Fine-scale Spatial Genetic Structure in the Cooperatively Breeding Brown-headed Nuthatch (Sitta pusilla)
Sarah. E. Haas, James A. Cox, Jordan V. Smith, and Rebecca T. Kimball
Southeastern Naturalist, Volume 9, Issue 4 (2010): 743–756
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2010 SOUTHEASTERN NATURALIST 9(4):743–756
Fine-scale Spatial Genetic Structure in the Cooperatively
Breeding Brown-headed Nuthatch (Sitta pusilla)
Sarah. E. Haas1,2, James A. Cox3, Jordan V. Smith1,
and Rebecca T. Kimball1,*
Abstract - Many cooperatively breeding birds exhibit fine-scale spatial genetic
structure as a result of restricted dispersal and habitat specialization. Sitta pusilla
(Brown-headed Nuthatch) is a cooperatively breeding bird restricted to mature
pine-dominated forests of the southeastern United States and has been undergoing
population declines across most of its range. We used five polymorphic microsatellite
loci developed for this species to examine fine-scale spatial genetic structure within
a site in northern Florida as well as broader genetic structure among this site and two
other sites (a second in northern Florida and one in southern Georgia). Spatial autocorrelation
analyses within the more densely sampled site detected positive spatial
genetic autocorrelation up to 1300 m in males when auxiliary males were included,
but no autocorrelation was found in females or in males when auxiliary males were
excluded. At the broader scale, we found small but significant genetic differentiation
among all three populations, including two sites that were separated by less than 40
km of suitable habitat. Our results suggest that both sexes of the Brown-headed Nuthatch
exhibit limited dispersal, with philopatric male auxiliaries contributing to more
pronounced genetic structure over small geographic distances compared to females.
Our sampled populations were in a region where much suitable habitat remains, yet
we still observed limited dispersal. This finding suggests that in more fragmented
regions, populations may become isolated and at risk of extinction.
Cooperative breeding in birds may occur when species have a limited
resource that selects for offspring that remain in the natal territory near
that resource (Stacey and Ligon 1987). As such, these species may exhibit
restricted dispersal and habitat specialization, both of which may make them
particularly sensitive to habitat loss, fragmentation, and degradation by hindering
migration to distant habitat patches (Walters et al. 2004). These characteristics
may also facilitate the formation of spatial genetic structure among
populations as well as fine-scale genetic structure within subpopulations
(Woxvold et al. 2006), thereby influencing patterns of genetic relatedness
over microgeographic scales. In cooperatively breeding birds, males often
inherit their natal territory or breed in neighboring territories (Greenwood
1980, Koenig et al. 1992), which may result in related demes of philopatric
1Department of Biology, University of Florida, PO Box 118525, Gainesville, fl32611. 2Current address - Center for Applied GIS, Department of Geography and
Earth Sciences, University of North Carolina- Charlotte, 9201 University City Boulevard,
Charlotte, NC 28223. 3Tall Timbers Research Station, 13093 Henry Beadel
Drive, Tallahassee, fl32312. *Corresponding author - email@example.com.
744 Southeastern Naturalist Vol. 9, No. 4
males, with less spatial genetic structure in the dispersing females (Double
et al. 2005, Painter et al. 2000, Temple et al. 2006, Woxvold et al. 2006),
although there are exceptions to this pattern (Beck et al. 2008).
Sitta pusilla (Latham) (Brown-headed Nuthatch) is a small (≈10 g),
non-migratory, cooperatively breeding passerine restricted to mature pinedominated
forests of the southeastern United States (Withgott and Smith
1998). The percentage of breeding territories in Florida containing one or
more auxiliary adults has been documented to vary from 10–32% among
sites and years (Cox and Slater 2007). Most groups containing more than two
adults consist of a breeding pair and a second-year (i.e., hatched the previous
breeding season) auxiliary male that is related to at least one breeding
adult (Cox and Slater 2007), though a few groups have been shown to have
up to three auxiliary males (J.A. Cox, unpubl. data). Breeding pairs maintain
long-term pair bonds and are highly sedentary after territory establishment,
frequently excavating nests within 100 m of nests used the previous year
(Cox and Slater 2007). The average distance between nearest neighboring
nests in north Florida is approximately 198.5 m (SD = 90.7) (Cox and Slater
2007). Field observations suggest natal philopatry is heavily male-biased,
although female helpers have been documented (Cox and Slater 2007).
Most observed dispersal for males occurs within 300 m of the natal territory,
which is generally the nearest neighboring territory (Cox and Slater 2007).
In contrast, median dispersal for the limited number of recaptured females
(n = 8) is 1450 m (J.A Cox, unpubl. data).
These characteristics of Brown-headed Nuthatches—territory site fidelity,
natal philopatry, limited dispersal, and habitat specialization (Cox
and Slater 2007, Lloyd and Slater 2007, Withgott and Smith 1998)—are
typical of other cooperative breeding birds and have been suggested to
increase susceptibility to habitat degradation and lead to fine-scale spatial
genetic structure (Walters et al. 2004, Woxvold et al. 2006). Long-term
population declines throughout the range of Brown-headed Nuthatches, attributed
to human development, fire suppression, and logging, have led to
increased conservation concern for this species (Sauer et al. 2005, USFWS
2002, Withgott and Smith 1998). Despite ongoing population declines and
the prediction that populations will continue to decline as forests become
further fragmented (Jackson 1988), there remains little research on the
Molecular assessments that examine spatial genetic structure within
and among populations could be useful for the conservation and management
of the Brown-headed Nuthatch by providing a greater understanding
about levels of genetic variability, dispersal patterns, and the probability
that populations may become isolated and eventually go extinct. In this
study, we examined fine-scale spatial genetic structure in the Brown-headed
Nuthatch using recently developed microsatellite markers for this species
(Haas et al. 2009). Samples were collected within a single well-studied site
2010 S.E. Haas, J.A. Cox, R.T. Kimball, and J.V. Smith 745
in northern Florida to address fine-scale genetic structure, and compared
with two other sampling areas in northern Florida and southern Georgia to
examine broader-scale spatial genetic structure.
Two sampling sites were located in northern Florida (Tall Timbers
Research Station in Leon County [TTRS; n = 70], and Osceola National
Forest in Baker County [ONF; n = 16]) and one site in southern Georgia
(Pebble Hill Plantation in Grady County [PHP; n = 17]) (Fig. 1). TTRS
encompasses 1630 ha and is dominated by upland pine habitats consisting
primarily of Pinus taeda L. (Loblolly Pine) and P. echinata P. Mill (Shortleaf
Pine). PHP consists of 1214 ha and has a mix of mature P. palustris
P. Mill (Longleaf Pine) and pine habitats similar to TTRS, while ONF
encompasses 63,631 ha and is dominated by pine flatwoods and cypresshardwood
swamps. Sampling at each site was conducted from February
through May of 2006 using mist-netting procedures described in Cox and
Figure 1. Maps showing the sampling sites used in this study. (a - inset) The three
sampling localities used in this study, including Tall Timbers Research Station
(TTRS, n = 70, lat/long: 30°39´N, 84°12´W), Pebble Hill (PHP, n = 17, lat/long:
30°45´N, 84°07´W), and Osceola National Forest (ONF, n = 16, lat/long: 30°19´N,
82°21´W); (b) The spatial configuration of sampled territories (n = 36, 40% of known
territories during the two years of study) at TTRS.
746 Southeastern Naturalist Vol. 9, No. 4
Adult birds from all three field sites were mist-netted, sampled for blood
(20–40 μL), banded, and released in the same location. The TTRS samples
were used for spatial autocorrelation analysis and consisted of 70 birds from
36 territories, which represented approximately 40% of known territories
on TTRS during the study. Of these 70 individuals, 33 were females and 37
were males, with the latter including eight auxiliary males. Only birds from
TTRS were color-banded, as these individuals have been monitored at TTRS
since 2001; monitoring methods can be found in Cox and Slater (2007).
Breeding status (i.e., breeder versus auxiliary) of individuals within groups
from TTRS that contained more than two adults was determined using
behavioral observations (e.g., dominance, incubation, and copulation) and
information from previous breeding seasons if available. The breeding status
of adults at PHP and ONF was unknown, and sampled birds at these sites
were fitted with a single federal band. Sampling locations were geographically
referenced with Universal Transverse Mercator (UTM) coordinates
using a hand-held global positioning system; nest locations were assumed
to represent the center of each territory for spatial autocorrelation analysis.
Blood samples collected in the field were stored in 1 mL of lysis buffer (0.1
M Tris-HCl, pH 8.0, 0.1 M EDTA, 0.01 M NaCl, 1% SDS).
DNA extraction, PCR amplification, and genotyping
Genomic DNA was extracted using a PUREGENE® DNA Purification Kit
(Biozym, Hess. Oldendorf, Germany), and molecular sexing for this sexually
monomorphic species was performed following procedures outlined in
Fridolfsson and Ellegren (1999). We used five polymorphic di-nucleotide
microsatellite markers specific to the Brown-headed Nuthatch to genotype
all individuals used in this study: SpuL5-6, SpuA6, SpuE19, SpuL4-31, and
SpuL4-3 (Haas et al. 2009). The microsatellites were amplified by PCR, with
each 10-uL reaction volume consisting of 1X PCR buffer (10mM Tris-HCl,
50mM KCl, 1.5mM MgCl2), 0.2 mM of each dNTP, 0.2 U Taq polymerase
(New England BioLabs), 0.3 μM of the forward and reverse primer, and
8 ng of genomic DNA. Magnesium concentrations and cycling conditions
can be found in Haas et al. (2009). Allele sizes were determined using a
MegaBACE 1000 DNA Sequencer (Amersham, Sunnyvale, CA), and raw
data were analyzed using GeneMarker® v.1.5 (SoftGenetics LLC, State College,
Genetic analyses included exact tests for departures from Hardy-Weinberg
equilibrium (HWE) using a Markov chain method with 5000 iterations
in GENEPOP, version 3.4 (Raymond and Rousset 1995). GENEPOP was
also used to evaluate linkage disequilibrium within each sampling area.
Auxiliary adults were excluded from these analyses because relatedness
between auxiliary and breeding adults could bias results. When performing
2010 S.E. Haas, J.A. Cox, R.T. Kimball, and J.V. Smith 747
multiple comparisons, sequential Bonferroni corrections were used to reduce
global Type I error (Rice 1989). Average number of alleles, observed
and expected heterozygosity, mean proportion of individuals genotyped,
and presence of null alleles were calculated using CERVUS, version 2.0
(Marshall et al. 1998).
Spatial autocorrelation analysis was performed using GenAlEx, version 6
(Peakall and Smouse 2006) to examine fine-scale spatial genetic structure
within TTRS. GenAlEx generates an autocorrelation coefficient, r, which
provides a measurement of the pairwise genetic similarity of individuals
whose geographic separation falls within a specified distance class. We
specified a base distance class size of 100 m for 15 runs so that the first
distance interval would calculate r based on all pairwise comparisons within
a distance of 0–100 m, the second analysis for 0–200 m, and so on until the
last run (i.e., 0–1500 m) was completed. This base distance class was chosen
because it was the smallest distance interval that still encompassed multiple
territories; four of the 36 (11.1%) territories from TTRS had sampled nearest
neighboring territories within this distance. Autocorrelation coefficients
were calculated for four sampling categories: (1) all individuals; (2) all
males (includes auxiliary males); (3) dominant males (breeding males only);
and (4) females. These non-independent categories were chosen in order to
explore the effects of sex and the presence of auxiliary adults on patterns
of fine-scale genetic relatedness. We did not analyze auxiliary males as a
separate sampling category due to the small sample size obtained for these
individuals (n = 8). Statistical significance (P ≤ 0.05) was tested in GenAl-
Ex6 using 1000 random permutations.
We used ML-RELATE (Kalinowski et al. 2006) to estimate relatedness
for pairs of individual dominant males and females separately within TTRS.
This program calculates maximum likelihood estimates of relatedness (r)
from co-dominant genetic data. Geographic distances separating pairwise
comparisons where r ≥ 0.50 were recorded for each sex. The statistical
software R (R Development Core Team 2008) was then used to perform a
one-tailed Wilcoxon rank sum test to assess whether the average geographic
distance separating related males differed significantly from that of related
females and a Levene’s test of homogeneity of variances was performed to
determine whether differences existed in the variation between male and female
distances. This additional approach for investigating fine-scale spatial
genetic structure was performed because spatial autocorrelation procedures,
which analyze all individuals located within user-specified distance classes,
may not entirely capture the underlying spatial genetic structure if sampling
is not exhaustive, as was the case at TTRS. We also estimated relatedness for
pairs of putatively related auxiliary and dominant individuals at territories
where helpers occurred.
We used F-statistics (Wright 1951) to assess genetic differentiation
among the three sampling sites. We calculated both global and pairwise Fstatistics
using approaches in Weir and Cockerham (1984), which corrects
748 Southeastern Naturalist Vol. 9, No. 4
for sample size variation among sampling units. We tested for genetic differentiation
in GENEPOP using Markov chain parameters that included
a dememorization number of 5000, 500 batches, and 5000 iterations per
batch (Guo and Thompson 1992). Global FST greater than zero indicates
greater subdivision of genetic variance among groups than within groups,
while pairwise FST estimates genetic differentiation between specific sampling
The five polymorphic loci had an average observed heterozygosity of
0.73; the average number of alleles per locus was 19.40 (range = 12–28)
(Table 1). Excluding auxiliaries, one locus (SpuL4-31, P = 0.0026) within
TTRS and one locus (SpuL4-3, P = 0.0016) within ONF deviated from
HWE following Bonferroni correction for multiple tests. These deviations
most likely arose from the presence of null alleles specific to these
sampling areas (null allele frequency estimates: SpuL4-31 = 0.10 in TTRS,
SpuL4-3 = 0.14 in ONF). None of the remaining loci showed evidence for
null alleles. Linkage disequilibrium was not detected within population
samples (P > 0.05), and the average proportion of individuals genotyped at
all five loci was 0.94.
Spatial genetic structure
Of the 70 individuals sampled from TTRS (n = 33 females, n = 37
males), eight of these were auxiliary males associated with seven of the 36
(19.4%) sampled territories. No female helpers were identified. Prior field
data available for two of these auxiliary individuals indicated that both were
banded the previous year as nestlings at the nest of the male they were currently
assisting (J.A. Cox, unpubl. data), and relatedness estimates (r ≥ 0.50)
confirmed parent-offspring relationships for these two pairs. Prior field data
were also available for one additional auxiliary individual that was sampled
as an adult helping at the same nest the year before; however, relatedness estimates
between this individual and the dominant male revealed an absence
of genetic relatedness (r = 0.00). Of the remaining five auxiliary males, in
Table 1. Allelic diversity of Brown-headed Nuthatches from three sampling sites (TTRS, ONF,
PHP) using five polymorphic microsatellite markers. k = number of alleles (number of unique
alleles in parentheses); HO = observed heterozygosity.
SpuA6 SpuE19 SpuL5-6 SpuL4-31 SpuL4-3
Locus k HO k HO k HO k HO k HO
TTRS (n = 70) 13 (5) 0.63 15 (7) 0.71 24 (6) 0.84 11 (2) 0.67* 20 (5) 0.73
ONF (n = 16) 10 (2) 0.75 5 (0) 0.63 13 (3) 0.75 7 (1) 0.88 12 (3) 0.67*
PHP (n = 17) 9 (1) 0.73 8 (1) 0.94 14 (1) 0.82 8 (0) 0.82 15 (1) 0.75
Combined (n = 95) 17 0.66 16 0.72 28 0.83 12 0.73 24 0.76*
*Deviation from Hardy Weinberg Equilibrium (auxiliary individuals were omitted from HWE
2010 S.E. Haas, J.A. Cox, R.T. Kimball, and J.V. Smith 749
which previous field data were unavailable, only a single individual exhibited
parent-offspring relatedness estimates with the dominant male, while
the other four auxiliaries had estimates of approximately r = 0.00.
Spatial autocorrelation analyses revealed that the all males category exhibited
significant positive genetic autocorrelation at all distance intervals
until 1300 m (range of significance for each distance class from 0–1300 m:
P = 0.002 to P = 0.043), except for 0–1000 m (P = 0.066), with higher autocorrelation
detected at small geographic distances followed by a decrease in
genetic relatedness as a function of geographic distance (Fig. 2a). A similar,
although non-significant, pattern was found in the all individuals category
(Fig. 2b), which also included females and auxiliary males. Dominant males
(Fig. 2c) and females (Fig. 2d) did not exhibit significant spatial genetic
autocorrelation nor demonstrate a pattern of decreasing autocorrelation as
geographic distance increased, suggesting that auxiliary males were driving
the observed spatial genetic patterns.
Using ML-RELATE, a total of 19 pairwise comparisons among the sampled
dominant males (n = 29) and 31 pairwise comparisons among the sampled
females (n = 33) from TTRS were observed that exhibited relatedness r ≥ 0.50.
The average distance separating related pairs of dominant males (1585 m) and
pairs of related females (1780 m) did not differ significantly (P = 0.40). The
test of homogeneity of variances revealed that the variance in the distances
separating pairs of related males and females was not statistically different
(P = 0.32). However, the range of distances separating males (193–2423 m)
was narrower than that for females (192–3799 m), and a test of homogeneity
of variances using only the top 50% of the distance values revealed significant
differences (P = 0.02) between the sexes (Fig 3).
The within-population results suggest there can be longer-range dispersal,
but it is likely limited. Consistent with this, examination across
populations resulted in small but significant genetic structure (FST = 0.01,
P < 0.001) among all three sampled locations. Tests of genetic differentiation
for pairwise estimates of FST among the three sites were also statistically
significant (FST range = 0.01–0.02; P < 0.01). We did not compare pairwise
FST for males and females separately due to the smaller sample sizes at PHP
Prior field data from TTRS based on color-band re-sighting of Brownheaded
Nuthatches suggest that males exhibit high rates of natal philopatry
and typically disperse short distances, while females help parents less frequently
and disperse greater distances than males (Cox and Slater 2007).
In this study, we sampled seven territories (19.4%) at TTRS that included
auxiliary males, which is in accordance with previous estimates of 10–32%
of breeding territories containing one or more auxiliary adults (Cox and
Slater 2007). The observation of unrelated auxiliaries has been previously
documented in Brown-headed Nuthatches, in which adult males provided
750 Southeastern Naturalist Vol. 9, No. 4
assistance at neighboring nests following the failure of their own nests or inability
to acquire their own territory (i.e., facultative helping; Cox and Slater
2007). In one of these cases in our study, the auxiliary was related to the
female but not the dominant male, and may have resulted from an extra-pair
copulation. For the others, we have insufficient data to determine whether
Figure 2. Genetic autocorrelation (r) across geographic distances. The permuted
95% confidence interval is shown (dashed lines represent the 25th and 975th limits).
Significant spatial genetic structure occurs when r exceeded the confidence intervals.
(A) all males (n = 37), (B) all individuals (n = 70), (C) dominant males (n = 29), and
(D) females (n = 33).
2010 S.E. Haas, J.A. Cox, R.T. Kimball, and J.V. Smith 751
these are unrelated individuals assisting a nest or offspring from previous
years resulting from extra-pair fertilizations.
This pattern of male-biased natal philopatry and limited dispersal should
lead to greater fine-scale spatial genetic structure in the philopatric sex, with
less structure in the dispersing sex (Peakall et al. 2003). Spatial autocorrelation
analysis revealed significant fine-scale genetic structure for all males,
but not just the dominant males. The difference is likely due to related
auxillaries within natal territories, to unrelated auxillaries that are likely
extra-pair offspring sired by neighboring males, and possibly from offspring
of neighboring territories that dispersed to become auxillaries. Other studies
implementing spatial autocorrelation analyses for assessing fine-scale spatial
genetic structure in cooperatively breeding birds also detected stronger
positive autocorrelation in the dispersal-restricted sex when auxiliary adults
were included in the analyses, and attributed these patterns to auxiliary individuals
being related to dominant individuals (Double et al. 2005, Temple
et al. 2006).
In spatial autocorrelation, the distance class at which genetic autocorrelation
is no longer significantly positive approximates the extent of
Figure 3. Boxplot illustrating the geographic distances (in meters) separating pairwise
comparisons of related (r ≥ 0.50) individuals for each sex (F = female, M = male).
752 Southeastern Naturalist Vol. 9, No. 4
detectable positive genetic structure (Peakall et al. 2003), and is similar to
the “genetic neighborhood” of a population (Golenberg 1987, Wright 1946).
In many cooperatively breeding species, these neighborhoods are characterized
by high genetic relatedness in the philopatric sex (Daniels and Walters
2000, Hegner and Emlen 1987). Spatial autocorrelation revealed significant
positive genetic structure among all males extending beyond six average
territory widths (1300 m, average territory width 200 m), excluding a single
distance class (0–1000 m) that was not significant. This estimate is similar
to field observations, which indicate that the average dispersal distance for
second-year males dispersing more than two territories from the natal territory
is 1358 m (Cox and Slater 2007). Pairwise estimates of relatedness
suggested that the average geographic distance separating related males
(excluding auxiliaries) at TTRS was approximately 1600 m, only slightly
higher than the genetic neighborhood estimate of 1300 m for all males using
spatial autocorrelation. Although the autocorrelation analysis did not detect
statistical significance in dominant males for any of the distance classes,
spatial autocorrelation takes into account all sampled individuals within a
user-specified distance class regardless of genealogical relationship. Not all
territories at TTRS could be sampled, and it is possible that denser sampling
might reveal positive spatial autocorrelation in both all males and the subset
dominant males, as was detected in Malurus cyaneus (Ellis) (Superb Fairywren)
and Ramphocinclus brachyurus (Vieillot) (White-breasted Thrasher)
(Double et al. 2005, Temple et al. 2006). Despite differing methodologies,
both approaches suggest that natal dispersal and genetic neighborhoods of
male Brown-headed Nuthatches occur within one to two kilometers of the
Contrary to field-based expectations of greater female dispersal, the average
geographic distance found between related pairs of females was only
200 m greater than that for related dominant males. This finding might
suggest that females are not dispersing substantially greater distances than
males, in contrast to the low mark-recapture success of females at TTRS
(Cox and Slater 2007). However, there was a statistically significant difference
in the variance of distances separating pairs of males and females
when only the top 50% of observations were used, and the maximum
distance between related females is much larger (1.4 km, or approximately
seven territory widths) than that between males. These findings suggest
that females may account for most long-distance dispersal events and are
likely important for maintaining genetic exchange among neighboring
and potentially fragmented populations. Moreover, the negative, albeit
statistically non-significant, spatial autocorrelation detected in females at
the smallest distance intervals could reflect the propensity of females to
disperse greater distances from the natal territory as compared to males, as
suggested by field observations (Cox and Slater 2007; J.A. Cox, unpubl.
data). Given the high variance in distance between related females, it may
2010 S.E. Haas, J.A. Cox, R.T. Kimball, and J.V. Smith 753
require much larger sample sizes for females to detect greater female dispersal
using spatial autocorrelation.
Supporting the limited size (less than 2 km) of male genetic neighborhoods
observed at TTRS, analysis of broader-scale genetic structure among the
three sampling localities suggested genetic differentiation can take place
over small geographic distances in the Brown-headed Nuthatch. Samples
from TTRS and PHP were separated by less than 40 km of suitable habitat,
yet still exhibited small but significant genetic differentiation. McDonald
et al. (1999) reported that genetic differentiation among populations of
cooperatively breeding Aphelocoma coerulescens (Bosc) (Florida Scrubjay)
was three times higher than in its nonsocial sister species, Aphelocoma
californica (Vigors) (Western Scrub-Jay). The authors attributed this finding
to differences in the ecology of the Florida Scrub-Jay, including the highly
sedentary lifestyle and habitat specialization of this cooperatively breeding
species, features also shared by Brown-headed Nuthatches.
Conservation and management implications
Molecular genetics approaches are useful for assessing levels of relatedness
among individuals within small and potentially isolated populations as
well as for inferring patterns of gene flow both within and among populations
(Allendorf and Luikart 2007). Such information can be valuable for
management objectives that seek to preserve the genetic health of threatened
species and may help to prevent the need for more drastic management actions
such as “genetic rescue”, in which translocations of individuals are
needed to maintain adequate levels of genetic variation in a population
(Tallmon et al. 2004). This preservation of within-population genetic diversity
may be particularly important for cooperatively breeding species, such
as the Brown-headed Nuthatch, since these species often exhibit sedentary
lifestyles, natal philopatry, and restricted dispersal (Walters et al. 2004,
Woxvold et al. 2006).
This paper provides the first assessment of genetic structure in the cooperatively
breeding Brown-headed Nuthatch. It has been suggested that
this species seldom ventures from pine-dominated forests due to their specialized
habitat requirements and limited dispersal (Cox and Slater 2007,
Lloyd and Slater 2007, Wilson and Watts 1999, Withgott and Smith 1998),
which has led to concerns that individuals will be unlikely to recolonize
distant fragments upon local extirpation (Withgott and Smith 1998). Our
results, which demonstrate genetic differentiation among geographically
close populations, are consistent with this suggestion. However, the differences
we found are small, and the data from TTRS suggest that some
individuals are likely to disperse longer distances. Thus, at least in areas
where sufficient suitable habitat remains, there may be sufficient gene flow
to prevent excess inbreeding and facilitate recolonization of extirpated
populations if necessary.
754 Southeastern Naturalist Vol. 9, No. 4
Additional molecular genetic studies of the Brown-headed Nuthatch
that analyze spatial genetic structure in relation to specific landscape features
such as habitat fragmentation (e.g., landscape genetics; Manel et al.
2003), as well as studies that enable a better understanding of their genetic
mating system will be important to fully understand how to best conserve
and manage this little-studied species. These areas of research will be especially
important given the prediction that populations of Brown-headed
Nuthatches will continue to become further isolated as habitat fragmentation
of southeastern pine forests proceeds (Jackson 1988).
We thank Ed Braun, Scott Robinson, and Jena Chojnowski for insightful commentary
on the manuscript. Lora Loke, Sergio Gonzalez, and Vanessa Schipani
provided helpful field and laboratory assistance. This project was supported in part
by the Wildlife Research Endowment at TTRS and a Riewald-Olowo Grant from
the Department of Biology at the University of Florida. This work conforms to the
legal requirements of the United States, including those related to animal conservation
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