Journal of Fish Biology (2010) 77, 329–340
doi:10.1111/j.1095-8649.2010.02677.x, available online at www.interscience.wiley.com
Population genetic structure of the round stingray Urobatis
halleri (Elasmobranchii: Rajiformes) in southern
California and the Gulf of California
S. M. Plank*†, C. G. Lowe*, K. A. Feldheim‡, R. R. Wilson jr.* and
J. A. Brusslan*
*Department of Biological Sciences, California State University, Long Beach, 1250 Bellflower
Blvd., Long Beach, CA 90840-3702, U.S.A. and ‡Field Museum, Pritzker Laboratory for
Molecular Systematics and Evolution, 1400 South Lake Shore Drive, Chicago, IL
60605, U.S.A.
(Received 12 August 2009, Accepted 25 February 2010)
The round stingray, Urobatis halleri, is a viviparous elasmobranch that inhabits inshore, benthic
habitats ranging from the western U.S.A. to Panama. The population genetic structure of this species
was inferred with seven polymorphic microsatellite loci in samples collected at three sites in coastal
southern California, one near Santa Catalina Island, California and one in the eastern Gulf of
California. Urobatis halleri is relatively common, but little is known of its movement patterns or
population structure. Small FST values (−0·0017 to 0·0005) suggested little structure among coastal
populations of southern and Baja California. The population sampled at Santa Catalina Island,
which is separated by a deep-water channel from the coastal sites, however, was significantly
divergent (large FST , 0·0251) from the other populations, suggesting low connectivity with coastal
populations. The Santa Catalina Island population also had the lowest allele richness and lowest
© 2010 The Authors
average heterozygosity, suggesting recent population bottlenecks in size.
Journal compilation © 2010 The Fisheries Society of the British Isles
Key words: founder event; genetic bottleneck; microsatellite alleles; population structure; Santa
Catalina Island.
INTRODUCTION
Near the top of the food chain in ocean ecosystems, elasmobranchs are surprisingly
understudied with regard to their life-history traits, breeding biology and population
genetics. Population genetic studies of elasmobranchs have mainly examined commercially and recreationally fished species that are either already, or in danger of
becoming, overexploited (Heist & Gold, 1999; Pardini et al., 2001; Keeney et al.,
2003; Schrey & Heist, 2003; Duncan et al., 2006; Hoelzel et al., 2006; Keeney &
Heist, 2006; Lewallen et al., 2007). As studies unexploited elasmobranchs are lacking, the knowledge of their population dynamics in the absence of human-imposed
pressures (e.g. fishing) is inadequate.
†Author to whom correspondence should be addressed. Tel.: +1 562 985 8133; fax: +1 562 985 8878;
email: splank81@gmail.com
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© 2010 The Authors
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S. M. PLANK ET AL.
The round stingray, Urobatis halleri (Cooper), is a small (<56 cm in length;
Eschmeyer et al., 1983), inshore, benthic ray that ranges from Panama Bay, Panama
to Humboldt Bay, California, U.S.A. (Miller & Lea, 1972; Eschmeyer et al., 1983).
This species is not part of the U.S. fishery despite being common along both sides
of the Baja California peninsula and into southern California (Eschmeyer et al.,
1983). It is rarely encountered north of Point Conception (Roedel, 1953), the transition point between the Oregonian and San Diegan faunal provinces (Briggs, 1974).
From there, the shoreline transitions from a north–south to west–east trend, resulting in a large inshore–offshore temperature differential south of Point Conception
where the coastline becomes sheltered from the cold, southerly California Current.
Water temperature influences movement patterns and the distributions of several
elasmobranchs, including Atlantic stingrays [Dasyatis sabina (LeSueur)] and bat
rays [Myliobatis californica (Gill)] (Snelson et al., 1988; Gray et al., 1997; Matern
et al., 2000; Wallman & Bennett, 2006). Babel (1967) hypothesized that U. halleri
preferred temperatures above 10◦ C and attributed its preference for shallow water
(>20 m) to this temperature constraint (Babel, 1967; Eschmeyer et al., 1983).
Evidence supports fairly high migration of U. halleri across shallow habitats.
Early tagging studies (Russell, 1955; Babel, 1967) reported movements of individuals
from 8·8 km to >24 km from tagging sites. Recently, Vaudo & Lowe (2006) reported
recovering a specimen of U. halleri in Newport Bay, California, 2 months after it had
been acoustically tagged at Seal Beach, California (30 km to the north). The stingray
returned to the Seal Beach vicinity the next year. Despite mobility of U. halleri,
temperature or other factors such as predation may inhibit extensive or frequent
movements over deep water. For example, nearly 42 km of deep water (500–900 m)
now separates a Santa Catalina Island population from those of the California coast,
whereas in recent decades U. halleri has not been abundant around Santa Catalina
Island.
A comprehensive survey of fishes associated with kelp and non-kelp habitats of
southern and Baja California between 1948 and 1954 did not report U. halleri at
Santa Catalina Island, whereas the species was reported at sites along the southern
California coast. Another, albeit more pelagic, stingray (Myliobatis californicus Gill)
was reported both at Santa Catalina Island as well as along the coast in the same
survey (Limbaugh, 1955). The earliest record of U. halleri at Santa Catalina Island is
from 1970 when personnel of the California Department of Fish and Game collected
four individuals (Los Angeles County Museum of Natural History Cat. No. 32658-1,
accessed via www.fishent2.net). Moreover, aggregations are now fairly common at
Santa Catalina Island (C. Lowe, unpubl. obs.), although comparable stingray populations appear to be absent from other offshore islands (David Kushner U.S. National
Park Service, Channel Islands & Dan Pondella, Vantuna Research Group Director,
pers. comm.).
Urobatis halleri may also be restricted in movement around the cape of the Baja
California peninsula, Mexico. Disjunct populations are observed for other fishes
with populations on both sides of the peninsula. Present (1987) listed 42 species,
representing 28 families that span 12 orders, considered to be disjunct between the
Gulf of California and the Pacific coast of Baja California. Urobatis halleri was
placed in category 4, a group of fishes considered to disjunct between these two
despite having been found at least as far south as Mazatlán, Mexico. The range of
U. halleri, however, extends much farther south than Mazatlán into Panama.
© 2010 The Authors
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Genetic studies of some species on Present’s (1987) list have confirmed eight
fishes with distinct genetic populations in the Gulf of California and the Pacific
coast of Baja California (Terry et al., 2000; Huang & Bernardi, 2001; Stepien et al.,
2001; Bernardi et al., 2003; Bernardi & Lape, 2005). The shovelnose guitarfish, Rhinobatos productus (Ayres), a species not included in Present’s original list, was also
genetically disjunct across the Baja California peninsula (Sandoval-Castillo et al.,
2004). Warm temperatures along the southern end of the peninsula seem to be the
main barrier to migration and gene flow among those species. Urobatis halleri is
most likely unaffected by these warmer temperatures, and should disjunction prove
to exist, it would most likely be due to another kind of barrier, such as a break in
suitable habitat.
To examine potential population genetic structure and migration barriers to gene
flow in U. halleri, four locations along California were sampled: three clustered on
the southern California coast near Long Beach, California and one at Santa Catalina
Island. In addition, samples were collected from the eastern central Gulf of California,
Mexico. Based on known migration capability from tagging studies and suggested
temperature preferences of this species, coupled with the findings of other genetics
studies of fishes, three predictions were made: (1) no genetic structure exists among
the proximal coastal California populations due to migration; (2) if populations of
coastal California and the Gulf of California are disjunct, little gene flow between
them would be expected; (3) only moderate genetic structure exists between the
Santa Catalina Island population and other populations that were sampled. These
predictions are based on previous results for viviparous and non-viviparous fishes
inhabiting the offshore islands (Haldorson, 1980; Beckwitt, 1983; Waples, 1987;
Waples & Rosenblatt, 1987; Bernardi, 2000; Luzier & Wilson, 2004).
MATERIALS AND METHODS
TISSUE COLLECTION
Sampling locations are shown in Fig. 1. Specimens of U. halleri were captured from
Catalina Harbour, Santa Catalina Island, California (Santa Catalina Island, 33◦ 26 N; 118◦
30 W), the 7th St. Pond, Seal Beach National Wildlife Refuge, Seal Beach, California
(SBNWR, 33◦ 42 N; 118◦ 03 W) and Silver Strand State Beach, San Diego, California
(San Diego, 32◦ 37 N; 117◦ 08 W) by an 8 m beach seine pulled manually parallel to shore.
One stingray was collected from Catalina Harbour by snorkel and hand-held dip-net. Sampling
trips took place as follows: Santa Catalina Island, October 2006 through June 2007; SBNWR,
August 2006; San Diego, August through September 2006. Tissues were also sampled from
stingrays collected at Seal Beach, California, in the area adjacent to the San Gabriel River
mouth (Seal Beach, 33◦ 44 N; 118◦ 06 W), in July 2000 and were subsequently frozen at
−20◦ C until tissue samples were taken during the summer of 2005. These fish had been
collected by a 30 m beach seine that was set parallel to the shoreline with the assistance of a
jet ski operated by the Seal Beach lifeguards and hauled onto the beach with the assistance of
hand lines. Urobatis halleri from the Gulf of California were collected from shrimp fishing
boats and fishery camps from the artisanal fishery in Sonora, Mexico, and stored at −20◦ C
until tissue samples were taken during the spring of 2007 by Maria del Pilar Blanca-Parra
of the Universidad Nacional Autónoma de Mexico, La Paz, Mexico. A small (<3 mm), triangular sample of tissue was taken from the trailing edge of the right pectoral disc edge of
each stingray using a fresh razor blade. Tissues were then immediately fixed in 95% ethanol
and stored at 4◦ C until DNA extraction. Because collection at Santa Catalina Island took
place over several months, these fish were fitted with a 1·3 cm Peterson disc tag (Floy Tag &
© 2010 The Authors
Journal compilation © 2010 The Fisheries Society of the British Isles, Journal of Fish Biology 2010, 77, 329–340
332
S. M. PLANK ET AL.
Seal Beach
SBNWR
Santa Catalina Island
N
San Diego
0
50
100
200 Kilometers
N
0
255
510
1020 Km
Fig. 1. Sampling locations of Urobatis halleri ; the map on the right shows the California–Mexico coast from
Point Conception, CA to the tip of Baja California, Mexico. The Gulf of California sampling area is
indicated by the oval. The cutaway to the left shows the southern California Bight from Point Conception
to the Mexican border. , sampling areas in southern California.
MFG., Inc.; www.floytag.com) to avoid resampling. At the other locations, sampling periods
were close enough together so that recaptured fish were identified by both a clipped caudal
spine combined with a fin clip marking and were subsequently released. A single recapture
was identified in this fashion at San Diego.
E X T R A C T I O N A N D A M P L I F I C AT I O N
Tissue samples of <1 mm2 were placed in a 0·5 ml thin-walled PCR tube with a 10%
Chelex solution (BioRad; www.bio-rad.com) and heated to 95◦ C for 20 min. The resulting
supernatant containing the genomic DNA was removed and stored at −20◦ C until further
analysis.
Microsatellite amplification was performed using seven sets of primer pairs developed for
U. halleri (MER primer database 37320–37326; Genbank accession numbers FJ985018–
FJ985024). For each primer pair, one primer (forward or reverse) was fluorescently labelled
with IRDye700 by LI-COR for detection in the model 4300 DNA sequencer (LI-COR;
www.licor.com), whereas the other was unlabelled (Operon, www.operon.com).
PCR mixtures consisted of 1 μl genomic DNA combined with a master mix (total volume 6 μl) containing 0·1 mM untagged primer, 0·05 mM tagged primer, 1 × Std Taq buffer
(10 mM Tris–HCl, 50 mM KCl, 1·5 mM MgCl2 , pH 8·3 at 25◦ C: New England Biolabs;
www.neb.com), 1·25 mM dNTP mixture (New England Biolabs) and 0·3 U Taq polymerase
(New England Biolabs). PCR amplification, conducted with a MJ Research (Waltham, MA)
PTC-100 thermal cycler, consisted of an initial denaturation of 5 min at 94◦ C followed by
30 cycles of 92◦ C for 1 min, Ta for 1 min and 72◦ C for 1 min followed by a final extension
at 72◦ C for 5 min.
M I C R O S AT E L L I T E A N A LY S I S
PCR products and 4 μl of loading dye (LI-COR) were denatured at 92◦ C for 4 min.
A small aliquot of this mixture (1 μl) was then loaded into 64 well sharkstooth combs (LICOR) and run on a 6·5% acrylamide gel. An IRDye700 size standard (50–350 bp; LI-COR)
was loaded after every eighth sample. Electrophoresis and band detection were performed by
a LI-COR 4300 sequencer, and SAGAGT software (LI-COR) was used to determine the base
pair (bp) length of each allele. Size analysis of each allele was subsequently checked by eye
to ensure that the samples were correctly scored.
© 2010 The Authors
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The following analyses were run using Arlequin 3.1 software (Excoffier et al., 2005). All
populations were tested for conformation to expectations of Hardy–Weinberg equilibrium.
Pair-wise FST calculations were performed between all population pairs, and a Bonferroni
correction (α = 0·005) was used to adjust for multiple tests. Because FST calculations are
modelled after a two allele system (which highly polymorphic loci do not follow precisely),
pair-wise G tests, which are log-likelihood tests and not based on specific population models,
were also performed between each sampling location using GENEPOP 4.0 (Rousset, 2008).
The Garza–Williamson index (M), a genetic indication of population reduction [i.e. bottlenecks, founder events; Garza & Williamson, 2001], was also determined. M is a ratio of
the number of alleles observed in a sample divided by the number of alleles expected under
the observed size range (i.e. number of repeats). According to Garza–Williamson’s models,
which were based on populations with known historical bottlenecks, values of M greater
than c. 0·82 are representative of stable (equilibrium) populations, whereas values of M less
than c. 0·70 suggest populations that have experienced a bottlenecking or founder event. An
a priori test for the Santa Catalina Island sample was also made using BOTTLENECK 1.2.02
(Cornuet & Luikart, 1996), which detects a recent genetic bottleneck by measuring heterozygosity excess. This occurs when the number of alleles is initially reduced in higher proportion
than the observed heterozygosity. In BOTTLENECK, ‘observed heterozygosity’ is calculated
from allele frequencies at each locus assuming Hardy–Weinberg proportions.
RESULTS
S A M P L I N G A N D M I C R O S AT E L L I T E L O C I
A total of 300 tissue samples were collected across the five sampling locations as
follows: Seal Beach, n = 74; SBNWR, n = 60; San Diego, n = 62; Santa Catalina
Island, n = 53; Gulf of California, n = 51. All seven loci exhibited several alleles
(10–37 alleles per locus; Table I) and conformed to Hardy–Weinberg expectations
at all sampling locations (data not shown).
P O P U L AT I O N G E N E T I C S T R U C T U R E
Gene flow along the southern California coastline between the areas near Seal
Beach and San Diego Bay, California, appeared to be high, as shown by the low
Table I. Number of alleles per locus in Urobatis halleri with mean expected heterozygosity (HE ) and Garza–Williamson index (M) for each of five populations and total expected
heterozygosity for each locus
Uha
Uha
Uha
Uha
Uha
Uha
Uha
HE
M
20
36
61
111
115
170
176
Seal
Beach
SBNWR
San
Diego
Santa Catalina
Island
Gulf of
California
Total HE
14
14
34
18
13
24
26
0·89
0·86
14
12
37
15
14
21
25
0·89
0·85
15
14
31
16
14
24
26
0·88
0·89
12
10
23
11
11
15
19
0·85
0·76
14
12
25
14
12
23
24
0·89
0·87
0·77
0·87
0·91
0·87
0·89
0·94
0·94
—
—
SBNWR, Seal Beach National Wildlife Refuge
© 2010 The Authors
Journal compilation © 2010 The Fisheries Society of the British Isles, Journal of Fish Biology 2010, 77, 329–340
334
S. M. PLANK ET AL.
Table II. Pair-wise G test (above diagonal) and FST values (below diagonal) for southern
California Bight and Gulf of California samples of Urobatis halleri
Seal
Beach
Seal Beach
SBNWR
San Diego
Santa Catalina Island
Gulf of California
SBNWR
San
Diego
—
21·32634 10·57431
0·00055
—
9·56981
−0·00170 −0·00108
—
0·01293a 0·01078a
0·01320a
0·00557
0·00694a 0·00187
Santa Catalina
Island
Gulf of
California
Infinitya
Infinitya
Infinitya
—
0·02511a
44·72691b
52·08526b
25·60964
Infinitya
—
SBNWR, Seal Beach National Wildlife Refuge
a P < 0·00001.
b P < 0·005.
Table III. Pair-wise G test (above diagonal) and FST P -values (below diagonal) for southern
California Bight and Gulf of California samples of Urobatis halleri
Seal Beach
SBNWR
San Diego
Santa Catalina Island
Gulf of California
Seal
Beach
SBNWR
—
0·35135
0·90090
0·00000a
0·00901
0·09356
—
0·80180
0·00000a
0·00000a
San
Diego
Santa Catalina
Island
Gulf of California
0·71911 Highly significanta
0·00004b
a
0·79291 Highly significant
0·00000b
a
—
Highly significant
0·02901
0·00000a
—
Highly significanta
0·16216
0·00000a
—
SBNWR, Seal Beach National Wildlife Refuge
a P < 0·00001.
b P < 0·005.
FST values (−0·0017 to 0·0005) and fully corroborated by the results of the G tests
(Tables II and III). Slightly larger FST values were found between coastal California
populations and the Gulf of California population (0·0019–0·0069; Table II), and
only one of these comparisons was significant (SBNWR and Gulf of California;
Table III). The greatest genetic differentiation was found between Santa Catalina
Island and all other populations (Tables II and III), with the largest FST comparison
found between Santa Catalina Island and the Gulf of California (0·0251).
B O T T L E N E C K R E S U LT S
Allelic richness was the lowest at Santa Catalina Island across all loci despite the
Gulf of California sample having a slightly smaller sample size (Table I). In addition,
some of the alleles at Santa Catalina Island occurred in much higher frequencies than
on the mainland (Fig. 3). Frequency distributions of alleles (Figs 2 and 3) were similar in appearance to the bottleneck examples given in Garza & Williamson (2001).
M was also much lower at Santa Catalina Island (0·75) compared with all other populations (Table I). BOTTLENECK results did not detect an excess in heterozygosity
at Santa Catalina Island under the infinite alleles–stepwise mutation model in either
the Sign Test (P = 0·25/0·049) or the Wilcoxon test (P = 0·078/0·98).
© 2010 The Authors
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335
P O P U L AT I O N G E N E T I C S O F R O U N D S T I N G R AY
Seal Beach
Santa Catalina Island
0·60
0·50
0·40
0·30
0·20
0·10
0·00
5
6
7
8
9
10
11
12
13
14
15
16
17
18
19
20
21
Frequency
0·60
0·50
0·40
0·30
0·20
0·10
0·00
5
6
7
8
9
10
11
12
13
14
15
16
17
18
19
20
21
Repeat
Repeat
0·40
0·40
0·30
0·30
Frequency
0·20
0·10
0·20
0·10
0·00
5
6
7
8
9
10
11
12
13
14
15
16
17
18
19
20
21
5
6
7
8
9
10
11
12
13
14
15
16
17
18
19
20
21
0·00
Repeat
Repeat
0·30
0·30
0·25
0·20
Frequency
0·15
0·10
0·05
0·20
0·15
0·10
0·05
Repeat
Frequency
48
53
0·40
0·30
0·20
0·30
0·20
0·10
0·00
0·00
17
18
19
20
21
22
23
24
25
26
27
28
29
30
31
32
33
34
35
0·10
17
18
19
20
21
22
23
24
25
26
27
28
29
30
31
32
33
34
35
Frequency
43
Repeat
0·40
(d)
38
28
8
48
0·00
53
43
38
28
33
18
23
8
13
0·00
23
Frequency
0·25
18
(c)
13
Frequency
(b)
33
Frequency
(a)
Repeat
Repeat
Fig. 2. Frequency distribution of microsatellite alleles in Urobatis halleri from the Seal Beach and Santa
Catalina Island samples in loci (a) Uha 20, (b) Uha 36, (c) Uha 61 and (d) Uha 111.
DISCUSSION
Urobatis halleri populations along coastal waters of southern California appear to
be panmictic with no genetic structure. In addition, the results indicated a low level
of genetic differentiation between the Gulf of California and the southern California
populations, suggesting that the U. halleri in the eastern central Gulf of California
are not isolated from those on the Pacific coast of Baja California. The results do
not support a model of disjunction between U. halleri populations on either side
of the Baja California peninsula. Although Present (1987) noted that the range of
U. halleri extended south of Cabo San Lucas along the Central American coast,
she listed the species as disjunct based on Hubbs (1960). Hubbs (1960) however,
described ‘representatives of the genera. . . Urolophus’ (= Urobatis) as possibly
© 2010 The Authors
Journal compilation © 2010 The Fisheries Society of the British Isles, Journal of Fish Biology 2010, 77, 329–340
336
S. M. PLANK ET AL.
Seal Beach
Frequency
0·15
0·1
0·25
0·2
0·15
0·1
0·05
0
0
7
8
9
10
11
12
13
14
15
16
17
18
19
20
21
22
23
0·05
Repeat
Repeat
0·20
0·20
0·15
0·15
Frequency
0·10
0·05
0·10
0·05
0·00
8
10
12
14
16
18
20
22
24
26
28
30
32
34
36
38
8
10
12
14
16
18
20
22
24
26
28
30
32
0·00
Repeat
(c)
34
36
38
Frequency
(b)
0·25
0·2
7
8
9
10
11
12
13
14
15
16
17
18
19
20
21
22
23
Frequency
(a)
Santa Catalina Island
Repeat
0·15
0·05
21
23
25
27
29
31
33
35
37
39
41
43
45
47
49
51
0
Repeat
0·1
0·05
0
21
23
25
27
29
31
33
35
37
39
41
43
45
47
49
51
Frequency
Frequency
0·15
0·1
Repeat
Fig. 3. Frequency distribution of microsatellite alleles in Urobatis halleri from the Seal Beach and Santa
Catalina Island samples in loci (a) Uha 115, (b) Uha 170 and (c) Uha 176.
being ‘trapped’ in the Gulf of California due to apparent scarcity in the Cape region,
but did not refer specifically to U. halleri. Two other described species of Urobatis
are also known in that area, Urobatis maculatus (Garman) and Urobatis concentricus
(Osburn & Nichols) (McEachran, 1995).
In contrast, there is a genetically distinct subpopulation of U. halleri on Santa
Catalina Island, c. 42 km from the mainland coast of California. This was shown
by both the FST and G tests. Although this finding aligns well with Bernardi’s
(2000) finding of distinct populations of black surfperch Embiotoca jacksoni (Agassiz) among the California Channel Islands based on mtDNA data, it is a finding
distinct from prior studies using allozymes and is a much stronger result compared
with any using microsatellite data (Selkoe et al., 2007).
The amount of time U. halleri has been present at the island or how it arrived
there is unknown. Initial colonization might have occurred if the fish had been physically transplanted to the island by some means. Also, during El Niño, southern
California experiences heavy rainstorms. Rivers in southern California have undergone channelling in which the bottoms and sides are lined with concrete, increasing
the velocity of water flow during a rain storm. Satellite images show post-rainstorm
freshwater plumes from the San Gabriel River near Long Beach, California, along
with other rivers emptying into the San Pedro Channel, occasionally extending to
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Santa Catalina Island (Nezlin & DiGiacomo, 2005). Because round stingrays may
form large aggregations at the mouth of the San Gabriel River (Babel, 1967; Vaudo
& Lowe, 2006; Lowe et al., 2007), it is possible that they could have been aided in
reaching the island via one or more plumes.
The low allelic richness at Santa Catalina Island is probably not an artefact of
sample size, since the Gulf of California population sample had two fewer individuals
than at Santa Catalina Island. Instead, low allelic richness suggests a founder event,
resulting in a reduction in the number of alleles introduced. The Garza–Williamson
index for Santa Catalina Island (M = 0·76) is in between what Garza & Williamson
(2001) considered to be a bottlenecked population and a stable population, though
their bottleneck threshold value of 0·70 may be conservative as it was modelled with
extremely reduced populations. In addition, according to their models, if a founder
population is large, it may take many generations of genetic drift to reach an index
of 0·70. For instance, in a population that starts off with an index of c. 0·82 and is
reduced to an effective size of 25 individuals, it would take about five generations to
reach 0·70. If a founder population had an effective size of 50 individuals, it would
take about 10 generations to reach 0·70.
These U. halleri specimens may not have been present at Santa Catalina Island
in the numbers seen today as recently as 15–20 years ago (C. Lowe, unpubl. obs.),
suggesting a recent founder event. If the 1970 capture record is used as a start time
and an age at maturity of c. 3 years as a low estimate of generation time, only ≤12
generations are expected to have passed. Age at maturity for this species has been
estimated from 2·6 years (Babel, 1967) to 4 years (Hale & Lowe, 2008).
Results from the BOTTLENECK, conversely, did not indicate the significant
deviations from heterozygosity expected at mutation-drift equilibrium that is characteristic of a genetic bottleneck. Keller et al. (2001), however, also failed to detect
a bottleneck using this programme a few years after a storm decreased an island
population of song sparrows by 95% (10 survivors). Similarly, enough generations
of random breeding may have occurred at Santa Catalina Island to restore heterozygosity to mutation-drift equilibrium, but not enough for M to be reduced <0·70. In
addition, Keller et al. (2001) described subsequent immigration of song sparrows to
the island following the population crash, which increased the number of alleles in
the population. Terrestrial runoff plumes may reach Santa Catalina Island following
any major rainstorm and could also be providing the island with subsequent immigration (and new alleles), maintaining a relatively high M for a genetically bottlenecked
or recently founded population.
According to Williamson-Natesan (2005), the methods used in the present study for
detecting bottlenecks or founder events [allele size range conditioned on the number
of alleles (M) and heterozygosity excess] had the lowest type I and type II error rates
when modelled with known population scenarios (stable and reduced populations).
Heterozygosity was a better indicator when events were recent, less severe and
either mutation rates were low or original populations were small. Conversely, M
was a better indicator if the events occurred several generations before the population
made a demographic recovery and either mutation rates were high or the pre-event
population was large. It can be argued that U. halleri have made a demographic
recovery at Santa Catalina Island since being commonly seen in the shallow waters
surrounding the island, and this appears to be a relatively recent occurrence. In
addition, if Seal Beach, or any other location along the California coast, was the
© 2010 The Authors
Journal compilation © 2010 The Fisheries Society of the British Isles, Journal of Fish Biology 2010, 77, 329–340
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S. M. PLANK ET AL.
source population, it could also be argued that the pre-event population was large,
as this species is highly abundant along the coast.
The present study using microsatellite loci appears to be the first to report a genetically isolated subpopulation of a fish species found both on Santa Catalina Island
and the mainland coast of southern California. Although there has long been interest
in gene flow and connectivity among marine fishes in relation to dispersal potential
and capability (Rosenblatt, 1963), dispersal has mostly meant planktonic dispersal.
In general, there have been few reported instances of genetic isolation among fishes
of the California Channel Islands and those have referred to viviparous surf perches
(Haldorson, 1980; Bernardi, 2000). Population connectivity among viviparous species
deserves more attention.
This study assessed the population structure of an unexploited elasmobranch using
microsatellite markers and revealed a previously unreported, and thus uncharacterized, subpopulation of stingrays on an offshore island of California. In addition, no
genetic evidence was found of disjunction of round stingrays between the Gulf of
California and Pacific coast populations of the Baja California peninsula.
We acknowledge the R. B. Loomis Award and the California State University, Long Beach
(CSULB) College of Natural Sciences and Mathematics Boeing Scholarship for funding, and
all volunteers especially I. Evans, C. Mull, K. Jirik, A. Fields, W. Plank, M. Plank and
members of the CSULB Shark Lab. We also thank C. Mireles for his assistance with the maps
and M. Blanco-Parra for providing the Gulf of Mexico samples. Microsatellite enrichment
was funded by the Grainger Foundation and was carried out in the Pritzker Laboratory for
Molecular Systematics and Evolution operated with support from the Pritzker Foundation.
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