873

Copan. 1991(4), pp. 873-896

Patterns of Gene Flow and Genetic Divergence in the Northeastern Pacific (Teleostei: Blennioidei), Based on Allozyme and Morphological Data

CAROLA. STEPIENAND RICHARDH. ROSENBLATT

Genetic relationships and distribution patterns among populations, subspe- cies, and species of northeastern Pacific myxodin clinids were analyzed from allozyme data. The most recent revision recognized six species and 12 subspecies in two genera, Heterostichus and . Allozymes from 40 gene loci from all 12 nominal taxa were analyzed to compare heterozygosity levels, Hardy- Weinberg equilibrium conformance, genetic distances, and phylogenetic rela- tionships. Sample sites ranged from Carmel, California, to central Baja Califor- nia, Mexico, and included areas of sympatry, disjunct distribution, and relative isolation. Offshore island sites included the California Channel, San Benito, and Guadalupe islands; the last with several endemic nominal taxa. In addition, morphological characters putatively defining closely related taxa were reex- amined because preliminary data suggested that some taxonomic separations had been made on the basis of sexually dimorphic characters and ecophenotypic variation. Most intraspecific samples shared close genetic relationship, consistent with little genetic isolation. Disjunct populations of G. montereyensis and G. metzi from north of Point Conception, California, and in areas of coldwater upwelling off northern Baja California, Mexico, respectively, are very similar. The Channel Island populations are little divergent from those of the mainland, however, the San Benito Islands population is slightly more genetically distinct. Populations of the geographically isolated Guadalupe Island are genetically divergent. Pat- terns of genetic relationships among populations may be explained by the rel- atively long larval life of clinids (up to two months), geographic continuity, and major coastal current patterns. Some allelic variation in G. elegans, G. montereyen- sis, and G. metzi also supports longitudinal clinal trends, which may suggest selection resulting from temperature. Both allozyme and morphological data failed to separate G. erythra from G. montereyensis. Gibbonsia erythra is a deepwater ecophenotype of G. montereyensis; males inhabit deeper water than females, and the supposed distinguishing char- acters are sexually dimorphic and/or depth related. Gibbonsia norae is a semi- isolated population of G. montereyensis inhabiting the San Benito and Guadalupe islands, Mexico. A new key to the northeastern Pacific Clinidae is given.

YXODIN clinids or kelpfishes are among cies of northeastern Pacific myxodins have two M the most common temperate nearshore general patterns of distribution: north (G. metzi fishes living in benthic algae along the Pacific and G. montereyensis) and south (G. elegans and coast of North America (Williams, 1954; Ste- H. rostratus) of Point Conception, California pien, 1986a; Stepien et al., 1988). According to (34.5"N, Fig. 1). A temperature boundary at C. Hubbs' (1952) revision, the group comprises Point Conception roughly separates the north- six species and 12 subspecies in two genera, Het- ern, cold temperate Oregonian biogeographic erostichus and Gibbonsia. The most abundant spe- region from the southerly warm temperate Cal-

0 1991 by the American Society of Ichthyologists and Herpetologists 874 COPEIA, 1991, NO. 4

50 120" 115" ..:. 1 I I I I I I

35

30'

2 5'

I

Fig. 1. Location of sample sites, numbered from north to south, as follows: 1 = Carmel, 2 = San Simeon, 3 = Santa Cruz Island, 4 = Santa Barbara, 5 = Santa Catalina Island, 6 = La Jolla (San Diego), 7 = Coronado Islands, 8 = Punta Clara, 9 = Guadalupe Island, 10 = San Benito Islands. Mean current flow patterns in the study area are represented (adapted from Waples and Rosenblatt, 1987 and based on data from Wyllie, 1966; Hickey, 1979; Owen, 1980; and Cowen, 1985). Consistent flow directions are shown with solid arrows: dashed arrows indicate more variable features. ifornian province (Hedgpeth, 1957; Valentine, and algae (Dawson, 1960; Abbott and Hollen- 1966; Briggs, 1974; see Table 1 for tempera- berg, 1976; Murray et al., 1980). ture comparisons). Point Conception is a dis- However, some of the northern species, in- tributional boundary for many other fishes (C. cluding the clinids G. montereyensis and G. metzi, L. Hubbs, 1960; Horn and Allen, 1978), inver- reappear in pockets of nearshore summer cold tebrates (Garth, 1960; Seapy and Littler, 1980), water upwelling off Baja California, Mexico, as STEPIEN AND ROSENBLATT-CLINID GENE FLOW AND DIVERGENCE 875

TABLE1. MEANSEASONAL TEMPERATURES(c) NEAR SOME CLINID COLLECTION SITES, SUMMARIZED FROM CALCOFI DATA 1950-78 (LYNNET AL., 1982).

Seasonal mean C A L C0 F I Depth station Location (4 Jan Apr July Oci Yearly mean 80052 Point Conception, California 0 13.66 11.95 12.76 16.07 13.61 34.5"N, 12Oo60'W 10 13.64 11.66 12.19 15.62 13.30 20 13.43 11.18 11.48 14.05 12.54 30 12.21 10.66 10.82 12.73 11.85 90028 Dana Point, California 0 14.27 15.21 19.15 18.57 16.80 33"N, 118"W 10 14.05 14.46 16.66 17.87 15.79 20 13.93 13.23 13.57 15.66 14.10 30 13.68 12.15 11.96 13.81 12.90 100030 Ensenada, Mexico 0 14.6 1 16.14 17.51 17.32 16.40 32"N, 116"30'W 10 14.49 15.99 15.03 16.23 15.44 20 14.24 15.09 13.33 14.42 14.27 30 13.84 14.28 12.10 13.40 13.43 110035 Punta Baja, El Rosario, Mexico 0 15.72 14.58 16.93 18.59 16.46 30"N, 116"W 10 15.68 14.47 16.27 18.41 16.21 20 15.48 13.92 15.14 17.86 15.60 30 15.27 13.34 14.06 16.52 14.80 1 10070 Guadalupe Island, Mexico 0 16.05 16.46 18.75 19.93 17.80 39'N, 118'45'W 10 15.96 16.38 18.51 19.84 17.67 20 15.85 16.28 18.17 19.79 17.52 30 15.79 16.17 17.72 19.66 17.34 120035 San Benito Islands, Mexico 0 16.30 15.68 18.64 20.22 17.71 28.5"N, 116"W 10 16.29 15.33 18.53 19.79 17.49 20 16.24 15.08 18.18 19.68 17.30 30 16.17 14.72 17.72 19.16 16.94 120045 Punta Eugenia, Mexico 0 16.67 15.45 18.40 20.60 17.78 28"N, 115"20'W 10 16.65 15.31 18.10 20.53 17.65 20 16.55 14.99 16.66 19.79 17.00 30 16.44 14.22 15.42 18.13 16.05

well as in deeper waters off some of the offshore at the Punta Clara upwelling site, which were islands (C. L. Hubbs, 1952, 1960; C. Hubbs, analyzed in the present study. No other site ex- 1952; Garth, 1960). This disjunct coastal dis- amined had such diversity of sympatric clinids. tribution pattern, although presumably wide- Waples and Rosenblatt (1987) and Waples spread (C. L. Hubbs, 1952; Dawson, 1960), has (1986, 1987) examined gene flow among pop- been little studied, and we do not know of other ulations of eight species of warm temperate fish- investigations that have focused on population es .having primary distributions south of Point genetics of these organisms. One of the goals Conception. Fishes from some of their study of the present study was to examine the degree areas were examined in the present study so of genetic isolation and gene flow among clinids comparisons can be made. Comparisons were having this disjunct distribution pattern. also made with other studies of population ge- Stepien et al. (199 1)recently completed a year- netics of fishes from some of these areas, in- long survey of fishes at one of the intertidal cluding the cottid Clinocottus analis (Swank, cold-water upwelling sites off northern Baja 1979), the hexagrammid Oxylebius pictus (Davis California (Punta Clara), where some species et al., 1981), the sciaenids Genyonemus lineatus characteristic of both marine provinces occur and Serzphus politus (Beckwitt, 1983), the ser- sympatrically. For example, four species of clin- ranid Paralabrax clathratus (Beckwitt, 1985), the ids (H. rostratus, G. elegans, G. metzi, and G. mon- stichaeid Anoplarchus purpurescens (Sassaman et tereyensis) were collected in the same tidepools al., 1983), the atherinid Atherinops afinis (Crab- 876 COPEIA, 1991, NO. 4

TABLE2. FORMERAND PRESENTSTATUS OF THE NORTHEASTERNPACIFIC MYXODIN CLINIDAE.

Former status (C. Hubbs, 1952) and general distribution Present status 1. H. rostratus Girard, 1854 1. Heterostichus rostratus a. H. r. rostratus Girard, 1854 a. not recognized -Baja California to Pt. Conception b. H. r. guadalupensis C. Hubbs, 1952 b. not recognized --Guadalupe Island endemic 2. G. elegans Cooper, 1864 2. a. G. e. elegans Cooper, 1864 a. not recognized -Baja Calif. to Pt. Conception, intertidal b. G. e. uelijiera C. Hubbs, 1952 b. not recognized -Baja Calif. to Pt. Conception, offshore c. G. e. erroli C. Hubbs, 1952 c. not recognized -Guadalupe Island, endemic d. G. e. rubrior C. Hubbs, 1952 d. not recognized --Guadalupe Island, endemic 3. G. metzi C. L. Hubbs, 1927 3. a. G. m. metzi C. Hubbs, 1952 a. not recognized -Pt. Conception to Alaska b. G. m. feroenter C. Hubbs, 1952 b. not recognized -Baja California to Pt. Conception 4. G. montereyensis C. L. Hubbs, 1927 4. a. G. m. monterejensis C. L. Hubbs, 1927 a. not recognized -Pt. Conception to Alaska, rough water b. G. m. vulgaris C. Hubbs, 1952 b. not recognized -Pt. Conception to Alaska, calm water 5. G. erythra C. Hubbs, 1952 5. Placed in the synonymy of G. montereyensis -Baja California to Pt. Conception, subtidal 6. G. nome C. Hubbs, 1952 6. Placed in the synonymy of G. montereyensis -Guadalupe and San Benito Islands, endemic

tree, 1986), the blenniid Hypsoblennius jenkensi (the endemic species was said to also occur at (Present, 1987),and the girellid Girella nigricans the San Benito Islands; see Table 2). At one (Orton, 1989). time, Guadalupe Island was believed to have Gene products from 40 allozyme loci of all many other endemic fishes (C. L. Hubbs and six North American myxodin chid species and Rechnitzer, 1958; C. L. Hubbs, 1960). How- 12 subspecies, as defined by C. Hubbs (1952), ever, more recent studies have shown that some were analyzed in the present study. Sample sites of these have more widespread distributions ranged along the North American Pacific coast (Greenfield and Wiley, 1968; Briggs, 1974), and from Soberanes Point, Carmel, California, to other genetic studies have suggested substantial central Baja California, Mexico, and included gene flow between some Guadalupe Island and several of the offshore islands, e.g., the Chan- mainland fish populations (other than clinids; nel, Coronado, San Benito, and Guadalupe is- Waples and Rosenblatt, 1987; Waples, 1986, lands (see Fig. 1). Sample sites represent both 1987; Orton, 1989). An objective of the present the center of the range of each species and areas study was to test whether, and to what degree, of infrequent occurrence and sympatry with re- clinid populations from Guadalupe Island are lated species. genetically distinct. Guadalupe Island, the most isolated site sam- Genetic relationships of all clinid taxa (Table pled, is 275 km west of the coast of central Baja 2) were analyzed in the present study, and some California, Mexico, and surrounded by deep of their morphological characters were also re- (>3000 m) water (Fig. 1). Several subspecies examined. C. Hubbs (1 952) divided the former and one species of clinid were described by C. G. montereyensis into three species, erecting G. Hubbs (1952) as endemic to Guadalupe Island erythra and G. norae. Gibbonsia erythra was sep- STEPIEN AND ROSENBLATT-CLINID GENE FLOW AND DIVERGENCE 877 arated from G. montereyensis on the basis of a the Scripps Institution of Oceanography (SIO) higher anterior portion of the dorsal fin and Marine Vertebrates Collection. squamation extending to the edge of the caudal Approximately equal numbers of females and peduncle (as opposed to a naked area on the males were analyzed for all populations sam- peduncle, characteristic of G. montereyensis). In- pled, excepting G. erythra (all males). Sexing was dividuals identifiable as G. erythra are most com- based on examination of whole gonads or go- mon in deeper subtidal areas south of Point nadal tissue, using a dissection microscope. Go- Conception, California. This complex .was a nadal maturities were ranked from 1 to 5, fol- particular focus of the present study because lowing Stepien (1986a), 1 being immature and preliminary examination suggested that all G. 5 being ripe. Separation of individuals of G. erythra are males. Gibbonsia norae, endemic to erythra from G. montereyensisfit C. Hubbs’ (1952) Guadalupe and the San Benito islands, Mexico, criterion based on degree of squamation on the was separated on the basis of having a smaller caudal peduncle and ratio of the height of the number of dorsal and anal-fin rays and fewer first dorsal spine (SH) to head length (HL). scale rows above the lateral line (C. Hubbs, To investigate sexual dimorphism, scale pat- 1952). terns on the caudal peduncle of G. montereyensis Many of the meristic characters utilized by C. and G. erythra were ranked from 1 to 5, ac- Hubbs (1 952) as discriminators overlap consid- cording to increasing degree of scale coverage. erably among the 12 clinid taxa. In the present Variation of these scale patterns among males study, allozymes provided a data set that was and females was tested with chi-square tests (So- analyzed separately from morphological data to kal and Rohlf, 1981). The SH, HL, standard test patterns of relationships and the delinea- length (SL), and total length (TL) were mea- tion of taxa. In addition, life-history and eco- sured, following the methods of C. Hubbs logical data for H. rostratus (Stepien, 1986a, (1952), using a dissection microscope, for a se- 1986b, 1987) and G. elegans (Williams, 1954; ries of collections of G. montereyensis and G. er- Stepien et al., 1988) showed that sexual dimor- ythra from known depths. In addition, compar- phism is common in this group and suggested isons of measurements of caudal peduncle length that some subspecies were defined on the basis (PL) : HL and SL and SH : HL and SL were of sexually dimorphic and depth-related char- made for G. elegans erroli and G. elegans rubrior acters. Sexes of North American clinids are of known depths from Guadalupe Island. All depth segregated; adult males are usually found measurements were taken prior to sexing. deeper than adult females and juveniles (Wil- liams, 1954; Stepien, 1986a, 1987; Stepien et Enzyme electrophoresis.-Separate extracts of eye, al., 1988), so that single collections are almost liver, and muscle were prepared from each spec- always skewed in sex ratio. The deep-versus- imen. Tissues were homogenized in a 1:l vol- shallow subspecies pairs described by C. Hubbs ume : volume mixture of tissue and 0.1 M po- (1952) were, thus, reexamined for sexually di- tassium phosphate grinding buffer (pH 7; Waples morphic and depth-related morphological vari- and Rosenblatt, 1987) and centrifuged at 20,000 ation, as well as tested for genetic divergence. g for 10 min. The supernatant fraction was then subjected to horizontal starch electrophoresis MATERIALSAND METHODS in 12.5% starch gels (Sigma starch; Sigma Chemical Co., St. Louis, Missouri 63178). The Species and locations analyzed.-Allozyme data enzymes and tissues surveyed, loci scored, and from all species (H. rostratus, G. elegans, G. metzi, buffer solutions used are listed in Table 3. Stain- G. montereyensis, G. erythra, and G. norae) and ing methods and recipes were adapted from Se- subspecies of North American myxodins, com- lander et al., 197 1; Waples, 1986; and Buth and prising all 12 taxa recognized by C. Hubbs Murphy, 1990. Enzyme nomenclature follows (1952), were analyzed. Our 10 collection local- recommendations of the International Union ities and general distribution patterns are given of Biochemistry (1 984). Alleles are designated in Figure 1 and Table 2, respectively. Speci- with lowercase letters. mens were collected by netting intertidally with Only 34 loci from the Guadalupe Island pop- use of the anesthetic quinaldine or subtidally by ulation of H. rostratus and loci from the Gua- scuba diving and were immediately frozen and dalupe Island population of G. elegans are in- stored at -40 C. Voucher specimens of rep- cluded because these samples were previously resentatives from all sites were deposited in analyzed by Waples (1986), who contributed tis- 878 COPEIA, 1991, NO. 4

TABLE3. LIST OF ENZYMESSURVEYED IN ELECTROPHORETICANALYSES.

Name (E.C. number) Locus Tissue' Buffer** Acid phosphatase (3.1.3.2) Acp- 1 Acp-A Aconitase hydratase (4.2.1.3) Acoh-A Adenylate kinase (2.7.4.3) Ak-A Alcohol dehydrogenase (1 .l.1.1) Adh-A Adh-B Aspartate aminotransferase (2.6.1.1) sAat-B sAat-A mAat-A Creatine kinase (2.7.3.2) Ck-B Ck-C Ck-A Esterase (3.1.1.-) Est- 1 Est-2 Est-3 Fumarate hydratase (4.2.1.2) Fumh-A Glucose-6-phosphate dehydrogenase (1.1.1.49) G6pdh-1 G6pdh-2 Glucose-6-phosphate isomerase (5.3.1.9) Gpi-A Gpi-B Glutamate dehydrogenase (1.4.1.2) Gtdh-A Glyceraldehyde-3-phosphate dehydrogenase (1.2.1.12) Gapdh-C Gapdh-A Glycerol-3-phosphate dehydrogenase (1.1.1.8) G3pdh-B L-Iditol dehydrogenase (1.1.1.14) Iddh-A Isocitrate dehydrogenase (NADP) (1.1.1.42) sIdh-A mIdh-A L-Lactate dehydrogenase (1.1.1.27) Ldh-C Ldh-A Ldh-B Malate dehydrogenase (1.1.1.37) sMdh-B sMdh-A Mannose-6-phosphate isomerase (5.3.1.8) Mpi-A Phosphoglucomutase (5.4.2.2) Pgm-A Phosphogluconate dehydrogenase (1.1.1.44) Pgdh-A Peptidase (glycyl-I-leucine) (3.4.1 1.-) Pep-A Peptidase (I-leucylglycylglycine) (3.4.1 1 .-) Pep-B Pep-3 Superoxide dismutase (1.15.1.1) sSod-A Xanthine dehydrogenase (1.1.1.204) Xdh-A

* Tissues: L = liver. M = muscle, E = eye (retina). ** Buffers: I = Trisiitric acid pH 6.9, 2 = Tris-citric acid pH 8.0, 3 = Tris-boric acid EDTA pH 8.6. 4 = Lithium hydroxide (recipes adapted from Selander et al.. 1971; Shaklee et al., 1982: Wapler, 1986; and Buth and Murphy. 1990). sue samples, fixed gels, and original scored data G6pdh-2, Iddh-A, Mpi-A, and Xdh-A for H. to this study. Condition of this frozen material rostrutus and Aat-A, Acp-1, Ck-C, Est-1, Est-2, precluded further electrophoretic work and Gapdh-C, G6pdh-1, G6pdh-2, and Iddh-A for fresh samples from Guadalupe Island could not G. eleguns. All gels and original data were re- be obtained. Gene products in these Guadalupe examined; and stains, buffers, and scoring cor- Island samples included all of the polymorphic responded to those used by Waples (1986). loci determined in the other populations of Het- erostichus and G. elegans. Loci examined includ- Data analjszs.-BIOSYS-l vers. 1.7 (Swofford ed all listed in Table 3 except Acp-1, Est-1, and Selander, 1981, 1989) was used to compute STEPIEN AND ROSENBLATT-CLINID GENE FLOW AND DIVERGENCE 879 measures of genetic variability (heterozygosity, There was some deviation (not significant; P > number of polymorphic loci, and F-statistics; 0.44) in the San Benito Islands sample of G. Wright, 1965, 1978), to quantify divergence elegans. That deviation is the result of a single among the geographic samples (contingency ta- locus (sSod-A; Tables 4, 5). Contingency table, ble analyses of heterogeneity among popula- F,, values, and genetic distances showed no sig- tions), to test conformance with Hardy-Wein- nificant temporal variation between samples an- berg equilibrium expectations (with Levene’s, alyzed by Waples (1986) and the present study. 1949 correction for small samples), and to cal- There was also no significant temporal variation culate Nei’s (1972) and modified Rogers’ (Rog- between collections made in different years from ers, 1972; Wright, 1978) genetic distances be- sample sites at La Jolla (G. elegans) and the San tween all pairwise combinations of taxa. This Benito Islands (H. rostratus and G. elegans) (see program was also used to construct distance Materials and Methods; Waples, 1986). Wagner trees (Farris, 1972), using modified Allozymic differences among all populations Rogers’ genetic distances (Wright, 1978). of all species, except for those from Guadalupe Allozyme data for G. elegans from Bird Rock, Island, are minor (Tables 5-8; Figs. 2,3). There California, were compared with data collected are greater differences in populations from by R. Waples (1982 collection unpubl.) using Guadalupe Island (Tables 5-8; Figs. 2,3),which chi-square contingency analyses (Sokal and show closest relationship to San Benito Islands Rohlf, 1981), to test for temporal variation in and other southern populations (Table 4; Fig. allelic frequencies. Collections of G. elegans, G. 2). Genetic variation between nominal subspe- metzi, G. montereyensis, and H. rostratus made in cies and species (as defined by C. Hubbs, 1952) 1986-87 and 1987-88 from San Simeon, La was tested with contingency chi-square tests Jolla, California, and Punta Clara, Mexico, were (Table 8). No significant differences were found also analyzed for temporal variation. among intraspecific populations other than those All statistical tests and distance clustering from Guadalupe Island. analyses were performed twice in the present Relationships among taxa are summarized in study, with the full data set of 40 loci for all Figures 2 and 3, which illustrate results of the populations except Guadalupe Island and again distance Wagner procedure (Farris, 1972), based with the data set of 31 loci for all populations on modified Rogers’ genetic distances (Wright, of Heterostichus and G. elegans. Analyses of mor- 1978). The tree shown in Figure 2, rooted with phological data (chi-square contingency and re- the South American myxodin vtridts, gression tests) were performed using SYSTAT has a cophenetic correlation of 0.97. Cophe- (Wilkinson, 1988). netic correlations for separate analyses of each individual species group are 0.97 for H. rostra- RESULTS tus, 0.98 for G. elegans, 0.99 for G. metzi, and 0.99 for G. montereyensis. Genotypic data for all polymorphic loci of H. All of the preserved specimens examined that rostratus, G. elegans, G. metzi, G. montereyenszs, G. fit the characters described by C. Hubbs (1952) erythra and G. norae populations are presented for G. erythra (high dorsal fin and scales ex- in Table 4. Measures of genetic variability are tending to the edge of the caudal peduncle) are given in Table 5. Modified Rogers’ (Wright, males. Of 73 specimens examined that were 1978) and Nei’s genetic distances (1972), cal- originally identified as G. erythra in the SI0 col- culated between all pairs of taxa are given in lection (and were large enough to be reliably Table 6. Mean F,, values and chi-square con- sexed), 24 did not fit the characters. Of these, tingency table comparisons of all populations 19 were females (with caudal squamation pat- per species are summarized in Table 7. Data in terns ranging from 1 to 3; see Fig. 4) and five Table 7 are grouped in analyses with and with- were males (with caudal squamation patterns out Guadalupe Island populations, because these ranked 3). Eighty-six percent (85 of 99) of iden- populations were significantly divergent. tifiable adult male G. montereyensis fit the char- Most populations of each species showed close acters of G. erythra. The remaining I4 speci- genetic relationship (Tables 5-7). Heterozy- mens had intermediate patterns of squamation gosity and percent polymorphism levels for H. ranked 3 (n = 10) and 2 (n = 4; Table 9). rostratus are somewhat higher than in species of Specimens of G. montereyensis from several lo- Gzbbonsia. All populations conformed to ex- cations had scale patterns on the caudal pedun- pected Hardy-Weinberg equilibria (P > 0.70). cle ranging from the naked area on the pedun- 880 COPEIA, 1991, NO. 4

- m- w- mw *- 0 00 00 “0 00 s 3%2% mumm 32

*P- m* m 00 mm “0mn 0 ma mm m

* w- -0- *- 0 zs “-0 5?z 3 mm 3%: mm

n r-- mm m 0 00 E0 1 m mu 0 m mm mmmu m

m- m m- *- 00 0 00 00 323 3%32

m- e- *m 00 00 00mm 3% 3% mm

nr- 00mm mm

m- w 00 0 3% 3

* w- 0 00 m mn m mm STEPIEN AND ROSENBLATT-CLINID GENE FLOW AND DIVERGENCE 88 1

< a- mm (om 4: cn- m-? -6 00 "0 E 00 -0 d 2% 2% mm d 2%1%

cn- mm 2 00 ??0 -0-0 c umumuu

5 Ln a 0; & n 882 COPEIA, 1991, NO. 4

cle characteristic of the species as described by C. Hubbs (1952) to squamation extending to the edge of the peduncle, characteristic of G. erythra (Fig. 4). In reexamining the scale pat- terns of 2 17 G. montereyensis, we found that sig- nificantly more males than females had a com- pletely scaled caudal peduncle (Table 9). There were no significant differences between ratios E-- w 5?8 $ of SH : HL (x* = 2.11, df = 1, P = 0.15) and mm m SH:SL(x'= 1.91,df= l,P=O.l7)formales (n = 102) versus females (n = 109). However, I.- I.- w there were significant increases in these ratios 00 0 71-0 u with increasing depth (Table 10). There were umu no significant differences, however, between w- w males from the 10 to 20 m and the 21 to 45 m 00 0 nn n classes. There was a significant difference be- nmn tween depth distributions of females and males (Table 11). Females dominated intertidal col- m m- 0 5?g leytions, decreasing in overall percentage with m mm increasing depth, and males were most common subtidally, increasing in overall numbers with mw depth. Genetic distances based on allozyme data nn00 among samples identified from morphology as nn G. erythra and G. montereyensis are shown in Fig- ure 3, further demonstrating that G. erythra can- wm m- ?%00 not be separated genetically from G. monterey- mm 1% ensir. Clustering reflects geographic, rather than morphotypic, relationships. f-w Reexamination of the characters distinguish- 00mm mm ing the Guadalupe Island endemic subspecies G. elegans erroli and G. elegans rubrior (purport- : : P- m- edly differences in SH HL and PL HL ratios; 0 00 C. Hubbs, 1952), from 103 specimens (38 fe- n nn n nm males and 65 males) of known collection depths yielded similar results. Ratios of SH : HL and P-w 00 SH : SL were significantly greater in males than 11 in females (x' = 4.94, df = 1, P = 0.026 and xz = 5.92, df = 1, P = 0.0 15, respectively). There r-- mm was also a significant increase in SH : SL ratio 00 00 with depth class for females (xz = 6.7 1, df = 2, 23 23 P = 0.035) and a less significant increase in this ratio with depth for males (x' = 2.96, df = 1, am m- 00 00 P = 0.85). The holotype and three paratypes of 1%2% G. elegans rubrior are all males and all have in- termediate SH : HL and SH : SL ratios not sig- nificantly different from the mean of males in the population (Mean spine height: SL = 1.44, SD = 0.15, SE = 0.02 for males and SL = 1.35, SD = 0.22, SE = 0.04 for females). There were no significant differences between the sexes in PL : HL or PL : SL ratios (x' = 0.40, df = 1, P = 0.84 and x2 = 0.81, df = 1, P = 0.78, re- spectively). Measures of PL : HL and PL: SL are directly correlated, and there is no evidence supporting C. Hubbs' (1 952) supposition of bi- STEPIEN AND ROSENBLATT-CLINID GENE FLOW AND DIVERGENCE 883

TABLE5. HETEROZYGOSITYAND POLYMORPHISMVALUES FOR POPULATIONSOF NORTHEASTERNPACIFIC CLINIDS.

Pk Polymorphism Mean number of alleles Species Population Mean H wr locus Der locus Direct count 0.95 Criterion H. rostratus Catalina Island 0.07 + 0.02 1.25 + 0.07 25.00 25.00 San Diego 0.07 + 0.02 1.30 + 0.09 25.00 22.50 Punta Clara 0.07 + 0.03 1.20 + 0.06 20.00 20.00 San Benito Islands 0.05 + 0.02 1.23 + 0.07 22.50 22.50 Guadalupe Island* 0.01 + 0.01 1.04 + 0.04 03.57 03.57 G. elegans San Simeon 0.03 + 0.02 1.10 + 0.05 10.00 10.00 Santa Barbara 0.02 + 0.01 1.15 + 0.07 12.50 12.50 Santa Cruz Island 0.02 + 0.01 1.08 + 0.04 07.50 07.50 Catalina Island 0.03 + 0.01 1.20 + 0.07 17.50 17.50 San Diego 0.04 + 0.01 1.42 + 0.12 30.00 12.50 Coronado Islands 0.03 + 0.01 1.12 + 0.05 12.50 12.50 Punta Clara 0.03 + 0.01 1.20 + 0.07 17.50 17.50 San Benito Islands 0.02 + 0.01 1.23 + 0.08 17.50 12.50 Guadalupe Island** 0.04 + 0.02 1.21 + 0.08 21.43 07.14 G. metzi Carmel 0.04 + 0.01 1.27 + 0.09 22.50 15.00 San Simeon 0.03 + 0.01 1.38 + 0.11 27.50 12.50 Punta Clara 0.04 + 0.01 1.32 + 0.09 27.50 20.00 G. montereyensis Carmel 0.03 + 0.01 1.17 + 0.06 17.50 17.50 San Simeon 0.04 + 0.01 1.27 + 0.08 25.00 15.00 Santa Barbara 0.03 + 0.02 1.10 + 0.05 10.00 10.00 Punta Clara 0.03 + 0.01 1.23 + 0.07 22.50 15.00 G. erythra*** San Simeon 0.03 + 0.01 1.15 + 0.06 15.00 15.00 Coronado Islands 0.04 + 0.02 1.12 + 0.05 12.50 12.50 G. norue*** Guadalupe Island 0.04 + 0.02 1.23 + 0.08 20.00 17.50

= Allozvme data collected from 34 loci. ** = Allozyme data collected from 3 1 loci. *** = Placed in the synonymy of G. montzrqvnsrr modality (the regression equation is PL = O.l(SL) 1987), including G. metzi (Somero and SoulC, - 1.0; RZ= 0.94, F = 1664, df = 1,101, P < 1974) and species of the labrisomid Neoclinus 0.0001). Ratios of PL : HL and PL : SL of the (Fukao and Okazaki, 1987). The Guadalupe Is- holotype and paratypes of G. elegans rubrior are land sample of Heterostichus had significantly not significantly different from the mean of the lower mean heterozygosity and polymorphism population (Mean = 0.841, SD = 0.076, SE = levels than the other populations. This may sug- 0.007). There was a significant difference be- gest a genetic bottleneck, either by an original tween proportions of males versus females at colonization by a few individuals (founder ef- various depths; only females were collected in- fect) or a reduction in population in the rela- tertidally, and males were more common than tively recent past (Holgate, 1966; Nei et al., females in subtidal waters (Table 11). All fe- 1975; Chakraborty and Nei, 1977). Alterna- males collected subtidally were ripe, having go- tively, lower heterozygosity may be a result of nadal maturities ranked 4 or 5. selection. Giant (Macrocystis integrfolia), which is one of the major habitats of Heterostz- DISCUSSION chus (Stepien, 1986a, 1986b, 1987), is not pres- ent at Guadalupe Island (C. L. Hubbs, 1960), Population relationships based on allozyme data.- and the observed difference in genetic vari- Mean heterozygosity levels (direct count) for ability may be associated with habitat. It is pos- chid populations (Table 5) approximate pre- sible that this low heterozygosity and polymor- vious estimates from allozyme data fur other phism may be an artifact of small sample size. marine fishes (Winans, 1980; Kirpichnikov, In contrast, Guadalupe Island populations of G. 1981; Beckwitt, 1983; Waples and Rosenblatt, elegans and G. montereyensis have high hetero- 884 COPEIA, 199 1, NO. 4

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d d d STEPIEN AND ROSENBLATT-CLINID GENE FLOW AND DIVERGENCE 885

Heferosfichus rosfrafus Catalina Island

Guadalupe Island San Diego 6 Punta ~~ara Catalina bland Santa Cruz Island

ISanBenito Islands Guadalupe Island

San Simeon

-Camel 1Gibbonsia qSan~~~g,,bara monfereyensis Punta Clara --CCoronado Islands -Guadalupe Island

I", ~"~"'1''It'/ 0.00 0.10 0.20 0.30 GENETIC DISTANCE Fig. 2. Distance Wagner tree, illustrating relationships among clinid species and populations and showing relative genetic distances (add lengths of horizontal branches for genetic distances among taxa), rooted to the South American myxodin clinid Myxodes viridis. zygosity and polymorphism levels in compari- netic divergence among most clinid popula- son to other populations and show some genetic tions, excepting that from Guadalupe Island. divergence but no suggestion of recent bottle- Waples (1986, 1987) and Waples and Rosen- necks. blatt (1987) also found close genetic relation- Orton (1 989), in the girellid Girella nigricans, ships between populations of several fishes from found slightly greater genetic distances be- some of the same areas, including the Channel tween Guadalupe Island and mainland popu- Islands, San Diego, Punta Eugenia-San Benito lations than among mainland populations. This Islands, and Guadalupe Island; and Beckwitt was largely a result of the presence of a unique (1 983) found little variation between popula- allele at the sSod-A locus in the Guadalupe Is- tions of three fish species in the southern Cal- land population. ifornia bight. However, Present (1987) found a Genetic distances (Table 6) and Wagner clus- significant allelic frequency difference between tering relationships (Figs. 2, 3) show little ge- populations of the blenny Hypsoblennius jenkinsi

TABLE7. SUMMARYOF F-STATISTICSAND CHI-SQUARECONTINGENCY TESTS FOR ALLELICVARIATION AMONG CLINIDPOPULATIONS, WITH AND WITHOUT GUADALUPEISLAND SAMPLES.

Contingency comparisons Mean Species and populations surveyed 'ST Chi-square df P H. rostratus Without Guadalupe 0.02 29.83 39 >OB55 With Guadalupe 0.07 5 1 .OO 52 >0.513 G. elegans Without Guadalupe 0.05 116.39 140 >0.927 With Guadalupe 0.13 200.44 52 <0.005* G. metzi 0.01 29.42 32 >0.598 G. montereyensis Without Guadalupe 0.04 39.02 60 >0.984 With Guadalupe 0.15 143.30 84 <0.001*

* = Significant deviation in frequencies of polymorphic alleles between populations based on chi-square contingency tests. 886 COPEIA, 1991, NO. 4

C. mnonlrrrycnris Carmcl

C. ntonterryenrir San Slmcon C. monlerryenrris Santa Barbara

C. monterryenris Punta Clara C. rrylhra Coronado Islands C. IOI~C Cuadalupe Island

,I'~'~II 0.00 0.05 0.10 0.15 GENETIC DISTANCE Fig. 3. Distance Wagner tree illustrating relation- ships among populations of G. montereyensis, G. norae, and G. erythra and showing relative genetic distances Fig. 4. Drawings of scale patterns on the caudal (add lengths of horizontal branches for genetic dis- peduncle of G. erythra and G. montereyensis. Patterns tances among taxa), rooted to G. metzi. are ranked from 1 to 5, according to extent of squa- mation (see Materials and Methods). Scales extend along the body to the point designated on the pe- from two southern California locations, Scripps duncle. Significant differences between male versus Pier (La Jolla) and San Diego Bay (separated by female scale patterns are shown in Table 9. approximately 25 km), which was attributed to possible differences in local selection. Swank (1979) found greater genetic distances hexagrammid Oxylebius pictus north versus south separating populations of the cottid Clinocottus of Point Conception (ranging from 0.005 to analis north and south of Point Conception 0.034) that were somewhat greater than those (ranging from 0.006 to 0.044) than were found in the present study. This was largely because in the present study. The predominant allele at of the presence of two unique alleles at separate the Pgm-A locus in the centra1,California pop- loci; one south and one north of Point Concep- ulations was abruptly replaced by an alternate tion. Swank (1979) and Davis et al. (1982) found allele that predominated in the mainland pop- greater allelic divergences between localities ulations of southern California and Baja Cali- north and south of Point Conception than were fornia. Davis et al. (1981) found Nei's (1972) found for G. elegans, G. montereyensis, and G. genetic distances separating populations of the metzi in the present study.

TABLE8. CONTINGENCYCOMPARISONS OF ALLELE FREQUENCIES AND NEI'S (1972) GENETICDISTANCES AMONG SUBSPECIESAND CLOSELYRELATED SPECIES.

Genetic Chi-square distance Taxon A and location Taxon B and location D X' df P H. rostratus guadalupensis H. rostratus rostratus 0.008 11.94 9 >0.217 Guadalupe Island San Benito Islands G. elegans veltfera G. elegans elegans 0.000 16.09 10 >0.097 La Jolla La Jolla G elegans erroli G. elegans elegans 0.0 12 7.44 17 >0.977 Guadalupe Island San Benito Islands G. metzi ferventer G. metri metzi 0.00 1 29.42 32 >0.597 Punta Clara San Simeon G. montereyenszs montereyensis G. montereyensis vulgaris 0.000 3.72 11 >0.978 Carmel San Simeon G. erythra G. monterejensis 0.000 3.28 11 >0.987 San Simeon San Simeon G. erythra G. monferejensis 0.001 2.13 9 >0.989 Coronado Islands Punta Clara G. norae G. monterejrnsis 0.0 18 43.21 12 <0.001 Guadalupe Island Punta Clara STEPIEN AND ROSENBLATT-CLINID GENE FLOW AND DIVERGENCE 887

TABLE9. CONTINGENCYTEST COMPARISONS OF SCALEPATTERN DISTRIBUTIONS (FIG. 3) AMONG MALEAND FEMALEGibbonsia monkreyensis.

Scale pattern Chi-square contingency test Sex Number I 2 5 4 5 X' df P Males 99 00 04 10 36 49 Females 118 08 57 42 11 00 135.41 4 <0.0005 217 08 61 52 47 49

Sassaman et al. (1983) found that Ldh-A in tant from each other than either is from the populations of the stichaeid Anoplarchus pur- San Diego sample, reflecting geographic prox- purescens ranging from Monterey Bay, Califor- imities. Close genetic relationships and little iso- nia, through Alaska exhibited a longitudinal lation of Channel Island populations from those clinal trend, which was persistent throughout of the mainland were also found by Waples 10 years of sampling. They concluded that sta- (1986, 1987) and Waples and Rosenblatt (1987). bility of geographical differences in allele fre- However, Swank (1979) found the Catalina Is- quency despite presumptive indications of ex- land population of the cottid Clinocottus analis tensive larval movement between sites suggested to be closer in genetic distance to populations that selection, rather than isolation, was the north of Point Conception than to the southern prime force promoting this local differentia- California mainland. Orton (1989) found a sig- tion. There is some evidence supporting lon- nificant difference in frequencies of one allele gitudinal clinal allelic variation in the present between populations of Girella nzgricans from study for G. elegans, G. montereyensis, and G. metzi Santa Catalina Island and the mainland, al- (Table 6). though it is possible that this may be an artifact Heterostichus rostratus from Santa Catalina Is- of sample size (n = 8 for the Santa Catalina land, San Diego, and Punta Clara have close Island population). Crabtree (1 986) also found genetic relationships; Santa Catalina and Puma some genetic differences between populations Clara samples are slightly more genetically dis- of the atherinid Atherinops afinis from Santa

TABLE10. CONTINGENCYTEST COMPARISONS OF FIRST DORSAL SPINE HEIGHT : SL AND SH : HL FOR Gibbonsia montereyensis FROM VARIOUSDEPTH CLASSES.

Depth class 0-3 m 4-10 m 11-20 m 21-45 m

A. Spine height: head length Number sampled 87 78 16 30 Mean 0.53 0.54 0.62 0.57 Standard deviation 0.07 0.08 0.09 0.1 1 Standard error 0.01 0.01 0.02 0.02 Chi-square 10.43 Degrees of freedom 3 Probability <0.001 B. Spine height :standard length Number sampled 87 78 16 30 Mean 1.15 1.26 1.34 1.31 Standard deviation 0.12 0.19 0.17 0.22 Standard error 0.01 0.02 0.04 0.04 Chi-square 23.03 Degrees of freedom 3 Probability <0.001 888 COPEIA, 1991, NO. 4

TABLE1 1. CONTINGENCYTEST COMPARISONS OF NUMBEROF MALEVERSUS FEMALEGibbonsia montereyensis AND GUADALUPEISLAND Gibbonsia elegans COLLECTEDAT VARIOUSDEPTHS.

Depth class 0-3 m 4-10 m 11-20 m 21-45 m A. Gibbonsta montprejensis Number of females 75 22 06 06 Number of males 12 56 10 24 7 otals 87 78 16 30 Chi-square 72.09 Degrees of freedom 3 Probability ~0.0001 B. Gzbbonsta ~legans(Guadalupe Island population) Number of females 07 25 06 - Number of males 00 42 23 - Totals 07 67 28 - Chi-square 15.25 Degrees of freedom 2 Probability <0.001

Catalina Island and the mainland. The Santa rings) to be three years old. It is possible that Catalina Island population was most similar to they were recruited from larvae transported the population sampled from Cedros Island, Baja north during the 1982 to 1983 El Niiio. Our California, Mexico (which is near San Benito sampling, as well as that by others from this area Islands), largely because of lack of a single gene (in the SI0 collection records), indicate that G. product at a single locus. elegans is relatively rare north of Point Concep- The San Benito Islands population of Heter- tion. ostichus is closest in genetic distance to that of Our data also are consistent with high levels Santa Catalina Island, which appears to be sim- of gene flow among all populations of G. elegans ilar to Crabtree’s (1986) findings for Atherinops sampled, with genetic relationships largely re- a8nis. Waples and Rosenblatt (1987) also found flecting geographic proximity (Table 6; Figs. 2, ‘ that San Benito Islands-Punta Eugenia fish pop- 3). The data also suggest some north to south ulations are more genetically different than clinal variation. For example, the “c” allele for those from northern sites and that in most spe- the sAcoh-A locus is absent from the four north- cies the closest relationship was to Santa Cata- erly population samples and increases in fre- lina Island samples, the remainder to La Jolla quency southward from its appearance in the (San Diego) samples. La Jolla sample. The “b” allele for Est-3 follows Heterostichus from Guadalupe Island are ge- a similar pattern, increasing in frequency south- netically separable from other populations, and ward from its appearance in the Santa Catalina their closest relationship is to the San Benito Island sample. There are also two cases of ap- Islands population. For example, both the Gua- parent allelic absence at geographic extremes. dalupe and San Benito populations uniquely The “b” allele of sMdh-B is absent from the share the losses of the “a” allele at the Acp-A two northernmost populations (San Simeon and locus and the “a” allele at the Ldh-B locus. These Santa Cruz Island) and the two southernmost results are similar to relationships between San populations (San Benito and Guadalupe Islands) Benito and Guadalupe Island populations for sampled, and the “b” allele at the sAcoh-A locus the labrisomid Alloclinus holderi determined by is absent from the three northernmost popu- Waples and Rosenblatt (1987). lations (San Simeon, Santa Cruz Island, and Individuals of G. elegans from San Simeon Santa Barbara), as well as from the San Benito were collected north of their primary range in and Guadalupe islands populations. The “d” Oct. 1986, and were determined (using otolith allele at the Acp-A locus is present only in the STEPIEN AND ROSENBLATT-CLINID GENE FLOW AND DIVERGENCE 889 northernmost populations sampled south of endemic to Guadalupe Island and San Benito Point Conception (Santa Cruz Island, Santa Islands, show genetic separation comparable to Catalina Island, and La Jolla; Table 4). that found in G. elegans and H. rostratus. These Genetic distance data suggest that the San results, together with the paucity of morpho- Benito Islands population is little divergent from logical characters delimiting G. norae (see next the other samples, excepting Guadalupe Island. section on morphological variation), suggest that However, the San Benito population is closer it should be at most a subspecies of G. monte- in genetic distance to that of Guadalupe Island reyensis. than are the other populations, as is the case in Genetic distances separating the Guadalupe Heterostichus. Guadalupe Island populations of Island populations of all three clinid species are G. elegans and Heterostichus are greater in genetic comparable to those separating other semiiso- distance from other sites but show closer rela- lated fish populations (Vawter et al., 1980; Wa- tionship to southern than northern populations. ples, 1986, 1987; Waples and Rosenblatt, 1987; Populations of G. metzi north of Point Con- Grant and Stahl, 1988). These genetic distances ception and in the coldwater upwelling site at (as well as data on morphological variation; see Punta Clara (off Baja California) are close in next section) are considerably less than those genetic distance (Table 6; Fig. 2). This species separating congeneric clinid (Stepien, 1992; see has a somewhat disjunct distribution pattern be- Fig. 2) and labrisomid species (Fukao and Oka- cause it is rare off coastal southern California zaki, 1987; Stepien, 1992). Additionally, Thorpe and the offshore islands, reappearing in large (1 983), utilizing 900 congeneric species com- numbers in these cold water upwelling areas off parisons, noted that only some 2% have Nei’s Baja California (C. Hubbs, 1952; Stepien et al., (1972) D values below 0.16 and only 0.5% below 1991). C. Hubbs (1952) considered the popu- 0.1. lations of G. metzi north and south of Point Con- There is additional support for north-south ception to be subspecifically different. Genetic clinal trends in allelic frequencies in populations distances in the present study suggest that this of G. montereyensis (including G. erythra and G. separation is unjustified because even the widely monterqrensis). The frequency of the “d” allele separated areas sampled in the present study at the Acp-B locus increases significantly from show little appreciable genetic divergence. north to south, with greatest frequency at Gua- There is some allelic variation between the dis- dalupe Island. There are similar southward in- junct populations: notably absence of three al- creases in the frequencies of the “b” allele at leles in the Punta Clara sample that are present the Fum-A locus and the “c” allele at the north of Point Conception; the “c” allele at the G3pdh-B locus. There is a unique “d” allele Gpi-A locus; the “d” allele at the sMdh-B locus; present at the G3pdh-B locus in the Guadalupe and the “a” allele at the PepB locus. The Punta Island population. Clara population also has a “b” allele at the As in the other clinids, the Guadalupe Island Pep-B locus that is absent from samples north population of G. montereyensis norae shows closer of Point Conception. However, this variation in genetic relationship to southern populations rare alleles, which may reflect clinal differences, than to those north of Point Conception. Un- and the close genetic distance between them, fortunately, samples of G. m. norae from the San indicates that they should not be subspecifically Benito Islands were not obtained in the present separated. study. Waples (1986, 1987) and Waples and Ro- Samples of G. montereyensis north of Point senblatt (1987) found that six out of eight spe- Conception and in the Punta Clara upwelling cies of Guadalupe Island fishes (other than clin- site show also close genetic relationship, consis- ids) were closer in genetic relationship to tent with apparent high levels of gene flow (Ta- populations from the Channel Islands and La ble 6; Figs. 2, 3). Samples fitting the characters Jolla than to those of the San Benito Islands. of the nominal G. erythra described by C. Hubbs Populations of several fishes from San Benito (1952) cannot be separated genetically from G. Islands and Punta Eugenia, Baja California montereyensis (Fig. 3), indicating that G. erythra (pooled by Waples and Rosenblatt), showed al- should be placed in the synonymy of G. monte- most as much genetic isolation from northern reyensis. These results are further supported by populations as did those from Guadalupe Is- morphological data, as discussed in the next sec- land. Relationships of chid populations from tion. Guadalupe Island samples of the nominal these areas are consistent with those deter- species G. norae, erected by C. Hubbs (1952) as mined by Waples (1987) and Waples and Ro- 890 COPEIA, 1991, NO. 4 senblatt (1987) for the labrisomid Alloclinus Northeastern Pacific myxodin clinids are sex- holderi and the labrid Semicossyphus pulcher. ually dimorphic in size; adult females are larger Mean F,, values for each species (Table 7) than males at given ages and attain greater indicate little overall genetic variation among lengths (Stepien, 1968a, 1987; Stepicen et al., populations of H. rostratus and G. metzi and mod- 1988). Such size dimorphism was previously erate variation among those of G. elegans and suggested by C. Hubbs (1952) for G. metzi and G. montereyensis, when Guadalupe Island popu- occurs in all species examined in the present lations are not included (according to genetic study. divergence levels specified by Wright, 1978, and In addition, there is sexual dichromatism in Hart1 and Clark, 1989). With inclusion of Gua- Heterostichus rostratus (color morphs; Stepien, dalupe Island, Heterostichus and G. elegans ex- 1986b, 1987) and G. elegans (belly color; Stepien hibit moderate levels of variation and G. mon- et al., 1988). Deepwater male G. elegans (des- tereyensis (including G. montereyensis norae) ignated as G. elegans uelijera and G. elegans borders on moderate to great genetic variation. rubrior by C. Hubbs, 1952) and G. montereyensis Chi-square tests (Tables 7, 8) show no signifi- (designated as G. erythra) have distinctive red or cant differences in overall frequencies of poly- red-brown color patterns with prominent ocelli morphic alleles among populations of all species on the body above the lateral line (C. Hubbs, and subspecies, when Guadalupe Island popu- 1952; Stepien, unpubl.). Their color matches lations are excluded. However, there are sig- the red algae among which they live and guard nificant differences in overall allelic frequencies nests. Females and juveniles in shallower areas among populations of G. elegans and G. monte- occur in a variety of red, green, and brown color reyensis when Guadalupe Island populations are patterns, which also match their algal habitats included. The following loci vary significantly: (Stepien et al., 1988). Some of these variations sAcoh-A and Gpi-A in G. elegans and Acp-2 and in color pattern were considered by C. Hubbs Gpi-B in G. montereyensis. (1952) to characterize various subspecies. Re- sults of the present study suggest that color pat- Morphological variation.-C. Hubbs’ (1 952) anal- tern variation within taxa (red and red-brown ysis of the northeastern Pacific myxodin clinids colors of deepwater specimens of G. elegans er- was based on meristic data, body proportions, ythra, G. elegans rubrior, and G. erythra) is cor- and combinations of meristic counts, many of related with depth and algal habitat and, in some which overlap considerably among groups and cases, sex. show depth-related variation. In examining pre- C. Hubbs (1952) divided G. metzi into two served clinids and samples collected for allo- subspecies, G. m. metzi north, and G. m. feruenter zyme data, we found almost all clinid samples south, of Point Conception on the basis of slight to be biased in sex ratio, being either mostly differences in lengths of the caudal peduncle adult males (samples from subtidal waters) or and first anal soft ray, stating, “When these two females and juveniles (intertidal samples; see measurements are added and their proportion Table 11). This pattern of depth segregation to the standard length plotted, their standard by sex has been previously described for G. ele- deviations scarcely overlap.” Allozyme data are gans (Williams, 1954; Stepien et al., 1988; data consistent with the hypothesis of extensive gene from the Guadalupe Island population exam- flow between these widely separated popula- ined in the present study are summarized in tions (central California versus Baja California, Table 11) andH. rostratus(Stepien, 1986a, 1987). Mexico; see Fig. 2) and do not substantiate sub- The same pattern occurs in G. metzi and G. mon- species designation. tereyensis (Table 1 l), according to material ex- Shallow and deepwater populations of G. ele- amined in the present study, as well as in the gans were separated as the subspecies G. elegans South American myxodin clinid Myxodes viridis elegans and G. elegans uelifera, which differed (Stepien, 1990). Mature female myxodin clinids slightly in relative proportions of SH : HL and (e.g.,. H. rostratus) briefly migrate to male ter- body depth : SL, but not in any meristic char- ritories in deeper water during the spring acters (C. Hubbs, 1952). Williams (1954) ex- spawning season to lay eggs in algal nests, which amined 777 specimens of G. elegans from vari- the males guard until hatching (Stepien, 1986a, ous depths and found significant differences in 1987). If morphological variation between pop- sex ratio between shallow and deepwater col- ulations and taxa is to be analyzed, depth seg- lections (primarily females in the former and a regation of the sexes necessitates sexing of all greater number of males in the latter). Williams’ chid material, as was done in the present study. data showed that morphological differences dis- STEPIEN AND ROSENBLATT-CLINID GENE FLOW AND DIVERGENCE 891

tinguishing G. elegans elegans and G. elegans ve- with those of other populations and are closest li&era were gradual changes resulting from depth- to the San Benito Islands and central Baja Cal- related phenotypic variation. He concluded that ifornia populations (C. Hubbs, 1952). A possible differences in sex ratio and morphological in- exception is the reduced number of scale rows tergradiation between the two forms indicated above the lateral line in G. norae (samples pooled that they represent a single population. In the from San Benito and Guadalupe islands), which present study, contingency chi-square tests does not overlap those of G. montereyensis ex- showed no significant allelic variation between amined by C. Hubbs (1952). However, this lack deep water G. elegans velgera (all males) and shal- of overlap may be an artifact of sampling, be- low G. elegans elegans (both males and females; cause C. Hubbs (1952) did not include any sam- La Jolla sample sites; see Table 8), further cor- ples from the mainland south of Ensenada. roborating Williams’ conclusions. C. Hubbs named two subspecies of G. monte- C. Hubbs (1952) also described two Guada- reyensis from areas of high wave action (G. m. lupe Island subspecies, G. elegans erroli and G. montereyensis) and lesser wave action (G. m. vul- elegans rubrior, as differing from each other in garis), the latter being more common and widely the same body proportions purportedly distin- distributed. These subspecies were distin- guishing G. elegans velijera from G. elegans ele- guished on the basis of overlapping differences guns. Gibbonsia elegans rubrior was described from in relative height of SH and eye diameter. They four specimens (the holotype and paratypes; were not separated by any meristic characters. which were examined in the present study and Specimens from the Soberanes Point, Carmel found to be males); we were not able to obtain site were identified as G. m. montereyensis, pur- any for allozyme work. Allozyme data were an- portedly found only on the Monterey Peninsula alyzed from six intertidal specimens identified and at Port Buchon (C. Hubbs, 1952). All other as G. elegans erroli. Examination of morpholog- populations corresponded to G. m. vulgaris. Our ical characters from preserved material dem- examinations of preserved material show that onstrated that proportional differences suppos- SH is correlated with depth (Table lo), as in G. edly distinguishing G. elegans erroli from G. $rguns (Williams, 1954). Allozyme data show no elegans rubrior are also a result of sexual dimor- genetic differences between these subspecies phism and depth-related variation. (Tables 4,6, 8; Figs. 2, 3), and the proportional C. Hubbs (1952) found that the Guadalupe differences appear nominal and a result of eco- Island population of G. elegans differed from logical variation. those of the mainland by having fewer dorsal Gibbonsia norae, endemic to San Benito and spines (31 to 33 versus 32 to 35), as well as in Guadalupe islands, was separated from G. mon- some body proportions. The Guadalupe pop- tereyensis by C. Hubbs (1952) on the basis of a ulation was regarded as most similar in mor- smaller number of scale rows above the lateral phology to that of the San Benito Islands, which line and fewer dorsal and anal-fin rays. The have similar temperatures (Table 1). These former character is the only one distinguishing population relationships are mirrored by results G. norae, because the others show extensive of the present study based on allozyme data overlap. Lower meristic counts in the San Be- (Table 6; Fig. 2). Allozyme data, sex differences nito and Guadalupe islands populations are in depth distribution, and morphological evi- common to all three clinid species and may be dence suggest that subspecies of G. elegans need a result of their more rapid development in not be recognized. warmer water (Barlow, 1961). Lack of morpho- Guadalupe Island samples of all three species logical characters distinguishing G. norae from (Heterostichus, G. elegans, and G. montereyensis) G. montereyensis, absence of fixed allelic differ- have somewhat reduced meristic counts, nota- ences, and the relatively small genetic distance bly number of fin rays, and this is probably re- separating them (which is comparable to those lated to warmer temperatures (Lynn et al., 1982; seen in other Guadalupe Island clinids) indi- Table 1). Many other fishes exhibit tempera- cates that species-level separation is unwarrant- ture-related variation in meristics, such as fin ed. We, thus, suggest that G. norue be placed in ray counts, which are reduced in warmer waters the synonymy of G. montereyensis. (C. L. Hubbs, 1926; Barlow, 1961). The lower Gibbonsia erythra was said to be found pri- counts are correlated with more rapid devel- marily in deeper habitats along southern Cali- opment at these temperatures and are, thus, not fornia, the Channel Islands, and northern Baja usually genetic. In all cases except one, the Gua- California, Mexico (C. Hubbs, 1952). The spe- dalupe Island meristic counts broadly overlap cies was separated from G. montereyensis on the 892 COPEIA, 1991, NO. 4 basis of scales extending to the edge of the cau- soft rays; often 2 or more ocelli on the body dal peduncle (as opposed to a naked area on the above the lateral line 3 peduncle characteristic of G. montereyensis) and 3A. Scales extending well onto caudal rays in both a higher SH. In all but one of the records from sexes ....- G. elegans 3B. No (or very few) scales on caudal fin; females the SI0 and Los Angeles County Museum often with a scaleless gap on the caudal pe- (LACM) collections in which more than one duncle ...... G. montereyensis specimen was collected (n = 6), G. erythra were collected sympatrically with G. montereyensis. We found that all G. erythra (fitting the characters Patterns of geneflow and distribution.-Patterns of given by C. Hubbs, 1952) are males. Addition- genetic relationships among populations of all ally, 86% of male G. monterepsis fit the defi- four clinid species may reflect similarities in their nition of G. erjthra. We examined caudal pe- life histories, length of larval phase, dispersal duncle squamation in 2 17 adult G. monterejensis patterns, and/or selective forces. Stepien from these collections and the fresh material (1 986a) found larvae of Heterostichus to be used in the present study. The amount of squa- planktonic for approximately two months, and mation on the caudal peduncle in G. monterej- species of Gibbonsia appear to share that length ensis varies extensively, ranging from C. Hubbs’ of larval life (Stepien, unpubl.). Larval collec- (1952) drawing of the pattern characteristic of tion data show that clinids are sometimes col- G. erjthra to that of G. monterejensis. However, lected some distance offshore throughout the patterns of few individuals fit either of these southern California bight (G. Moser and G. extremes. Scales usually extend further along McGowen, pers. comm.; Stepien, unpubl.), and the sides of the peduncle and in the center (Fig. the species may, thus, be capable of long dis- 4). Our results show that extent of the naked tance dispersal. In addition, adults andjuveniles area on the peduncle is correlated with sex (Ta- have been found rafting offshore in pieces of ble g), females having a significantly lesser de- drift algae (Stepien, unpubl.). This capacity for gree of squamation than do males. This differ- dispersal may account for the apparent high ence was apparent in the smallest specimens. levels of genetic uniformity found among clinid Allozyme data in the present study demonstrate populations. that there is no genetic divergence between G. In the present study, disjunct populations of rrjthra and G. montereyensis (Tables 4, 6;Fig. 3). the cooler-water species, G. metzi and G. mon- Height of the anterior portion of the dorsal tereyensis showed surprisingly little genetic di- fin in the nominal G. erythra, as in the nominal vergence considering the distance between the G. elegans uelijera (Williams, 1954), G. elegans sites north of Point Conception and at the Punta rubrior, and G. montereyensis vulgaris, is positively Clara, Baja California upwelling site. South of correlated with depth and characteristic of deep Point Conception, these species are found in water male-dominated samples. Results of the cold water locations such as the upwelling areas present study suggest that G. erythra and G. norue of northern Baja California, as well as subtidally should be placed in the synonymy of G. monte- off the mainland and some of the Channel Is- reyensis (see Table 2). The following key distin- lands (C. Hubbs, 1952; Stepien et al., 1991). guishes the northeastern Pacific clinid species: The combination of long planktonic larval life and coastal current patterns (Fig. 1) may also serve to transport them long distances before KEY TO THE NORTHEASTERN settlement, maintaining high levels of gene flow. PACIFICCLINIDAE Patterns of genetic relationships among pop- ulations of all species corresponded to geo- 1A. Caudal fin forked; snout sharply pointed; graphic proximities. Presumed gene flow pat- more than 30 anal soft rays; 11 or more dor- terns also appear related to the major offshore sal soft rays ...... H. rostratzrs currents (Fig. l), which probably serve as ave- 1 B. Caudal fin slightly rounded; snout not sharp- nues of larval transport. For example, the Chan- ly pointed; fewer than 30 anal soft rays; 10 nel Islands are little divergent from mainland or fewer dorsal soft rays ...... 2 2A. Dorsal soft rays relatively evenly spaced; 7 to populations, as found in other studies of fishes 10 dorsal soft rays; ocelli on the body above by Waples (1986, 1987) and Waples and Ro- the lateral line either small or absent ..... G. metzi senblatt (1 987). Similarly, populations of G. ele- 2B. Posterior dorsal soft rays markedly more guns and G. montereyensis from the Coronado widely spaced than anterior rays; 4 to 8 dorsal Islands off northern Baja California are genet- STEPIEN AND ROSENBLATT-CLINID GENE FLOW AND DIVERGENCE 893 ically close to Punta Clara and San Diego pop- among all areas sampled (except Guadalupe Is- ulations. Among populations of G. eleguns, one land), including the disjunct populations of the of the closest genetic relationships is between former group, which appears to reflect their Santa Catalina and Santa Cruz islands, which high capacity for dispersal. The geographic iso- are linked by the offshore eddy pattern shown lation of Guadalupe Island accounts for the ge- in Figure 1. In contrast to our findings, Hal- netic divergence of its chidpopulations. There dorson (1 980) found significant variation in gene is also some evidence supporting north-south frequencies between Santa Cruz Island and clinal geographic variation, which may suggest mainland populations of two species of surf- temperature-related selection. perches (Embiotocidae), which may be linked to their viviparity and consequent reduced va- gility. Our results suggest that populations from the San Benito Islands are only slightly diver- MATERIALEXAMINED gent from mainland populations, which corre- Sppcimenr ustd for ollorymr analyses and cmoucher rprctmrn numberr.-Hel- sponds to their proximity to the nearest main- rrosttchus rosfmlus IO between 5 and I5 m in depth, Santa Catalina land and their apparent link with currents Island. California (SI0 90-81);35 from trawl samples 5 to IO m deep, Mission Bay, San Diego (SI0 90-80); 6 intertidally, Punta Clara. Baja passing close to the mainland (Fig. 1). California, Mexico (SI0 90-82); IO between 0 and 15 m in depth, San The three clinid populations from Guadalupe Benito Islands, Baja California, Mexico (SI0 90-83);6 between 0 and Island (Heterostichus, G. eleguns and G. monter- 20 m in depth, Guadalupe Island, Baja California, Mexico (SI0 90-84); G. rlegans rlrganr 3 intertidally. San Simeon, California (SI0 90-88):9 eyensis norm) are significantly more genetically between 0 and 5 m in depth, Santa Barbara, California (SI0 90-87);4 isolated from the other populations. Genetic between 5 and I5 m in depth, Pelican Bay, Santa Cruz Island. California (SI0 90.90): IO between 5 and IO m in depth from Cherry Cove, Santa distances distinguishing them are similar but Catalina Island, California (SI0 90-81);53 intertidally from Bird Rock, slightly greater in G. monterejensis, which may La Jolla, California (SI0 90-85);5 between 5 and 30 m in depth, Middle be a result of its being primarily a more north- Coronado Island, northern Baja California. Mexico (SI0 90.89); IO intertidally, Punta Clara. Baja California, Mexico (SI0 90.82); 20 be- ern (cold water) species. Relative genetic isola- tween 0 and 20 m in depth, San Benito Islands, Baja California, Mexico tion of Guadalupe is probably a result of a com- (SI0 90-83); C. eleganr vrlfem 1 I from IO and 15 m depth, Boomer Beach, La Jolla, Calfornia (SI0 90-86);C. rleganr crrolt 13 intertidally, bination of factors, including its small size and Guadalupe Island, Baja California, Mexico (SI0 90-84);G. mrfzz melit sharp drop-off (limiting shallow water algal ar- 11 intertidally. Soberanes Point, Carmel, California (SI0 90-91);53 eas available for clinid habitats), considerable intertidally, San Simeon, California (SI0 90-88):G. mrtn J~~nenfcr21 intertidally, Punta Clara, Baja California, Mexico (SI0 90-82);G. mon- distance from mainland and other island pop- ltr~ynnswlganr IO intertidally Soberanes Point, Carmel, California ulations, the surrounding realm of very deep (SI0 90-91);G. rnonfrreymsts montpreyenris 3 I intertidally, San Simeon, California (SI0 90-88); 3 between 10-20 m in depth, Santa Barbara, water, and current patterns that only remotely California (SI0 90-87):19 i crtidally, Punta Clara, Baja California, link it with other chid populations (Fig. 1). Mexico (SI0 90-82);G. nome 12 intertidally, Guadalupe Island, Mexico These factors may account for genetic drift and/ (SI0 90-84);C. erylhra 8 in deep tidepools, San Simeon, California (SI0 90-88);4 between 20 and 35 meters in depth, middle Coronado Island, or natural selection resulting in the divergence Baja California, Mexico (SI0 90-89);Myxodes mndis (South American of these populations. These populations show a myxodin chid used for tree rooting) 30 intertidally from Montemar, very small degree of genetic divergence and, Vina del Mar, Chile (SI0 87-132). therefore, no clear-cut genetic characteristics Presrtvrd malennl examined.-G. monfereyenrisSI0 73-220. Piedras Blan- cas Point, San Luis Obispo, California (20); SI0 80-21,Piedras Blancas to support their recognition as separate species. Point, San Luis Obispo (19); SI0 69-245-61,San Simeon, San Luis Although temperature tolerance experiments Obispo(10); LACM 39975-9,San Simeon (IO); SI067-1 51, San Simeon (Davis, 1977) showed that G. metzi has greater (60); SI0 H47-97,Santa Rosa Island (I); SI0 H51-244,Santa Cruz Island (2);SI0 H51-227,Santa Catalina Island (5); SI0 H48-122,Point tolerance for warm temperatures than does G. Loma (I), SI0 H51-23,Punta Banda, Baja California, Mexico (23);SI0 montereyensis, G. metri has not been collected at H49-173. Rio Santo Tomas (5); SI0 61H47-203,Punta Clara (54); SI0 52-158-61A,San Geronimo Island (17); G. cglhra SI0 51-244, either the San Benito or Guadalupe islands. Santa Cruz Island, California (8): SI0 51-240-61A.Santa Crur Island (I), SI0 51-249,Santa Crur Island (32);SI0 51-260-61.SI0 91-251, Summary.-In conclusion, although the four Santa Crur island (20);LACM 3-9975-9,San Simeon (7); Santa Rosa Island (I); SI0 51-241-61A,Santa Rosa Island (I); SI0 51-241-618, species of North American clinids, as defined Santa Rosa Island (I); SI0 54-190-61,San Miguel Island (I); SI0 58- in the present study, display two general pat- 502-6112,La Jolla (I); SI0 61-527-61A.La Jolla (I); SI0 H49-151. South Coronado Island, Baja California, Mexico (2); SI0 58481-61, terns of distribution, either primarily in cooler Coronado Islands (6); SI0 59-305-61C,Punta Banda (I); SI0 H52- waters (north of Point Conception and in areas 215, Bahia San Carlos (I); C. norac SI0 65-71,Guadalupe Island, Mex- of cold water upwelling) or in warmer waters ico(8);SIO65-51,GuadalupeIsland(l);SIO57-l90,GuadalupeIsland (3); SI0 69-178,Guadalupe Island (2); SI0 70-49,Guadalupe Island (south of Point Conception), there is consider- (5); SI0 58-492, Guadalupe Island (I); SI0 60-15.Guadalupe Island able sympatry in the southern coastal upwelling (3);SI0 63-174,Guadalupe Island (2); SI0 71-108,Guadalupe Island (2); SI0 H51-12461A, Cuadalupe Island (7); G. elcganr nrbrior CAS areas, as well as off some of the offshore islands. SU 16272,holotype, Guadalupe Island (I); CAS SU 16272, paratypes, Our results are consistent with high gene flow Guadalupe Island (5); G. clrgons moli and G. elegans nrbrior (mixed) SI0 a94 COPEIA, 1991, NO. 4

50-38, Guadalupe Island (25); SI0 54-213, Guadalupe Island (6); SI0 erinidae). Unpubl. Ph.D. diss., Univ. of California, 58-453, Guadalupe Island (18); SI0 58-492, Guadalupe Island (20); Los Angeles. SI0 58-497, Guadalupe Island (8); SI0 60-14, Guadalupe Island (15); SI0 60-14-16C. Guadalupe Island (2); SI0 63-184-618, Guadalupe DAVIS,B. J. 1977. Distribution and temperature ad- Island (5). aptation in the teleost fish genus Gibbonsia. Marine Biol. 42:315-320. ACKNOWLEDGMENTS -,E. E. DEMARTINI,ANDK. MCGEE. 1981. Gene flow among populations of a teleost (painted green- This research was supported by a National ling, Oxylebius pictus) from Puget Sound to southern Science Foundation postdoctoral fellowship California. Ibid. 65:17-23. grant in Systematic Biology, #BSR-8600 180, to DAWSON,E. Y. 1960. A review of the ecology, dis- C. Stepien This manuscript benefited substan- tribution, and affinities of the benthic flora. Sym- tially from critical reviews by D. S. 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