THE USE OF MOLECULAR MARKERS IN WILD TURKEY MANAGEMENT
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THE USE OF
MOLECULAR MARKERS
IN WILD TURKEY
MANAGEMENT
Emily K. Latch1 Karen E. Mock
Department of Forestry and Natural Resources, Department of Fisheries and Wildlife,
715 W. State Street, Purdue University, 5230 Old Main Hill, Utah State University,
W. Lafayette, IN 47907, USA Logan, UT 84322, USA
Olin E. Rhodes, Jr.
Department of Forestry and Natural Resources,
195 Marstellar Street, Purdue University,
W. Lafayette, IN 47907, USA
Abstract: A variety of genetic markers now are available for use in the management and conservation of wildlife
species. In the wild turkey (Meleagris gallopavo), these markers have been used to address questions at levels
ranging from the individual to the subspecies, and with issues ranging from species-wide evolution to forensics.
Genetic studies involving translocated populations have provided managers with additional information to consider
when designing optimal translocation strategies to maximize growth and long-term stability of such populations.
In this paper, we discuss the molecular markers available for wild turkeys, and review their applications in wild
turkey management, including subspecies identification, intraspecific hybridization, domestic introgression, genetic
bottlenecks, population structure, gene flow, cryptic behavioral and social patterns, and forensics.
Proceedings of the National Wild Turkey Symposium 9:33–44
Key words: AFLP, allozyme, DNA sequencing, gene flow, genetic, hybridization, Meleagris gallopavo, micro-
satellite, mitochondrial, molecular marker, population, subspecies, translocation.
Genetic markers have become a standard tool in However, it also is clear that the selection of the most
the management and conservation of wildlife species, appropriate class of genetic markers, both in terms of
enabling scientists to address wildlife management inheritance patterns and rates of evolution, is important
questions at levels of biological resolution that previ- if these tools are to be applied successfully at varying
ously had been unattainable with traditional tech- scales of biological organization.
niques. When integrated with information from disci- In the wild turkey, a number of different types of
plines such as ecology, morphology, or paleontology, molecular markers have been developed. These tools
genetic data allow us to better understand evolutionary have been used in a variety of different applications
and demographic phenomema such as population to address management-oriented concerns at scales
structure (Sarre 1995, Sinclair et al. 1996, Kyle et al. ranging from the subspecies to the flock. Molecular
2000), dispersal rates (Beheler 2001, Richardson et al. markers also have been used to investigate evolution-
2002, van Hooft et al. 2003, Zenger et al. 2003), pop- ary relationships among subspecies and populations.
ulation bottlenecks and range expansion (Rogers and In this paper, we will provide a brief review of the
Harpending 1992, Rogers 1995, Luikart et al. 1998), molecular tools that are available for use in wild tur-
cryptic behavioral and social patterns (van Staaden et keys, and summarize the management-related research
that has been or is being conducted using these tools.
al. 1996, DeWoody et al. 1998, Piertney et al. 1999,
Zenuto et al. 1999, Storz et al. 2001), parentage
(DeWoody et al. 2000, Beheler et al. 2003, Carew et MOLECULAR MARKERS AVAILABLE
al. 2003, Sinclair et al. 2003, Stapley et al. 2003), hy- FOR WILD TURKEYS
bridization (Adams et al. 2003), taxonomic status
Allozymes
(Miththapala et al. 1996, Stephen et al. 2005a), and
individual identity (Cronin 1991, Guglich et al. 1994, Allozymes are alternate (allelic) forms of nuclear
Boyd et al. 2001, Manel et al. 2002). It has become DNA-encoded enzymes. Mutations in the DNA se-
apparent that the tools of modern molecular biology
hold great value for the field of wildlife management. 1 E-mail: latche@purdue.edu
3334 Managing Wild Turkey Populations
quence coding for an enzyme can induce changes in 1994). Nuclear loci represent DNA inherited from both
its protein structure. These differences in protein struc- parents, and therefore can be useful for questions fo-
ture are detectable by starch-gel electrophoresis, which cused at almost any biological scale, from establishing
separates the enzyme alleles based on size, shape, and relatedness among individuals to discernment of spe-
electrical charge. Early studies of allozyme variation cies (Sinclair et al. 2003, Verma and Singh 2003, Wil-
among populations, beginning with a series of papers liams et al. 2003a). In particular, highly polymorphic
in 1966, revealed a surprising amount of genetic var- nuclear markers, often associated with noncoding re-
iability in natural populations (Harris 1966, Hubby and gions of the genome, are essential for studies in which
Lewontin 1966, Johnson et al. 1966). Allozyme mark- individuals must be unambiguously identified (i.e.,
ers have proven to be useful for applications ranging parentage studies or assignment of unknown individ-
from characterizing broad-scale variation across a spe- uals to a population of origin; Anderson et al. 2002,
cies range to investigating local mating patterns Manel et al. 2002, DeYoung et al. 2003). However, the
(Rhodes et al. 1993, Pope 1998, Lode 2001, Gabor abundant polymorphisms that make highly variable
and Nice 2004). Analysis of allozyme markers is rel- nuclear markers attractive for applications at the in-
atively inexpensive, and the markers are codominant, dividual level can, in some cases, obscure patterns of
meaning that all variants at a locus can be visualized. differentiation at higher taxonomic levels (e.g., spe-
However, the utility of allozyme markers is limited by cies; Hedrick 1999).
low levels of polymorphism, resulting from the fact
that allozyme analysis detects only a subset of the total Microsatellites.—Nuclear microsatellites are short
variation (that which affects the migration of the en- segments of noncoding DNA (typically 2–4 base pairs
zyme through a gel). Most enzymes are not polymor- in length) which are tandemly repeated many times.
phic (e.g., average of 23% polymorphism for 551 spe- Microsatellite loci tend to mutate by adding and sub-
cies of vertebrates), and polymorphic loci rarely have tracting these segments, so allelic variation is generally
more than 3 alleles (Nevo et al. 1983). Thus, the rel- in the form of length, which is easily detectable using
atively low expense and ease of data collection often electrophoresis. Microsatellite length polymorphisms
are offset by the large number of allozyme loci typi- can be abundant within and among populations, and it
cally needed to adequately assess genetic variability in is thought that slippage during DNA replication plays
a sample. Additionally, because allozymes are ex- a major role in generating length variation among al-
pressed genes, they are subject to selection, and pat- leles (Levinson and Gutman 1987, Jeffreys et al. 1991,
terns of population variation may not always reflect Schlötterer and Tautz 1992). Suites of highly poly-
the neutral processes assumed to drive divergence and morphic microsatellite loci can provide tremendous
gene flow (Eanes 1999). discriminatory power, allowing for the unique identi-
Twenty-eight allozyme loci have been optimized fication of individuals within populations and the ex-
for surveys of genetic diversity in wild turkeys (Stan- clusion of individuals as potential parents of offspring.
gel et al. 1992). Although subsequent studies screened The highly polymorphic nature of microsatellite loci
all 28 loci, they typically found only 4–5 loci that also means that they can be prone to a phenomemon
exhibited polymorphism among the groups of interest termed homoplasy, where convergent mutations in dif-
(Leberg 1991, Leberg et al. 1994, Rhodes et al. 1995, ferent lineages have led to the same allele. Thus, al-
Boone and Rhodes 1996). Although turkeys exhibit leles that are alike may not represent common ances-
slightly fewer polymorphic loci than the average for try, resulting in inferred relationships among groups
vertebrate species, they are well within the range of that may not accurately represent evolutionary histo-
values described for bird species (Nevo et al. 1983). ries. The potentially confounding effects of homoplasy
Despite reduced genetic variability in comparison to often can be alleviated by analyzing many microsat-
DNA-based markers, allozymes are still valuable tools ellite loci.
for subspecies- and population-level applications in the Microsatellite markers are relatively inexpensive
wild turkey (Leberg 1991, Stangel et al. 1992, Leberg to analyze, and are available for countless species in
et al. 1994, Rhodes et al. 1995, Boone and Rhodes virtually every major taxonomic group. Furthermore,
1996). microsatellites developed for one species often can be
used in related taxa (Frankham et al. 2002), further
reducing the time and expense of their development
DNA-based Markers for newly studied species.
Nuclear DNA Currently, 24 microsatellite loci have been opti-
mized for use in wild turkeys. Eighteen of these loci
In recent decades we have witnessed a shift from originally were developed for domestic turkeys (Don-
protein-based (allozyme) to DNA-based marker sys- oghue et al. 1999, Huang et al. 1999, Reed et al. 2000),
tems for estimation of genetic parameters in wildlife but proved to be polymorphic in wild turkeys with
species. DNA-based markers not only reveal more ge- modifications (Shen 1999, Latch 2004). The remaining
netic variation than their allozyme predecessors, but 6 loci were developed by screening microsatellite re-
also allow investigators to choose among sets of loci peats found in wild and domestic turkey DNA se-
with different patterns of inheritance (nuclear versus quences (Latch et al. 2002). Robust subsets of these
mitochondrial DNA) or evolutionary constraints (cod- 24 loci have been used for numerous studies of wild
ing versus noncoding regions of the genome; Mitton turkey ecology and taxonomy (Mock et al. 2001, 2002,Genetic Markers for Wild Turkey Management • Latch et al. 35
2004; Latch 2004; Krakauer 2005; Latch and Rhodes taining to higher level systematics and phylogenetics
2005, 2006; Latch et al. 2006a,b). Numerous addition- (Saetre et al. 2001, Abbott and Double 2003). Because
al microsatellite loci have been developed for domestic mitochondrial sequences are generally nonrecombin-
turkeys but have not been thoroughly screened for ing, molecular clocks can be used to estimate diver-
polymorphism in wild turkeys (e.g., Reed et al. 2000, gence times of various taxa. In addition, because of
2002, 2003). Given the previous success of domestic their mode of inheritance, mitochondrial markers as-
turkey markers in their wild relatives (Shen 1999, sociated with maternal lineages are also useful for
Latch 2004, Krakauer 2005), this represents a potential questions focused on population establishment, social
reservoir of microsatellite loci for future applications. structure, and hybridization (Zink and Dittmann 1993,
In the wild turkey, the utility of nuclear microsatellites Pilgrim et al. 1998, Boyce et al. 1999, Adams et al.
has been shown for elucidating genetic structure 2003). However, despite relatively high levels of poly-
among turkey populations and identifying individual morphism at certain hypervariable regions of the mi-
animals (i.e., Latch and Rhodes 2005, Latch et al. tochondrial genome, mtDNA markers may not possess
2006b). sufficient variability for individual identification. This
low variability can be a major limitation for the use
Amplified Fragment Length Polymorphisms
of mtDNA markers in population-level studies.
(AFLPs).—Amplified fragment length polymorphism
(AFLP) is another type of nuclear DNA-based marker Control Region.—The most variable portions in
system available for rapid screening of genetic diver- the mitochondrial genome are within the control re-
sity among individuals (Vos et al. 1995, Mueller and gion (D-loop), a noncoding region. Control region se-
Wolfenbarger 1999). AFLP polymorphisms result quences frequently are the mitochondrial marker of
from differences in restriction fragment lengths caused choice for assessing patterns of genetic differentiation
by single base mutations, insertions, or deletions that below the species level. In many investigations, nucle-
create or destroy restriction enzyme recognition sites. ar markers are combined with control region data to
AFLP methods involve the detection of these sites by characterize differences in patterns of genetic differ-
polymerase chain reaction (PCR) amplification and entiation between the sexes (Scribner et al. 2001, John-
electrophoresis. Because AFLP methods can generate son et al. 2003, Zenger et al. 2003) and to provide a
hundreds of genome-wide polymorphic markers with- temporal framework for phylogenetic reconstruction.
out any prior sequence knowledge, AFLPs can be a Two sets of PCR primers have been developed to am-
powerful, low-cost tool for use in systematics and pop- plify the control region in wild turkeys. One set am-
ulation genetics, as well as for generating ‘‘DNA fin- plifies a product of approximately 1,300 base pairs
gerprints’’ for individual identification and studies of (Mock et al. 2001, 2002), and the other set amplifies
kinship (Escaravage et al. 1998, Mueller and Wolfen- a smaller product of about 500 base pairs (Latch 2004,
barger 1999, Whitehead et al. 2003). The primary lim- Latch et al. 2006b). In wild turkeys, control region
itation associated with AFLP markers is that they are sequences exhibit substantial variability at the subspe-
a dominant marker system, requiring the assumption cies and population levels. Questions concerning sex-
of Hardy-Weinberg equilibrium for the estimation of specific processes, such as sex-biased dispersal and in-
allele frequencies in populations. In addition, AFLP trogression, will benefit from the use of maternally in-
profiles can be sensitive to varying laboratory condi- herited markers such as the control region (e.g., Latch
tions, rendering them difficult to replicate over long et al. 2006b).
periods of time in different laboratories.
AFLP protocols have been optimized in wild tur- Cytochrome b.—The mitochondrial cytochrome b
key, and these markers have been used effectively to gene is a relatively large mitochondrial gene that codes
resolve evolutionary relationships among subspecies for a protein that has been well studied with respect
and to determine the subspecies of origin of a given to structure and function (Howell and Gilbert 1988,
population (Mock et al. 2001, 2002). Because of the Tron et al. 1991, Crozier and Crozier 1992). This gene
large number of polymorphic AFLP loci in wild tur- as a whole evolves relatively slowly and therefore is
key, this marker system may also prove to be infor- fairly conserved across taxonomic groups, although
mative for fine-scale questions at the population, flock, the third codon positions within the gene can show
or individual level. higher levels of polymorphism than first or second po-
sitions. Because of the conserved nature of this gene,
Mitochondrial DNA sequence polymorphisms at the DNA and amino acid
level often provide information at higher levels of bi-
In contrast to the nuclear genome, mitochondrial ological organization (e.g., species, subspecies) than
DNA (mtDNA) is cytoplasmically inherited, and thus might be achieved for more rapidly evolving markers
is derived almost exclusively from maternal lineages. such as microsatellites. Although cytochrome b has
Although the mtDNA of any individual can be unique, most often been used to describe genetic relationships
the highly conserved nature of homologous functional between subspecies, species, or genera, it may some-
genes across a wide variety of organisms allows for times be suitable for analyses at lower levels of bio-
direct comparisons of mtDNA sequences at many dif- logical organization (i.e., among populations; Wenink
ferent taxonomic scales. Thus, mitochondrial markers, et al. 1993). Cytochrome b DNA amplification and
particularly those representing coding regions of the sequencing methods have been developed in wild tur-
genome, are particularly valuable for questions per- keys, yielding high-quality sequence data from a 50036 Managing Wild Turkey Populations
base pair portion of the cytochrome b gene (Latch not uncommon. Marker-related phenomena such as ho-
2004, Latch et al. 2006a). Although there is not a sub- moplasy can confound estimates of divergence times
stantial amount of diversity in this region, pilot studies and relationships among groups, particularly at higher
suggest that cytochrome b sequences may be practical levels of biological organization. However, the inabil-
for comparisons among eastern (eastern [M. g. silves- ity of microsatellite markers to correctly resolve evo-
tris], Florida [M. g. osceola], and Rio Grande [M. g. lutionary relationships among wild turkey subspecies
intermedia]) and western (Merriam’s [M. g. merriami] does not preclude their use at the subspecies level for
and Gould’s [M. g. mexicano]) subspecies of the wild classification purposes (see Subspecies identification
turkey (Latch 2004). and hybridization in translocated populations section
below).
Latch (2004) performed a preliminary assessment
APPLICATIONS IN WILD TURKEY of the utility of cytochrome b gene sequences for re-
MANAGEMENT creating the evolutionary relationships among wild tur-
key subspecies. These data indicate that although the
Subspecies-level Applications differences between eastern (eastern, Florida, and Rio
Grande) and western turkeys (Merriam’s and Gould’s)
Subspecies Delineation in Naturally-occurring
are substantial, the relatively slow rate of evolution
Populations
within the cytochrome b gene has resulted in little or
Subspecies are taxonomic units thought to repre- no structuring among subspecies within these broad
sent evolutionary lineages below the species level. regional groups.
There is broad agreement among biologists that ge-
netic variation below the species level could be im- Subspecies Identification and Hybridization in
portant for the evolutionary flexibility of the species Translocated Populations
(Mitton and Grant 1984, Allendorf and Leary 1986).
In the wild turkey, subspecies designations coincide Although translocations have been a critical com-
with broad geographic/ecotypic regions and are pre- ponent of the successful restoration and expansion of
sumed to represent units with some degree of common wild turkey in North America (Kennamer and Ken-
ancestry and local adaptation, which has been namer 1996), the genetic implications of these trans-
achieved over many thousands of years of evolution- locations are poorly understood. Programs to reintro-
ary experience. Subspecies boundaries are an impor- duce turkeys into previously occupied habitats, or to
tant management concept, because translocations of introduce them outside their historical range, often
birds from one area to another may lead to the genetic have not considered traditional species or subspecies
‘‘swamping’’ of locally adapted populations. Because ranges. Such programs threaten to disrupt historical
translocation is one of the most widely used manage- patterns of genetic diversity and gene flow, which po-
ment practices for the wild turkey, understanding of tentially could lead to irretrievable loss of genetic rec-
historical relationships among subspecies is critical to ords of populations (Avise 2004), increased homoge-
the selection of appropriate source stock for translo- nization of subspecies and the loss of unique, locally
cations. adapted forms, not to mention forced extinctions of
Mock et al. (2002) used a combination of DNA- native populations (Avise 2004). Furthermore, some of
based markers, both nuclear (AFLPs and microsatel- these programs have led to situations in which multiple
lites) and mitochondrial (control region DNA sequenc- subspecies or variants now co-occur in regions where
es), to characterize historical patterns of genetic diver- no such associations historically existed. Such situa-
sity in relict wild turkey populations from each of the tions have immediate implications for local hybridiza-
5 recognized subspecies, and to assess the genetic va- tion between subspecies, and also mean that the best
lidity of current subspecies designations (see range source stock for a translocation may no longer be that
map available at http://www.nwtf.org/images/range which is geographically closest. Before evolutionarily
maplarge.jpg or in Tapley et al. this volume). All 3 significant trajectories within the subspecies are com-
marker types showed less genetic diversity in the pletely eroded by human-mediated movements, it is
Gould’s subspecies than in the other subspecies. Re- important to understand their historical and contem-
lationships among subspecies suggested by AFLP and porary distributions as well as the underlying genetic
control region data corroborated our understanding of basis for differentiation among them.
historical habitat continuity. Microsatellite data sug- DNA-based markers, including microsatellites,
gested somewhat different evolutionary relationships AFLPs, and mitochondrial control region sequences,
among the subspecies. Mock et al. (2002) suggested can be used to determine the origin of an individual
that the relatively small number of microsatellite loci bird that has been translocated or that has migrated
and the weak statistical support for the groupings may from one region to another (Paetkau et al. 1995, Ran-
have led to the alternate pattern; however, adding 9 nala and Mountain 1997, Cornuet et al. 1999, Pritchard
additional microsatellite loci and screening a subset of et al. 2000). Microsatellites are particularly promising
the samples used in Mock et al. (2002) did not change for this application, because of their high level of poly-
the inferred relationships among subspecies (Latch morphism, their codominance, and the replicability of
2004). Differences in the evolutionary relationships data within and among laboratories.
among groups inferred by different marker systems are In southeastern Arizona, wild turkey managersGenetic Markers for Wild Turkey Management • Latch et al. 37
were concerned that efforts to reintroduce the Gould’s migrant Rio Grande males mating with resident Mer-
subspecies into its historical range had been impeded riam’s females.
by previous reintroductions of Merriam’s turkeys into
the area. Mock et al. (2001) used molecular markers Domestic Introgression
to determine whether the turkeys currently inhabiting
Early in the history of wild turkey translocation
the Huachuca Mountains in southeastern Arizona were
programs, managers considered the potential utility of
descended from the Gould’s turkeys translocated there game-farm or domestic turkeys as source stock for
in the 1980s, or if interbreeding had occurred with translocations into the wild. One concern was that the
descendents of Merriam’s turkeys introduced to the long history of artificial selection in non-wild stock
area in 1950. Given the utility of these markers for had left these turkeys with insufficient genetic diver-
distinguishing wild turkey subspecies (i.e., Mock et al. sity for success in the wild. In 1985, Stangel et al.
2002), the authors used a combination of AFLPs, mi- (1992) initiated a survey to characterize levels of ge-
crosatellites, and control region sequences. They found netic diversity in eastern wild turkeys, game-farm tur-
that turkeys in the Huachuca Mountains consistently keys, and domestic turkeys. Using allozyme markers,
grouped with reference individuals from the Gould’s the authors found significant differences in the distri-
subspecies (from Mexico) rather than with reference bution of allele frequencies among the 3 groups. Wild
Merriam’s turkeys from central Arizona (Mock et al. turkeys exhibited levels of genetic diversity compara-
2001). Thus, these data strongly indicated that the wild ble to that of other native game birds, whereas do-
turkey population in the Huachuca Mountains was de- mestic turkeys possessed significantly less genetic di-
scended from the translocations of Gould’s turkeys versity than wild or game farm turkeys. Game-farm
made in the 1980s, and showed no evidence of inter- turkeys exhibited a large range in genetic variability,
breeding with the Merriam’s subspecies. Each of these likely due to the wide variety of different breeding
3 markers performed extremely well in this study, pro- strategies used by game farmers and the many differ-
viding managers with several cost-efficient methods ent types of farms sampled for this study (Stangel et
for distinguishing Merriam’s and Gould’s subspecies. al. 1992). The authors did not find sufficient allozyme
In Kansas, extensive translocation efforts have differentiation among wild, game-farm, and domestic
confounded subspecies distributions throughout the turkeys to permit identification of domestic introgres-
state. Today, 3 subspecies of wild turkey are believed sion in wild stock. However, a project is currently un-
to co-occur in Kansas—eastern, Rio Grande, and Mer- derway to screen a variety of DNA-based markers to
riam’s. Given the likely disruption of historical sub- assess their utility for the differentiation of wild tur-
species structure within the state, and the inability of keys from domestic breeds. A higher level of vari-
morphological methods to unambiguously resolve the ability in DNA-based markers as compared to allo-
subspecific status of turkeys, DNA-based methods zyme markers increases the probability of finding
were used to address these concerns. Microsatellites ways to detect domestic introgression into wild turkey
(Latch et al. 2006a) and control region and cyto- stock.
chrome b sequences (Latch 2004) were employed to
characterize the genetic variability of wild turkey pop-
Population-level Applications
ulations throughout Kansas, in an effort to clarify the
current distribution of pure and mixed turkey subspe- Genetic Bottlenecks/Founder Effects
cies. These molecular data were able to delineate sub-
Genetic bottlenecks, resulting in a loss of genetic
species boundaries and detect zones of hybridization diversity, can occur as a result of genetic drift when a
between them. Furthermore, these data clearly indi- population is reduced in size for many generations
cated areas in which undocumented translocations sig- (Nei et al. 1975). Founder effects, a related phenom-
nificantly impacted the subspecific composition of tur- enon, refer to the change in allelic composition when
keys in particular regions. a small subset of one population is used to establish a
In the Davis Mountains of Texas and within near- new population, leading to allele frequencies that dif-
by Rio Grande turkey populations, Latch et al. (2006b) fer from those of the original population. In both phe-
assessed the subspecific status and degree of hybrid- nomena, the effect is more pronounced when the bot-
ization of individuals within an introduced population tlenecked or founding population is small (Baker and
of Merriam’s turkeys. Data from the Merriam’s source Moeed 1987, Merila et al. 1996, Mock et al. 2004).
population in New Mexico was used as a baseline ref- Populations established via translocation programs are
erence for the genetic characteristics of the Merriam’s at risk for diversity losses and changes in allelic com-
subspecies. Nineteen years following the introduction position as a result of both processes. A number of
event, microsatellite data indicated that the genetic in- empirical studies have demonstrated significant reduc-
tegrity of the introduced population of Merriam’s tur- tions of genetic variability in translocated wildlife pop-
keys in the Davis Mountains Preserve has been eroded ulations relative to their sources (Fitzsimmons et al.
by both immigration from and hybridization with near- 1997, Williams et al. 2000, Williams et al. 2002,
by Rio Grande populations. Data from the mitochon- 2003b). Translocated populations also may exhibit
drial control region allowed for further characteriza- shifts in allele frequency distributions relative to their
tion of parental contributions to hybrid individuals, source (Fitzsimmons et al. 1997, Luikart et al. 1998,
and indicated that most hybrids were the result of im- Rowe et al. 1998, Williams et al. 2000), relative to38 Managing Wild Turkey Populations
other native populations (Baker and Moeed 1987, possible. However, if dispersal among populations is
Perez et al. 1998, Stephen et al. 2005b), or relative to low, genetic similarities between a reintroduced pop-
theoretical expectations (Scribner and Stuwe 1994, ulation and its source may persist.
Fitzsimmons et al. 1997). Many, if not most, extant Allozyme, microsatellite, and control region data
wild turkey populations have been established as a re- have been used to characterize interactions among re-
sult of translocation, both within and beyond historical introduced populations and between reintroduced and
range boundaries. As a result the loss of genetic di- native populations (Leberg et al. 1994, Latch and
versity in populations and shifts in allelic frequency Rhodes 2005). Leberg et al. (1994) utilized allozymes
distributions are potentially very serious issues in wild to determine whether the genetic similarities among
turkey management. populations were more affected by geographic prox-
Leberg (1991) used allozyme markers to deter- imity or by shared reintroduction histories. The authors
mine if populations of wild turkeys established as a found that reintroduced populations from common
result of translocations had higher levels of genetic sources were more similar than expected given their
differentiation among populations than turkeys that geographic proximity, even decades after the reintro-
have not experienced founder events. Although the to- duction events. Therefore, it seems that although dis-
tal amount of genetic differentiation he found was low, persal likely has occurred, it has not resulted in a de-
likely due to the time of sample collection (see Social tectable relationship between genetic and geographic
and Behavioral Dynamics section below) and the low distance, as would be expected in naturally occurring
variability of allozymes, it nonetheless was evident populations. These results also suggested that while
that reintroduced wild turkey populations exhibited founders make genetic contributions to the populations
higher levels of genetic differentiation among popu- into which they are released, they may have a minimal
lations (presumably due to genetic drift occurring in- effect on nearby populations (although the reverse is
dependently among populations) than did relict pop- not necessarily true; see Subspecies identification and
ulations that had not experienced severe reductions in hybridization in translocated populations section
size. above).
Ten years later, Mock et al. (2001) used microsat- Latch and Rhodes (2005a) also used microsatellite
ellite, control region, and AFLP data to detect reduced and control region sequences to demonstrate that the
genetic diversity in a reintroduced population of genetic relationships between reintroduced populations
Gould’s turkeys in the Huachuca Mountains of south- and their sources are not quickly eroded by dispersal
eastern Arizona compared to relict Gould’s turkey pop- from nearby populations, corroborating the findings of
ulations in Mexico. Thus, Mock et al. (2001) recom- Leberg et al. (1994). Taking advantage of well-docu-
mended that although this population is stable, it may mented reintroduction histories of turkey populations
benefit from supplementation of turkeys from the more in Indiana, the authors assessed the degree to which
diverse relict populations. gene flow among reintroduced populations has ob-
Mock et al. (2004) assessed the genetic impact of scured genetic signatures left by the founding events.
3 well-documented translocation events in the Merri- Effects were measured in regions characterized by
am’s subspecies, each occurring approximately 50 high habitat continuity and a high potential for dis-
years ago. These translocations differed in the number persal among populations and as well as in regions
of source individuals used, the number of trapping where the opportunity for dispersal among populations
sites used to capture source individuals, and the size was reduced due to the low density of turkey popu-
of the habitat into which founders were established. lations. The genetic signatures left by reintroduction
Microsatellite data indicated that all 3 translocations events were strongly evident in most populations, even
exhibited reduced genetic diversity relative to their after several decades. Latch and Rhodes (2005a) fur-
founding populations, including 1 translocated popu- ther showed that the density of populations in a region
lation that is now very large and robust. Unfortunately, did not significantly affect these relationships. For
these results suggest that losses in genetic diversity are each of the reintroduced populations, the authors were
a common consequence of translocations, even under able to identify the magnitude of the effect of dispers-
the best of circumstances. On the basis of their find- ers, as well as their most likely population of origin.
ings, Mock et al. (2004) recommended particular cau- Despite a few cases in which the apparent presence of
tion in the practice of ‘‘serial translocations’’, where individuals from prior reintroductions significantly im-
translocated populations become the source for further pacted the genetic structure of populations, the results
translocation. of this study indicated an overall paucity of gene flow
among reintroduced populations in Indiana, even
Gene Flow Among Local Populations where the opportunity for dispersal appeared high.
At a regional scale, if populations within a region Social and Behavioral Dynamics
exchange migrants (gene flow), the potential negative
effects associated with genetic drift and low population The underlying social organization of most wild
sizes may be alleviated (Wright 1978, Allendorf 1983). species often can be difficult to resolve (Sugg et al.
Furthermore, the evolution of newly established pop- 1996). The social structure, mating tactics, and move-
ulations is not limited by the genetic contribution of ment behaviors of a species ultimately sculpt the tem-
founders if gene flow among regional populations is poral and spatial patterns of genetic structure that itGenetic Markers for Wild Turkey Management • Latch et al. 39
exhibits (Chesser 1991a, Chesser 1991b, Chesser et al. persal and migration, and detection of hybridization
1993). Therefore, examination of fine-scaled genetic and introgression (Manel et al. 2002, Randi and Luc-
structure in wild species can in turn lead to a clearer chini 2002, Cegelski et al. 2003, Haig et al. 2004, Mc-
understanding of social and behavioral dynamics. In Loughlin et al. 2004). Cases of poaching also could
the wild turkey, interpreting patterns of genetic struc- benefit from individual identification, where individual
ture within localized regions may provide insight into animals may be classified by location of harvest.
the social organization of wintering flocks, interactions Additionally, mark-recapture studies based on in-
among flocks, and the mechanisms involved in the dis- dividual molecular-based identification could be a
sociation of flocks in the spring. valuable non-invasive method for estimating popula-
Leberg (1991) found that within regions, almost tion sizes in managed populations (Mowat et al. 2002,
none of the allozyme variability he found in wild tur- Wilson et al. 2003). At a local scale, individual iden-
keys was accounted for by differences among sam- tification and measures of relatedness among individ-
pling localities. However, the opposite result was uals can be used to characterize family groups in wild-
found in Kansas, where allozymes revealed significant life studies, providing insight into behaviors such as
genetic variability among wintering flocks (Rhodes et paternity and mate choice (Okada and Tamate 2000,
al. 1995). Boone and Rhodes (1996) also found sig- Kerth et al. 2002, Nievergelt et al. 2002).
nificant allozyme differentiation between two winter Microsatellite loci are currently the marker of
flocks in South Carolina. Latch and Rhodes (2005b) choice for identifying individual turkeys. High levels
used microsatellites, control region sequences, and of polymorphism in microsatellites mean that this
previously-collected allozyme data (Boone and marker type is generally associated with lower prob-
Rhodes 1996) to investigate the reason for this di- abilities of identity (the probability that two randomly
chotomy regarding genetic differentiation at a local chosen individuals will have the same multilocus ge-
scale. It appears that timing and method of sample notype) than other marker types. Using 10 of the mi-
collection are responsible for the discrepancy between crosatellite loci most commonly used in turkeys, we
estimates of local genetic structure. Leberg (1991) uti- can achieve an overall probability of identity of 3.5 ⫻
lized samples from male turkeys collected during the 10⫺14, almost ensuring that species-wide, no two tur-
spring, whereas Rhodes et al. (1995) and Boone and keys will share a multilocus genotype (Latch 2004).
Rhodes (1996) used samples from both sexes of tur- This attests to the tremendous power of multilocus mi-
keys collected during winter trapping activities. In crosatellite genotypes in individual identification.
winter, samples are collected from discrete flocks, and Highly variable microsatellites have been used suc-
thus genetic differentiation can be detected among cessfully to assign individual turkeys to a population
them (Rhodes et al. 1995, Boone and Rhodes 1996, or subspecies (Latch and Rhodes 2005, Latch et al.
Latch and Rhodes 2005b). However, flocks dissociate 2006b) and to identify migrant individuals into a re-
in the spring; thus, spring-collected samples from a cently established population (Latch et al. 2006b). As-
given geographic location contain turkeys from mul- signment tests using the available set of microsatellite
tiple flocks and do not exhibit local genetic structure loci proved to be extremely useful for detecting and
(Leberg 1991, Latch and Rhodes 2005b). These results characterizing hybridization between wild turkey sub-
emphasize the need to interpret genetic data in light of species (Latch et al. 2006a, b). Ongoing research will
the social organization of the species at the time of determine the utility of these markers for detecting in-
sample collection. These studies also have demonstrat- trogression of domestic genes into wild stock and for
ed the utility of molecular markers, both protein- and providing evidence in poaching cases.
DNA-based, for investigating small scale genetic
structure.
Very recently, microsatellite loci have been used CONCLUSIONS
to investigate kin selection and cooperative courtship
in the wild turkey (Krakauer 2005). He used genetic A suite of molecular markers has been optimized
data to estimate relatedness among individuals in a for use in the wild turkey, representing an array of
flock, and combined with data on reproductive success marker systems (protein- and DNA-based markers), in-
was able to demonstrate that the indirect fitness ben- heritance patterns (biparental and maternal), and mu-
efits obtained by non-breeding subordinate males off- tation rates. The body of existing research using mo-
set the cost of helping. It is rare that a long-standing lecular markers in the wild turkey illustrates their pow-
controversial theory such as kin selection can be con- er for applications ranging from the subspecies-level
firmed, but this certainly is an example of where in- to the individual-level, and for questions ranging from
credible progress can be made when the appropriate species evolution to forensics.
molecular tool is applied to a species in which the Highly variable markers such as nuclear microsat-
biology is well understood. ellites are particularly useful for elucidating genetic
structure among turkey populations, and even for iden-
Individual-level Applications tifying individual birds. Maternally-inherited mito-
chondrial DNA markers such as cytochrome b and
Identification of individual animals has a multitude control region sequences exhibit less variability among
of potential applications for wildlife forensics: assign- individuals, but may be indispensable in questions re-
ment of population or subspecies origin, studies of dis- garding hybridization, sex-biased dispersal, and female40 Managing Wild Turkey Populations
lineage establishment. Low levels of genetic variability Adams, J. R., B. T. Kelly, L. P. Waits. 2003. Using faecal DNA
in allozymes have not precluded their use in the wild sampling and GIS to monitor hybridization between red
wolves (Canis rufus) and coyotes (Canis latrans). Molec-
turkey; however, high levels of variability in DNA-
ular Ecology 12:2175–2186.
based markers make them ideal candidates for studies Allendorf, F. W. 1983. Isolation, gene flow, and genetic differ-
of genetic variation in wild turkeys. Fortunately, sev- entiation among populations. Pages 51–65 in C. M. Scho-
eral studies, including one in the wild turkey, have newald-Cox, S. M. Chambers, B. MacBryde, and L. Thom-
shown that allozyme data corroborates with data ob- as, editors. Genetics and conservation: a reference for man-
tained from DNA-based markers (Spruell et al. 2003, aging wild animal and plant populations. Benjamin/Cum-
Zhou et al. 2003, King and Eackles 2004, Latch 2004). mings, Menlo Park, California, USA.
, and R. F. Leary. 1986. Heterozygosity and fitness in
It has become apparent that the tools of modern
natural populations of animals. Pages 57–56 in M. E. Soulé,
molecular biology hold great value for wild turkey editor. Conservation biology: the science of scarcity and
management. It also is clear that decisions pertaining diversity. Sinauer, Sunderland, Massachusetts, USA.
to the selection of genetic markers, both in terms of Anderson, J. D., R. L. Honeycutt, R. A. Gonzales, K. L. Gee,
inheritance patterns and rates of evolution, are impor- L. C. Skow, R. L. Gallagher, D. A. Honeycutt, and R. W.
tant if these tools are to be applied successfully at DeYoung. 2002. Development of microsatellite DNA mark-
varying scales of biological organization. In the wild ers for the automated genetic characterization of white-
tailed deer populations. Journal of Wildlife Management 66:
turkey, appropriate utilization of molecular tools has 67–74.
led to a better understanding of the evolutionary his- Avise, J. C. 2004. Molecular Markers, Natural History, and Evo-
tory of turkeys, their behavior, and their population lution, Second edition. Sinauer Associates, Sunderland,
dynamics, which in turn can be used to manage pop- Massachusetts, USA.
ulations to optimize growth and long-term stability. Baker, A. J., and A. Moeed. 1987. Rapid genetic differentiation
Similarly, genetic evaluations of previous transloca- and founder effect in colonizing populations of common
tions have advanced our understanding of founder mynahs (Acridotheres tristis). Evolution 41:525–538.
Beheler, A. A. 2001. Characterization of dispersal and reproduc-
events and post-translocation processes within and tive strategies in the eastern phoebe (Sayornis phoebe). Dis-
among populations. sertation, Purdue University, West Lafayette, Indiana, USA.
The future of wild turkey management looks , and O. E. Rhodes, Jr. 2003. Within-season prevalence
bright. The application of molecular tools will contin- of extra pair young in broods of double-brooded and mate-
ue to advance our understanding of wild turkey biol- faithful eastern phoebes (Sayornis phoebe) in Indiana. Auk
ogy and ecology, thereby improving our ability to ef- 120:1054–1061.
fectively manage this species. Recent advances in our Boone, M. D., and O. E. Rhodes, Jr. 1996. Genetic structure
among subpopulations of the eastern wild turkey (Meleagris
ability to determine the genetic composition (subspe- gallopavo silvestris). American Midland Naturalist 135:
cies status) of individual animals, or even entire re- 168–171.
gions, have profound implications for the future of Boyce, W. M., R. R. Ramey, T. C. Rodwell, E. S. Rubin, and R.
wild turkey management. We are now able to objec- S. Singer. 1999. Population subdivision among desert big-
tively determine what subspecies exist in what areas, dhorn sheep (Ovis canadensis) ewes revealed by mitochon-
and if turkeys in that area show evidence of hybrid- drial DNA analysis. Molecular Ecology 8:99–106.
ization with another subspecies. Another area of wild Boyd, D. K., S. H. Forbes, D. H. Pletscher, and F. W. Allendorf.
2001. Identification of Rocky Mountain gray wolves. Wild-
turkey management likely to show incredible growth life Society Bulletin 29:78–85.
is the prosecution of poaching cases. The ability of Carew, P. J., G. J. Adcock, and R. A. Mulder. 2003. Microsat-
molecular tools to enable identification of individual ellite loci for paternity assessment in the black swan (Cyg-
animals and analysis methodology to assign individu- nus atratus: Aves). Molecular Ecology Notes 3:1–3.
als to a population of origin means that in many in- Cegelski, C. C., L. P. Waits, and N. J. Anderson. 2003. Assessing
stances, poached animals can be objectively identified population structure and gene flow in Montana wolverines
with confidence. Molecular tools may also advance our (Gulo gulo) using assignment-based approaches. Molecular
Ecology 12:2907–2918.
understanding of wild turkey biology, particularly at a Chesser, R. K. 1991a. Gene diversity and female philopatry. Ge-
local scale. We should be able to determine the genetic netics 127:437–447.
relationships among individuals within flocks, and . 1991b. Influence of gene flow and breeding tactics on
such data could be combined with radio-telemetry data gene diversity within populations. Genetics 129:573–583.
to better understand the movements and associations , O. E. Rhodes, D. W. Sugg, and A. Schnabel. 1993.
of turkeys within a flock throughout the year. It is an Effective sizes for subdivided populations. Genetics 135:
exciting time to be involved in wild turkey manage- 1221–1232.
Cornuet, J. M., S. Piry, G. Luikart, A. Estoup, and M. Solignac.
ment, and we feel that molecular tools offer a unique
1999. New methods employing multilocus genotypes to se-
perspective by which we can optimize wild turkey lect or exclude populations as origins of individuals. Ge-
translocation strategies and management programs to netics 153:1989–2000.
ensure the future of this species. Cronin, M. A. 1991. Mitochondrial DNA in wildlife forensic
science: species identification of tissues. Wildlife Society
Bulletin 19:94–105.
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