentric and submetacentric chromosomes, whereas northeast Pacific abalones have those types and additionally have intermediates between those types, and two (Minkler 1977) telocentric pairs of chromosomes, or one submetacentric-subtelocentric in this study. The importance of defining chromosome types as intermediates between two classes comes from different conclusions reached in different studies for the same species. For example, northwest abalone species described for northwest Pacific are very homogeneous in number of metacentric and submetacentric chromosomes, with most reports indicating that there are 10 pairs of metacentric and 8 pairs of submetacentric chromosomes in H. discus (H. discus discus, H. discus hannai, and H. madaka), and H. gigantea (Arai et al. 1982, Okumura et al. 1995 in Okumura et al. 1999, Miyaki et al. 1997, Miyaki et al. 1999). However, there are also two reports (Wang et al. 1988, Okumura et al. 1999) indicating 11 pairs of metacentric and 7 pairs of submetacentric for H. discus (H. discus hannai). The differences reported for H. discus (H. discus hannai) have been attributed to three pairs of chromosomes (4, 9, and 17) that have arm ratios close to the limits of the classification between metacentric and submetacentric (Okumura et al. 1999), resulting in ambiguous classification even within which today is believed to be the same species.
Contrasting the homogeneity in types of chromosomes for northwest Pacific species, the northeast Pacific species evaluated so far indicate less homology in the numbers of metacentric (m), submetacentric (sm), and subtelocentric (st) chromosomes between species (H. cracherodii with 8 m: 8 sm: 2 st, but H. fulgens with 10 m: 3 m-sm: 4 sm: 1 sm-st, and H. rufescens with 8 m: 6 m-sm: 3 sm: 1 sm-st. Lack of homology in karyotypes has also been reported for the Indo-Pacific species studied so far, which are characterized by a diploid chromosome number of 2 n = 32. However, lack of homology in karyotypes has been reported also for what is now believed (Lee & Vacquier 1995) to be the same species (Table 2). This result can be explained by the reduced sample size used for karyotyping, or by using low quality metaphases. For example, within this group of Indo-Pacific abalone species, two conflicting karyotypes have been reported within two species, H. varia (Nakamura 1986, Arai et al. 1988, Jarayabhand et al. 1998) and H. diversicolor (Nakamura 1985, Arai et al. 1988). Nakamura (1986) states that his data for H. varia are not precise because of the small size (1.41 to 3.63 [micro]m) of some of the chromosomes he found, and Jarayabhand et al. (1998) attributes the difference in his study with that in Arai et al. (1988) to different methodological conditions. However, the microphotographs of H. varia karyotype included in Jarayabhand et al. (1998) indicate a possible problem with measurements because of the small chromosome size and a low definition of metaphases. The differences reported for karyotypes within H. diversicolor can be explained by one author classifying 2 chromosomes as submetacentric, whereas the other one classifies those chromosomes as submetacentric-subtelocentric, indicating that the centromeric index is in the limits of both classes, pointing again to the need for more detailed classification when the chromosome centromeric indices are in, or close to the limits of two classifications.
Based on the results obtained in this study, indicating that whereas the chromosomes of H. rufescens and H. fulgens do not differ in their relative length (RL), that 5 of the 18 chromosomes were different in centromeric index (CI), relative length of short arm, and relative length of long arm, it is possible to propose causes for the differences in chromosome structure between these two species. For all of those chromosomes that were different (4, 7, 9, 11, and 18), pericentric inversions can be proposed to be the evolutionary force differentiating the two species. Pericentric inversions represent a structural chromosome change known to be the most frequent mutations in the evolution of karyotypes (White 1978). Finally, another important difference between the karyotypes of the two species is the position of the only submetacentric-subtelocentric chromosome in each, based on decreasing RLs, which is in position on chromosome number 14 for H. fulgens and position on chromosome number 18 for H. rufescens, suggests a possible translocation event in the common linage of these species.
A characteristic among abalone species reported in the literature is the presumable existence of hybrids. The occurrence of hybridization has been inferred from morphologic characteristics in natural populations (Owen et al. 1971) or from mating experiments in the laboratory (Leighton & Lewis 1982, Koike et al. 1988, Hoshikawa et al. 1998). However, genetic confirmation of hybridization has only been done for hybrids of H. kamtschatkana and H. discus hannai (Hoshikawa et al. 1998). Given the karyotype differences observed in this study it is possible to conclude that even if fertilization between these two species can be achieved producing hybrids, those hybrids would be expected to have a reduced fertility because of improper synapses of not perfectly homologous chromosomes during meiosis (Freeman & Herron 2001). In agreement, Leighton & Lewis (1982) found a low viability (0.1%) to postlarva when mating (presumed, not genetically certified) hybrids of red and green abalone.
TABLE 1. Karyotype comparison of Haliotis fulgeus (H.f.) and Haliotis rufescens (H.r.): relative length RL, short arm length SA, long arm length LA, centromeric index CI, and chromosome classification derived from 10 metaphases for each species. Standard deviations are presented ([+ or -] sd) for each mean. RL [+ or -] sd Chrom pair H.f H.r. 1 7.14 [+ or -] 0.38 (a) 6.71 [+ or -] 0.51 (a) 2 6.77 [+ or -] 0.59 (a) 6.68 [+ or -] 0.31 (a) 3 6.70 [+ or -] 0.34 (a) 6.63 [+ or -] 0.40 (a) * 4 6.55 [+ or -] 0.33 (a) 6.23 [+ or -] 0.66 (a) 5 6.43 [+ or -] 0.53 (a) 6.09 [+ or -] 0.45 (a) 6 6.05 [+ or -] 0.28 (a) 6.08 [+ or -] 0.45 (a) * 7 5.79 [+ or -] 0.46 (a) 5.93 [+ or -] 0.22 (a) 8 5.70 [+ or -] 0.55 (a) 5.88 [+ or -] 0.45 (a) * 9 5.55 [+ or -] 0.26 (a) 5.64 [+ or -] 0.25 (a) 10 5.27 [+ or -] 0.26 (a) 5.42 [+ or -] 0.24 (a) * 11 5.22 [+ or -] 0.35 (a) 5.15 [+ or -] 0.33 (a) 12 5.19 [+ or -] 0.28 (a) 5.13 [+ or -] 0.24 (a) 13 4.80 [+ or -] 0.19 (a) 5.09 [+ or -] 0.25 (a) 14 4.68 [+ or -] 0.25 (a) 5.06 [+ or -] 0.18 (a) 15 4.64 [+ or -] 0.28 (a) 4.61 [+ or -] 0.20 (a) 16 4.55 [+ or -] 0.35 (a) 4.60 [+ or -] 0.22 (a) 17 4.53 [+ or -] 0.25 (a) 4.59 [+ or -] 0.26 (a) * 18 4.45 [+ or -] 0.27 (a) 4.48 [+ or -] 0.15 (a) SA [+ or -] sd Chrom pair H.f. H.r. 1 2.97 [+ or -] 0.13 (a) 3.18 [+ or -] 0.22 (a) 2 2.53 [+ or -] 0.29 (a) 2.88 [+ or -] 0.17 (a) 3 3.11 [+ or -] 0.19 (a) 3.02 [+ or -] 0.23 (a) * 4 1.96 [+ or -] 0.16 (a) 2.44 [+ or -] 0.20 (a) 5 2.88 [+ or -] 0.25 (a) 2.07 [+ or -] 0.16 (b) 6 1.91 [+ or -] 0.18 (a) 2.26 [+ or -] 0.23 (a) * 7 2.22 [+ or -] 0.17 (a) 1.81 [+ or -] 0.18 (b) 8 2.06 [+ or -] 0.24 (a) 2.52 [+ or -] 0.21 (b) * 9 2.64 [+ or -] 0.17 (a) 2.18 [+ or -] 0.18 (b) 10 1.73 [+ or -] 0.10 (a) 2.26 [+ or -] 0.11 (b) * 11 2.11 [+ or -] 0.14 (a) 2.47 [+ or -] 0.13 (b) 12 2.27 [+ or -] 0.15 (a) 1.98 [+ or -] 0.09 (b) 13 1.96 [+ or -] 0.13 (a) 2.24 [+ or -] 0.12 (b) 14 1.26 [+ or -] 0.13 (a) 1.74 [+ or -] 0.05 (b) 15 1.69 [+ or -] 0.10 (a) 1.66 [+ or -] 0.11 (a) 16 2.12 [+ or -] 0.21 (a) 1.90 [+ or -] 0.10 (a) 17 2.18 [+ or -] 0.12 (a) 2.11 [+ or -] 0.13 (a) * 18 1.85 [+ or -] 0.13 (a) 1.13 [+ or -] 0.07 (b) LA [+ or -] sd Chrom pair H.f H.r. 1 4.17 [+ or -] 0.32 (a) 3.53 [+ or -] 0.33 (a) 2 4.24 [+ or -] 0.38 (a) 3.80 [+ or -] 0.19 (a) 3 3.59 [+ or -] 0.19 (a) 3.61 [+ or -] 0.19 (a) * 4 4.59 [+ or -] 0.32 (a) 3.79 [+ or -] 0.52 (b) 5 3.55 [+ or -] 0.31 (a) 4.02 [+ or -] 0.39 (a) 6 4.13 [+ or -] 0.16 (a) 3.83 [+ or -] 0.27 (a) * 7 3.57 [+ or -] 0.32 (a) 4.11 [+ or -] 0.20 (b) 8 3.64 [+ or -] 0.36 (a) 3.36 [+ or -] 0.38 (a) * 9 2.91 [+ or -] 0.14 (a) 3.46 [+ or -] 0.11 (b) 10 3.55 [+ or -] 0.19 (a) 3.16 [+ or -] 0.22 (a) * 11 3.12 [+ or -] 0.25 (a) 2.68 [+ or -] 0.21 (b) 12 2.92 [+ or -] 0.16 (a) 3.15 [+ or -] 0.17 (a) 13 2.84 [+ or -] 0.14 (a) 2.85 [+ or -] 0.19 (a) 14 3.42 [+ or -] 0.18 (a) 3.32 [+ or -] 0.17 (a) 15 2.95 [+ or -] 0.22 (a) 2.95 [+ or -] 0.13 (a) 16 2.43 [+ or -] 0.15 (a) 2.70 [+ or -] 0.16 (a) 17 2.35 [+ or -] 0.16 (a) 2.48 [+ or -] 0.15 (a) * 18 2.59 [+ or -] 0.18 (a) 3.35 [+ or -] 0.14 (b) IC [+ or -] sd Chrom pair H.f H.r. 1 41.70 [+ or -] 1.85 (a) 47.40 [+ or -] 1.44 (b) 2 37.32 [+ or -] 2.44 (a) 43.10 [+ or -] 1.36 (b) 3 46.38 [+ or -] 1.41 (a) 45.55 [+ or -] 1.29 (a) * 4 29.92 [+ or -] 2.29 (a) 39.33 [+ or -] 2.72 (b) 5 44.83 [+ or -] 1.39 (a) 34.10 [+ or -] 2.43 (b) 6 31.59 [+ or -] 1.78 (a) 37.07 [+ or -] 1.71 (b) * 7 38.40 [+ or -] 1.41 (a) 30.54 [+ or -] 2.64 (b) 8 36.07 [+ or -] 2.05 (a) 42.97 [+ or -] 3.17 (b) * 9 47.63 [+ or -] 1.52 (a) 38.66 [+ or -] 1.63 (b) 10 32.76 [+ or -] 1.14 (a) 41.80 [+ or -] 2.13 (b) * 11 40.37 [+ or -] 1.75 (a) 48.03 [+ or -] 0.87 (b) 12 43.79 [+ or -] 1.33 (a) 38.62 [+ or -] 1.05 (b) 13 40.80 [+ or -] 1.95 (a) 43.96 [+ or -] 1.91 (a) 14 26.86 [+ or -] 1.95 (a) 34.45 [+ or -] 1.26 (b) 15 36.45 [+ or -] 1.64 (a) 36.07 [+ or -] 1.42 (b) 16 46.58 [+ or -] 1.46 (a) 41.37 [+ or -] 1.42 (b) 17 48.07 [+ or -] 1.34 (a) 46.0 [+ or -] 1.38 (a) * 18 41.67 [+ or -] 1.59 (a) 25.14 [+ or -] 1.32 (b) C Chrom pair H.f. H.r. 1 m m 2 m-sm m 3 m m * 4 sm m-sm 5 m sm 6 sm sm-m * 7 m-sm sm 8 sm m * 9 m m-sm 10 sm m * 11 m m 12 m m-sm 13 m m 14 sm-st sm 15 sm-m sm-m 16 m m 17 m m * 18 m sm-st * indicates that the chromosomes between the two species are different in SA, LA, and IC. Different letters between species indicate significant differences based on confidence intervals (P < 0.05). m, metacentric; sm, submetacentric; st, subtelocentric. TABLE 2. World abalone species evaluated for their karyotype. Distribution Species s n 2n FN m European-Mediterranean (1) H. tuberculata 28 56 8 " 14 28 H. Lamellosa 14 28 * Indo-Pacific (2) H. varia 16 32 64 * 13 " 32 64 * 9 " 32 64 * 8 H. planata 32 64 * 9 H. diversicolor 16 32 64 * 8 aquatilis H. diversicolor 32 64 * 8 diversicolor H. asinina 32 64 * 10 H. ovina 32 62 * 9 Pacific Northwest (3) H. discus 36 72 * 10 " 36 72 10 " 36 72 10 H. discus 36 72 * 10 hannai " 36 72 11 " 36 72 * 10 " 36 72 * 11 H. madaka 36 72 10 H. gigantea 18 36 * 36 72 10 Pacific Northeast (3) H. cracherodii 36 72 * 8 H. fulgens 36 72 10 H. refuscens 36 72 8 Distribution Species m-sm sm sm-st st t European-Mediterranean (1) H. tuberculata 6 " H. Lamellosa Indo-Pacific (2) H. varia 3 " 6 1 " 8 H. planata 6 1 H. diversicolor 5 2 1 aquatilis H. diversicolor 7 1 diversicolor H. asinina 6 H. ovina 6 1 Pacific Northwest (3) H. discus 8 " 8 " 8 H. discus 8 hannai " 7 " 8 " 7 H. madaka 8 H. gigantea 8 Pacific Northeast (3) H. cracherodii 8 2 H. fulgens 3 4 1 H. refuscens 6 3 1 Distribution Species R[L.- C[L.- A[R.- sup.L] sup.L] sup.L] European-Mediterranean (1) H. tuberculata " H. Lamellosa Indo-Pacific (2) H. varia " " H. planata H. diversicolor aquatilis H. diversicolor diversicolor H. asinina H. ovina Pacific Northwest (3) H. discus " " H. discus hannai " 7.09 " " 6.88 1.21 H. madaka H. gigantea Pacific Northeast (3) H. cracherodii H. fulgens 7.14 41.70 1.40 H. refuscens 6.71 47.40 1.11 Distribution Species R[L.- C[I.- A[R.- sup.S] sup.S] sup.S] European-Mediterranean (1) H. tuberculata " H. Lamellosa Indo-Pacific (2) H. varia " " H. planata H. diversicolor aquatilis H. diversicolor diversicolor H. asinina H. ovina Pacific Northwest (3) H. discus " " H. discus hannai " 4.11 " " 4.64 1.10 H. madaka H. gigantea Pacific Northeast (3) H. cracherodii H. fulgens 4.45 41.67 1.41 H. refuscens 4.48 25.14 3.01 Distribution Species Reference European-Mediterranean (1) H. tuberculata Arai & Wilkins 1986 " Colombera & Tagliaferri 1983 H. Lamellosa Indo-Pacific (2) H. varia Nakamura 1986 " Arai et al. 1988 " Jarayabhand et al. 1998 H. planata Arai et al. 1988 H. diversicolor Nakamura 1985 aquatilis H. diversicolor Arai et al. 1988 diversicolor H. asinina Jarayabhand et al. 1998 H. ovina Jarayabhand et al. 1998 Pacific Northwest (3) H. discus Arai et al. 1982 " Miyaki et al. 1997 " Miyaki et al. 1997 H. discus Arai et al. 1982 hannai " Wang et al. 1988 " Okumura et al. 1995 in Okumura et al. 1999 " Okumura et al. 1999 H. madaka Miyaki et al. 1999 H. gigantea Nakamura 1986 Miyaki et al. 1997 Pacific Northeast (3) H. cracherodii Minkler 1977 H. fulgens Present study H. refuscens Present study (1) Eurotis, (2) Padollus, (3) Nordotis: subgenera subdivision within the Haliotidae (Lee & Vacquier 1995). FN fundamental number, m metacentric, sm submetacentric, st subteloceniric, t telocentric, RL relative length, CI centrometric index, AR arm ratio, [sup.L] largest chromosome, s smallest chromosome. * data inferred (for FN: m, sm, st = 4, and for t = 2). (S) indicates within the same block species which have been later found to be the same one.
The authors thank the abalone laboratories BC Abalone, Erendira and Cooperativa de Buzos y Pescadores Isla, Natividad for the donation of biological material, and also Susana Avila from CIBNOR for laboratory technical support. The authors also thank Dr. Nick Elliot (CSIRO) and anonymous reviewers for valuable comments on the manuscript. This research was supported by CONACYT grant 38860-B to A. M. Ibarra.
Arai, K., K. Fujino & M. Kudo. 1988. Karyotype and zymogram differences among three species of the abalones Haliotis planata, H. varia, and H. diversicolor diversicolor. Nippon Suisan Gakkaishi 54:2055-2064.
Arai, K., H. Tsubaki, Y. Ishitani & K. Fujino. 1982. Chromosomes of Haliotis discus hannai Ino and Haliotis discus Reeve. Bull. Japan. Soc. Sci. Fish. 48:1689-1691.
Arai, K. & N. P. Wilkins. 1986. Chromosomes of Haliotis tuberculata L. Aquaculture 58:305-308.
Colombera, D. & F. Tagliaferri. 1983. Chromosomes from male gonads of Haliotis tubercolata and Haliotis lamellosa (Haliotidae, Archeogasteropoda, Mollusca). Caryologia 36:231-234.
Freeman, S. & J. C. Herron. 2001. Evolutionary analysis. Upper Saddle River, NJ: Prentice Hall. pp. 90-91.
Hara, M., Y. Fujio. 1992. Genetic relationships among abalone species. Suisan Ikushu. Mar. Aquacult. 17:55-61 (in Japanese).
Hoshikawa, H., Y. Sakai & A. Kijima. 1998. Growth characteristics of the hybrid between pinto abalone, Haliotis kamtschatkana Jonas, and ezo abalone, H. discus hannai Ino, under high and low temperatures. J. Shellfish Res. 17:673-677.
Jarayabhand, P., R. Yom-La & A. Popongviwat. 1998. Karyotypes of marine molluscs in the family Haliotidae found in Thailand. J. Shellfish Res. 17:761-764.
Koike, Y., Z. Sun & F. Takashima. 1988. On the feeding and growth of juvenile hybrid abalones. Suisanzoshoku 36:231-235.
Lee, Y.-H. & V. D. Vacquier. 1995. Evolution and systematics in Haliotidae (Mollusca: Gastropoda): inferences from DNA sequences of sperm lysin. Mar. Biol. 124:267-278.
Leighton, D. L. & C. A. Lewis. 1982. Experimental hybridization in abalones. Int. J. Invert. Reprod. 5:273-282.
Levan, A., K. Fredga & A. Sandberg. 1964. Nomenclature for centromeric position on chromosomes. Hereditas 52:201-220.
Lindberg, D. R. 1992. Evolution, distribution and systematics of Haliotidae. In: S. A. Shepherd, M. J. Tegner & S. A. Guzman del Proo, editors. Abalone of the world. Biology, fisheries and culture, 1st ed. Cambridge: Fishing News Books. pp. 3-18.
Minkler, J. 1977. Chromosomes of the black abalone (Haliotis cracherodii). Specialia 15:1143.
Miyaki, K., M. Matsuda & O. Tabeta. 1999. Karyotype of the giant abalone, Nordotis madaka. Fisheries Sci. 65:317-318.
Miyaki, K., O. Tabeta & H. Kayano. 1997. Karyotypes of the two species of abalones Nordotis discus and N. gigantea. Fisheries Sci. 63:179-180.
Nakamura, H. K. 1985. The chromosomes of Haliotis diversicolor aquatilis (Archaeogastropoda: Haliotidae). Mal. Rev. 18:113-114.
Nakamura, H. K. 1986. Chromosomes of Archaeogastropoda (Mollusca: Prosobranchia), with some remarks on their cytotaxonomy and phylogeny. Publ. Seto. Mar. Biol. Lab. 31:191-267.
Okumura, S., S. Kinugawa, A. Fujimaki, W. Kawai, H. Maehata, K. Yoshioka, R. Yoneda & K. Yamamori. 1999. Analysis of karyotype, chromosome banding, and nucleolus organizer region of pacific abalone, Haliotis discus hannai (Archaeogastropoda:Haliotidae). J. Shellfish Res. 18:605-609.
Okumura, S., S. Yamada, T. Sugie, D. Sekimiya, A. Toda, H. Hajime, H. Hatano & K. Yamamori. 1995. C-banding Study of chromosomes in Pacific abalone Haliotis discus hannai (Archaeogastropoda: Haliotidae) Chrom Inf. Ser. 18:605-609.
Owen, B., J. H. McLean & R. J. Meyer. 1971. Hybridization in the eastern pacific abalones (Haliotis). Sci. Bull. Nat. Hist. Mus. Los Ang. Cty. 9:1-37.
Spotorno, A. E. 1985. Conceptos y metodos en cariologia descriptiva y comparada. In: R. Fernandez-Donoso, editor. El nucleo, los cromosomas y la evolucion. UNESCO, pp. 137-165.
Thiriot-Quievreux, C. 1984. Analyse comparee des caryotypes d'Ostreidae (Bivalvia). Cah. Biol. Mar. 25:407-418.
Wang, Q., Q. Ma & Y. Wang. 1988. The karyotype study of Haliotisdiscus-hannai Ino. Zool. Res. 9:171-174.
White, M. J. D. 1973. Animal cytology and evolution. Cambridge: Cambridge University Press, 3rd. ed. 961 pp.
White, M. J. D. 1978. Modes of Speciation. San Fracisco CA: W. H. Freeman. 455 pp.
NORMA K. HERNANDEZ-IBARRA, (1) CARLOS MARQUEZ, (2) JOSE L. RAMIREZ (1) AND ANA M. IBARRA (1) *
* Corresponding author: E-mail firstname.lastname@example.org
(1) Centro de Investigaciones Biologicas del Noroeste, S.C., Lab. de Genetica Acuicola A.P. 128. La Paz B.C.S., Mexico 23000; (2) Universidad Autonoma de Baja California, Facultad de Ciencias. Carr. Tijuana, Ensenada Km. 106, Ensenada B.C., Mexico 22800
|Printer friendly Cite/link Email Feedback|
|Author:||Ibarra, Ana M.|
|Publication:||Journal of Shellfish Research|
|Date:||Dec 1, 2004|
|Previous Article:||Transplanting of wild and cultivated juveniles of green abalone (Haliotis fulgens Philippi 1845): growth and survival.|
|Next Article:||A comparative evaluation of the habitat value of shellfish aquaculture gear, submerged aquatic vegetation and a non-vegetated seabed.|