Populations identified as
xanthoptica, unblotched
salamanders with large amounts of orange pigmentation (especially
ventrally) and a bright yellow upper iris, occur in the North, South
and East Bay regions and in the west-central Sierra Nevada. This taxon
occupies a key position in the ring complex. A zone of morphological
intergradation between
xanthoptica and
eschscholtzii extends from Atascadero northward in the Coast
Range to the Monterey Bay region (
7). Morphological intergradation of
xanthoptica with
oregonensis occurs from near
Monterey Bay north to the vicinity of Ft. Ross (
7). In the Sierra
Nevada
xanthoptica hybridizes with
platensis
(
14). While acknowledging the validity of the analysis of coloration
(
7), there is little evidence of the intergradation described above
using molecular markers.
General results are summarized in Fig.
2.
Although the distribution of
xanthoptica is interrupted by
major present-day barriers, the taxon maintains some integrity as a
unit, especially with respect to coloration and the monophyly of DNA
sequences. Minimal
D is 0.08 between North Bay and East Bay
localities, and 0.05 between East Bay and South Bay localities.
However, between South Bay and North Bay localities there is relatively
great and varying divergence (
D = 0.15–0.47). The
genetic connection between the North Bay and South Bay appears to be
via the East Bay; San Francisco Bay and associated Carquinez Straits
(north) and Santa Clara Valley (south), which currently interrupt the
range, are apparently recent barriers. There are some relatively high
D values (to 0.19) between the East Bay and the South Bay
(populations likely to be even more divergent have not been included in
the same study as yet). There is variation within each of these three
areas.
D within the North Bay reaches 0.15 (
n,
number of populations compared = 5), within the East Bay, 0.09
(
n = 4), and within the South Bay, 0.31
(
n = 6 in each of two studies using different
populations). In the eastern part of the South Bay distances are below
0.15, but some western populations are highly divergent from everything
studied (these also are the populations with the greatest divergence to
North Bay
xanthoptica). Several populations contain both
xanthoptica and
oregonensis alleles; these
introgressed populations were not classified.
| Figure 2Distribution of taxa of Ensatina
in the San Francisco Bay region, showing D (21) based on
allozyme data between selected neighboring populations. Bold face type,
D between taxa; normal type, D within
taxa. The mean and range of D between North Bay (more ...) |
There is a finger-like projection of
xanthoptica into
oregonensis in the North Bay, and this small range is
divided by inhospitable (now agricultural and urban) lowlands to the
west of Santa Rosa. To the west, north, and east, populations are
genetically
oregonensis.
D values between the two
taxa exceed 0.3. Based on allozymes, populations identified by
coloration (
7) as
xanthoptica are correctly assigned, but
populations identified as morphological intergrades are assigned to
oregonensis (with exceptions discussed below).
On the southern San Francisco Peninsula in the Santa Cruz Mountains
oregonensis and
xanthoptica meet with a genetic
gap of
D = 0.16–0.32. Further south, the genetic
distance between
xanthoptica and
eschscholtzii
across the Pajaro River is somewhat less (
D =
0.15–0.2). There is little evidence as yet for gene flow between
nearby populations of
oregonensis and
xanthoptica
in this region, although two local populations appear to be admixed.
There remain small local geographic gaps in our sampling. However, as
we have shortened the geographic distance between
xanthoptica and
eschscholtzii in the vicinity of
Monterey Bay,
D has dropped from 0.32 (
12) to 0.15, and
there remains a zone about 30 km in width which is largely unsampled
(habitat along the Pajaro River has been disrupted by agricultural
activities and urbanization). These data suggest that
D will
drop further as additional populations are discovered in the
intervening area.
We sampled only a small portion of the distribution of
oregonensis (it ranges to southern Canada), but uncovered
surprisingly great local differentiation. The first study included 18
populations extending from northern Mendocino down to southern Marin
counties.
D ranged as high as 0.26, and 31% of population
comparisons exceeded
D = 0.15 (the approximate level at
which species borders typically occur in the closely related genus
Plethodon; ref.
22). Detailed analysis of this variation is
beyond the scope of the present paper, but I observe that variation is
great and no areas of high uniformity or of potential species borders
were uncovered; furthermore, borders determined from haplotypes do not
coincide with those determined from allozymes (D.B.W. and C.J.
Schneider, unpublished data). The highest values of
D within
oregonensis involved comparisons across the range, between
populations along the Pacific Coast and those relatively far inland.
For no nearest neighbor comparison is
D = 0, and many
are in the range
D = 0.02–0.07. The third study
included 12 populations (a few repeats from the earlier study but
mainly different) of
oregonensis extending from the Russian
River area through the Coast Range to southern Marin County, with a few
populations in eastern Sonoma County. Even in this relatively small
region genetic diversification is great, with
D reaching a
high of 0.23 (across the breadth of the range) and 36% of the
comparisons exceeding
D = 0.15. Near neighbors always
have the lowest values, but rarely less than
D = 0.04.
Genetic distances across the Russian River range from 0.08 to 0.15,
suggesting that it has restricted gene flow to some extent.
Populations of oregonensis occur in the South Bay, mainly on
the northern part of the San Francisco Peninsula, but extending
southeast to near Loma Prieta. Within this small peninsular area
diversification is great. A maximum D = 0.16 is present
in study three (n = 4), with only one comparison
D < 0.1. In study two (n = 3) the
highest value is D = 0.08.
The mean D between oregonensis north and south of
the Golden Gate is 0.16 (range, 0.08–0.27; 15 populations). There are
three comparisons in the range of 0.08–0.09, showing that the Golden
Gate has not been a major distributional barrier.
There is a genetic gap between
oregonensis and
xanthoptica in the North Bay.
D ranges from 0.28
to more than 0.5, but in the areas where populations of the two
approach most closely
D = 0.3–0.4. There are five to
eight potentially useful loci for constructing hybrid indices (
14), but
none are fixed and there is so much variation, especially in
oregonensis, that indices would only be useful locally. Some
populations appear to be introgressed or admixed (see below). There is
no evidence of hybridization
per se (i.e., no clear
F
1 hybrids or backcrosses).
In two areas near Santa Rosa there is evidence of gene flow between
oregonensis and
xanthoptica (Fig.
3), in the form of admixture. This is at the
extreme northwestern limit of the range of
xanthoptica, in
the hills immediately north of Santa Rosa and on the west side of the
valley that separates these hills from the main Coast Range near
Forestville. In the first area three populations were sampled from
nearly continuous habitat near Mark West Creek. One of these
populations (no. 28,
n = 19) is similar to
xanthoptica in coloration, and another (no. 31,
n = 10) is similar to
oregonensis. These
populations are separated by less than 10 km, but
D =
0.34. Both are highly variable (no. 28 has 36 alleles; no. 31 has 34
alleles at 22 loci), but only no. 28 shows signs of limited gene flow
from the other taxon (alleles characteristic of
oregonensis
are present at low frequency for four loci). A third population (no.
24,
n = 5), 5 km south of population no. 31, displays
coloration somewhat intermediate between
oregonensis and
xanthoptica, but genetic distances are high to both
neighboring populations (0.22 to no. 28; 0.30 to no. 31). There are 32
alleles in the relatively small sample, but no evidence of
F
1 hybrids. However, the sample is fixed for an otherwise
rare allele for malate dehydrogenase (Mdh; EC
1.1.1.37) (found at a
frequency of 0.06 in population 31; absent in population 28), fixed for
an allele for Acon 1 (EC
4.2.1.3) that is relatively common in
population 31 and absent in no. 28, and fixed for an allele for proline
depeptidase (Pep-d; EC
3.4.13.9) which is in high frequency in
population 28 (0.91) but absent in population 31. Acon 2 has an allele
found only in population 24 and an admixed population across the valley
to the west. Population 24 lacks an allele for glutamic-oxaloacetic
transaminase (Got; EC
2.6.1.1) that is fixed in population 31 but
absent in no. 28, and it has two of the three alleles that appear in
population 28. Evidently gene flow as well as some sorting of variants
has occurred. This suggests that there is no intrinsic barrier (e.g.,
specific mate recognition systems, or postmating isolating mechanisms)
to genetic exchange (there is no evidence of such barriers anywhere in
the complex). The region of admixture is narrow, in relation to the
range of the taxa, but probably not with respect to the relatively
narrow home ranges known to be characteristic of this complex (
23,
24).
Some additional populations in this area are introgressed as well and
these are not assigned to any taxon.
| Figure 3The xanthoptica–oregonensis
contact zone north of San Francisco Bay in the Santa Rosa–Russian
River area. Populations 22 and 24 are intermediate in nature.
D values between selected populations are indicated.
Shading in upper part (more ...) |
The second area is even narrower (Fig.
4).
Across the Russian River at the northwestern limit of the range of
xanthoptica there is a genetic gap
D = 0.3
in less than 1 km. As much as 0.15 occurs within
oregonensis
just to the west of the contact zone, but the intertaxon distance is
substantially greater and implies secondary contact of well
differentiated groups. There is also evident change in color pattern on
either side of the Russian River; on the east and south salamanders
have extensive orange pigmentation and a bright yellow dorsal iris,
whereas on the west and north orange pigmentation is greatly reduced,
especially ventrally, and the upper iris is much paler. Two relatively
large samples separated by less than 5 km have a
D =
0.36. The
oregonensis population (no. 25,
n
= 16) contains 41 alleles, and the
xanthoptica population
(no. 23,
n = 11) contains 31 alleles, but only one
locus (different in each population) is potentially introgressed from
the other taxon in either population. The population of
xanthoptica (no. 30) closest to
oregonensis (no.
25) is small (
n = 5) and has
oregonensis
alleles at only one locus. One population (no. 22,
n =
6) has high genetic distance to all neighboring populations, even those
less than 10 km distant (
D = 0.11 to one
xanthoptica; 0.22 to two
oregonensis), including
the other admixed population (
D = 0.31 to no. 24). This
sample is of mixed origin, but its heterozygosity (mean direct count
0.12) is about the same as populations 25 and 23 and there are no clear
hybrid genotypes. Specimens have the coloration of
xanthoptica, but alleles characteristic of
oregonensis are present in all six potential marker loci and
it has a high total number of alleles for a small sample (population
36), further indicating its composite nature.
| Figure 4Expansion of Fig. 3, showing the Russian River
contact zone. Populations are sorted by taxon, but population 22 is
intermediate in most respects. pop, Population number in study three;
n, sample size; , mean heterozygosity (direct (more ...) |
In the South Bay the genetic gap between
xanthoptica and
oregonensis is generally less than in the North Bay (Fig.
5). In the second study,
D ranges
from 0.16–0.32 (mean, 0.23) between South Bay
oregonensis
and all South Bay and East Bay
xanthoptica, with the largest
and smallest values both representing South Bay comparisons. The mean
is identical for South Bay and East Bay comparisons. Two populations
(one small sample from the east slopes of the Santa Cruz Mountains and
the other from the Pacific coastal zone of the mid-peninsula) appear to
be admixed, although it is more difficult to detect possibly diagnostic
loci than in the North Bay. The coastal population (
n =
7) is genetically equidistant between the two taxa (
D =
0.11–0.29, mean 0.20 to
xanthoptica; 0.21–0.24 to
oregonensis). In the third study,
D between South
Bay
oregonensis and
xanthoptica ranges from 0.22
to 0.35 (mean, 0.28). One population appears to be admixed
(
D = 0.17–0.34 to South Bay
xanthoptica;
D = 0.17–0.22 to South Bay
oregonensis,
some only ≈5 km distant), but it is a small sample (
n
= 3) and distances are high because of sampling effects. Distances in
the third study would be expected to be greater than in the second,
because only more variable, potentially diagnostic loci were selected
for study. The values in Fig.
5 reflect the likely upward bias.
| Figure 5 Modern barriers to dispersal in the San Francisco
Bay area for taxa discussed in this paper. Genetic distances between
selected populations indicated on lines connecting them. Bold
D values are between taxa. |
Distances between xanthoptica and eschscholtzii
are slightly less than between xanthoptica and
oregonensis: D = 0.21–0.37 between East Bay
xanthoptica and eschscholtzii, and 0.14–0.32
between South Bay xanthoptica and eschscholtzii.
In the third study D = 0.15–0.39, mean 0.23 for South
Bay xanthoptica and eschscholtzii;
D = 0.24–0.38, mean 0.29 for eschscholtzii
to oregonensis. Populations of xanthoptica and
eschscholtzii that are closest geographically have the
lowest values.
More than 80 populations have been sampled for sequence variation in
the cytochrome
b gene (ref.
15 and unpublished data).
Corrected sequence divergence between the three taxa considered here is
0.05–0.07 for
xanthoptica to
eschscholtzii, in
excess of 0.09 for
eschscholtzii to
oregonensis,
and in excess of 0.11 for
xanthoptica to
oregonensis. There is substantial variation within all taxa,
but especially
oregonensis (which is paraphyletic with
respect to this gene). A phylogenetic analysis of sequence data
indicates that
xanthoptica and
eschscholtzii are
sister taxa and form a monophyletic group (
15), but their closest
relative is unclear and recent analysis of a much larger sample has
failed to find a closest relative. The base of the cytochrome
b gene tree for the
Ensatina complex is unstable.
The contact zones detected with allozymes described herein are also
detectable with mitochondrial DNA; a detailed study by D. Parks in this
laboratory is in progress.