Volume 134, 2017, pp.

811–820
DOI: 10.1642/AUK-16-162.1

RESEARCH ARTICLE

Extrapair paternity and nest parasitism in two sympatric quail

Craig A. Davis,1* Jeremy P. Orange,1a Ronald A. Van Den Bussche,2 R. Dwayne Elmore,1 Samuel D.
Fuhlendorf,1 J. Matthew Carroll,1 Evan P. Tanner,1 and David M. Leslie, Jr.3
1
Department of Natural Resource Ecology and Management, Oklahoma State University, Stillwater, Oklahoma, USA
2
Department of Integrative Biology, Oklahoma State University, Stillwater, Oklahoma, USA
3
U.S. Geological Survey, Oklahoma Cooperative Fish and Wildlife Research Unit, Department of Natural Resource Ecology and
Management, Oklahoma State University, Stillwater, Oklahoma, USA
a

Downloaded from https://academic.oup.com/auk/article/134/4/811/5149124 by guest on 05 July 2021

Current address: Department of Geography, College of Liberal Arts & Sciences, University of Florida, Gainesville, Florida, USA
* Corresponding author: craig.a.davis@okstate.edu
Submitted August 3, 2016; Accepted May 4, 2017; Published July 12, 2017

ABSTRACT
We conducted a comparative study of 2 closely related and sympatric species, Northern Bobwhite (Colinus virginianus)
and Scaled Quail (Callipepla squamata), to explore the drivers of interspecific variation in alternative reproductive
strategies. Specifically, we used parentage analyses to determine rates of extrapair paternity and intraspecific brood
parasitism for each species, and evaluated possible mechanisms for explaining variation in these rates between the 2
species. During 2013–2014, we genotyped hatched (n ¼ 388 for Northern Bobwhite and n ¼ 214 for Scaled Quail) and
unhatched (n ¼ 32 for Northern Bobwhite and n ¼ 9 for Scaled Quail) eggshells from 34 Northern Bobwhite and 22
Scaled Quail nests in western Oklahoma, USA. Extrapair paternity occurred in 85% of Northern Bobwhite nests and 9%
of Scaled Quail nests. The number of sires for each nest was greater in Northern Bobwhite nests (x̄ ¼ 2.29 6 0.14 SE
sires per nest) than in Scaled Quail nests (x̄ ¼ 1.09 6 0.06 sires per nest). Intraspecific brood parasitism rates varied
considerably between Northern Bobwhite (21%) and Scaled Quail (0%). Northern Bobwhites also parasitized Scaled
Quail nests. Variation in extrapair paternity and intraspecific brood parasitism rates between the Northern Bobwhite
and Scaled Quail appeared to be related to differences in their life history strategies (r-selected vs. K-selected strategy)
as well as differences in breeding population densities.
Keywords: Callipepla squamata, Colinus virginianus, extrapair paternity, intraspecific nest parasitism, Northern
Bobwhite, reproductive strategies, Scaled Quail

Paternidad Extrapareja y Parasitismo de Nidada en dos Especies Simpátricas de Codorniz

RESUMEN
Realizamos un estudio comparativo de dos especies cercanamente emparentadas y simpátricas (Colinus virginianus y
Callipepla squamata) para evaluar los causantes de variación intraespecı́fica en las estrategias alternativas de
reproducción. Especı́ficamente, usamos análisis de parentesco para determinar las tasas de paternidad extrapareja
(PEP) y de parasitismo de nidada intraespecı́fico (PNI) para cada especie y evaluamos los posibles mecanismos para
explicar la variación en las tasas entre especies. Durante 20132014, determinamos el genotipo de las cáscaras de
huevo eclosionadas (n ¼ 388 para C. virginianus y n ¼ 214 para C. squamata) y no eclosionadas (n ¼ 32 para C.
virginianus y n ¼ 9 para C. squamata) provenientes de 34 nidos de C. virginianus y 22 nidos de C. squamata del oeste de
Oklahoma. La PEP se presentó en el 85.3% de los nidos de C. virginianus y en el 9.1% de los nidos de C. squamata. El
número de progenitores para cada nido fue mayor en los nidos de C. virginianus (x̄ ¼ 2.29 6 0.14 [EE] progenitores por
nido) que en los de C. squamata (x̄ ¼ 1.09 6 0.06 progenitores por nido). Las tasas de PNI variaron considerablemente
entre C. virginianus (21%) y C. squamata (0%). C. virginianus también parasitó los nidos de C. squamata. La variación en
las tasas de PEP y PNI entre C. virginianus y C. squamata parecerı́a estar relacionada con las diferencias en sus
estrategias de historia de vida (estrategias r vs. K) tanto como en las diferencias en las densidades poblacionales
reproductivas.
Palabras clave: Callipepla squamata, Colinus virginianus, estrategias reproductivas, parasitismo de nidada
intraespecı́fico, paternidad extrapareja

Q 2017 American Ornithological Society. ISSN 0004-8038, electronic ISSN 1938-4254

Direct all requests to reproduce journal content to the AOS Publications Office at pubs@americanornithology.org
812 Alternative reproductive strategies in two quail species
INTRODUCTION
Molecular parentage studies have revealed that many of
the bird species initially thought to be socially monoga-
mous exhibit a high incidence of extrapair paternity (EPP)
through extrapair copulations (Bennett and Owens 2002).
It is estimated that ,25% of all socially monogamous bird
species practice true genetic monogamy (Griffith et al.
2002). The widespread occurrence of EPP is not surprising
given that it can result in strong sexual selection in socially
monogamous systems (Albrecht et al. 2006, Webster et al.
2007). Although a majority of bird species engage in
extrapair copulations, rates of EPP may range from 0% to
95% of clutches containing extrapair offspring (Arnold and
Owens 2002). Hypotheses proposed to explain variation in
EPP rates among species and populations include
increased breeding density and synchrony, high adult
mortality rates, and reduced parental care (Mulder et al.
1994, Wink and Dyrcz 1999, Arnold and Owens 2002,
Griffith et al. 2002). Griffith et al. (2002) suggested that
these hypotheses contribute to our understanding of
variation in EPP, but that they should be viewed
hierarchically in explaining variation in EPP. For example,
variation in EPP among major lineages may be due to gross
differences in parental care and reproductive life span,
while variation in EPP between closely related species or
populations of the same species may be due to contem-
porary ecological factors and genetic benefits (Arnold and
Owens 2002).
Another less common mechanism resulting in EPP in
birds is intraspecific brood parasitism (IBP), whereby
females lay eggs in the nests of conspecifics. IBP has been
documented in 234 bird species and is particularly
prevalent in precocial species (e.g., Anatidae and Galli-
formes; Geffen and Yom-Tov 2001). Within precocial
species, variation in IBP rates vary greatly from 0% to
50% in clutches (Arnold and Owens 2002). This variation
in IBP is likely related to fundamental differences in life
history and parental care that have occurred over
evolutionary history. Species with limited parental care
and large brood sizes may be predisposed to engage in IBP
(Sorenson 1992, Geffen and Yom-Tov 2001), and the
strongest correlate of high IBP rates is fecundity (Arnold
and Owens 2002). In contrast, variation in IBP rates
among closely related species or within populations may
be a response to contemporary ecological factors such as
nest densities, nest site and resource availabilities, and nest
predation rates (Yom-Tov 1980, Eadie et al. 1988, Petrie
and Møller 1991, Robertson et al. 1992). The hierarchical
distinction between evolutionary and contemporary fac-
tors as drivers of variation in IBP rates and other
alternative reproductive strategies such as extrapair
copulations emphasizes the complexity and limitations of
studying alternative reproductive strategies at single
The Auk: Ornithological Advances 134:811–820, Q 2017 American Ornithological Society
C. A. Davis, J. P. Orange, R. A. Van Den Bussche, et al.
temporal scales. It also highlights the need to conduct
more comparative field-based genetic studies to better
understand mechanisms of interspecific variation in
alternative reproductive strategies.
Comparative studies that use closely related and
sympatric species offer unique opportunities to explore
the drivers of interspecific variation in alternative repro-
ductive strategies. The Northern Bobwhite (Colinus virgin-
ianus) and Scaled Quail (Callipepla squamata) are 2
closely related species (Johnsgard 1973, Gutiérrez 1993,
Hosner et al. 2015) that co-occur at the western (Northern
Bobwhite) and eastern (Scaled Quail) extremes of their
Downloaded from https://academic.oup.com/auk/article/134/4/811/5149124 by guest on 05 July 2021
distributions (Dabbert et al. 2009, Brennan et al. 2014).
Excluding areas where Northern Bobwhites and Scaled
Quail are sympatric, these 2 species generally inhabit quite
different plant communities throughout most of their
distributions. Northern Bobwhites are widely distributed
throughout the eastern United States and tend to inhabit
mesic, early successional shrublands (Brennan et al. 2014),
whereas Scaled Quail are regionally restricted to the
southwestern U.S. and northern Mexico and predomi-
nantly inhabit xeric, mid- to late-successional shrublands
(Dabbert et al. 2009). Giuliano et al. (1998) suggested that
Scaled Quail have adapted to inhabiting arid regions by
allocating more resources to self-maintenance than to
reproduction as a strategy to increase survival and lifetime
reproductive potential (K-selection strategy), especially
during periods of severe water deprivation. In contrast,
Giuliano et al. (1998) suggested that Northern Bobwhites
allocate relatively more resources to reproduction than to
self-maintenance (r-selection strategy), even during peri-
ods of water deprivation, because they have evolved under
more mesic conditions. Finally, the 2 species have evolved
from 2 very different physiographic regions, with Callipe-
pla diverging in the Nearctic and Colinus diverging in
Central America south to Central Panama (Hosner et al.
2015).
Scaled Quail and Northern Bobwhite were originally
considered to be socially monogamous species (Dabbert et
al. 2009, Brennan et al. 2014). However, Northern
Bobwhites appear to be more flexible in their mating
behaviors as they exhibit breeding between single, mated
pairs, breeding between females and multiple males, and
breeding between males and multiple females (Faircloth
2008). The multiple matings exhibited by both sexes
suggest that Northern Bobwhites engage in polygamous
mating, but the facts that Northern Bobwhites frequently
develop pair bonds and that the duration of their pair
bonds may last up to several months (Brennan et al. 2014)
suggest that these multiple matings may be more
associated with opportunities to engage in extrapair
copulations. As such, we consider it appropriate to use
the term extrapair paternity in describing the mating
system of the Northern Bobwhite.
C. A. Davis, J. P. Orange, R. A. Van Den Bussche, et al.
Given that the Northern Bobwhite and Scaled Quail
appear to have evolved different life history strategies (r-
selection strategy vs. K-selection strategy), we would
expect them to exhibit different rates of EPP and IBP.
However, an examination of 2 life history characteristics
(parental care and adult mortality) that have been
hypothesized to influence rates of EPP and IBP may
suggest otherwise. For species that have a high degree of
male participation in parental care, EPP rates are
hypothesized to be lower because males would be less
likely to raise broods that have a high proportion of
offspring that are not their own (Mulder et al. 1994,
Griffith et al. 2002). Male participation in the care of young
(i.e. brooding and protecting young) occurs in both
species, which would suggest a low rate of EPP in both
species. In contrast, species with high adult mortality are
hypothesized to exhibit high rates of EPP (Arnold and
Owens 2002). Scaled Quail and Northern Bobwhites both
experience high annual mortality rates, although Scaled
Quail are thought to have higher survival rates than
Northern Bobwhites (Johnsgard 1973, 1988), indicating
that both species may exhibit high rates of EPP, but that
rates of EPP in Scaled Quail may be lower than those in the
Northern Bobwhite. An important contemporary factor
that may also affect variation in EPP and IBP is breeding
density (Westneat and Sherman 1997). When high
breeding densities occur, opportunities to pursue extrapair
copulations and to engage in IBP increase as encounters
between congeners increase. Because Northern Bobwhites
and Scaled Quail vary greatly in abundance based on
environmental conditions (Bridges et al. 2001, Lusk et al.
2001, Perez et al. 2002), an examination of the relationship
between density and the occurrence of EPP and IBP may
provide insight into the mechanisms of population
regulation in these 2 species.
The overlapping distributions of Northern Bobwhites
and Scaled Quail in western Oklahoma, USA, provided us
with an opportunity to study the mating systems of 2
sympatric species that exhibit different reproductive
strategies and life history characteristics. Specifically, we
used parentage analyses to determine the rates of EPP and
IBP for each species and evaluated possible mechanisms
for explaining the variation in these rates between the 2
species. Our approach was to focus on both evolutionary
(life history strategy, parental care investment, adult
mortality rate) and contemporary factors (breeding
density) to provide explanations for differences between
the 2 species, if differences existed. We recognize the
limitations of a comparative study of only 2 species, but
argue that conducting a comparative study of 2 closely
related, sympatric species under the same environmental
conditions (e.g., weather, food resources, habitat availabil-
ity) can nevertheless provide useful insight into the factors
driving variation in EPP and IBP at the population level.
The Auk: Ornithological Advances 134:811–820, Q 2017 American Ornithological Society
Alternative reproductive strategies in two quail species 813
METHODS
Sample Collection
We collected samples for genetic analyses from Northern
Bobwhites and Scaled Quail in Beaver River Wildlife
Management Area (BRWMA) and Packsaddle Wildlife
Management Area (PSWMA) in western Oklahoma in
2013–2014. BRWMA (11,315 ha) and PSWMA (7,955 ha)
are owned and managed by the Oklahoma Department of
Wildlife Conservation. Populations of Scaled Quail and
Northern Bobwhite occur in BRWMA, but only Northern
Bobwhites occur in PSWMA. Adults of both sexes of
Northern Bobwhite and Scaled Quail were captured using
Downloaded from https://academic.oup.com/auk/article/134/4/811/5149124 by guest on 05 July 2021
Stoddard funnel traps (Stoddard 1931) from August to
April of each year, and a 7-g necklace VHF radio-
transmitter (Advanced Telemetry Systems, Isanti, Minne-
sota, USA) was attached to each captured bird. The sexes
of each species were distinguished by distinct plumage
characteristics. During handling after capture, we collected
5–10 contour feathers from the flank of each bird and
stored feathers at room temperature in individual paper
envelopes. Adults were tracked 5 days per week during the
nesting season, and a bird was determined to be nesting
based on daily signals being detected from the same
location on consecutive days. A nonincubating male was
determined to be the putative sire if he was located in close
proximity to the nest during nest initiation and incubation.
After eggs hatched and precocial young abandoned the
nest (~12 hr after hatching), we collected the eggshells of
all hatched eggs to genetically assess EPP and IBP. Samples
were uniquely labeled and stored in individual coin
envelopes within a larger airtight bag containing 3–4
desiccant packets. We also collected unhatched eggs,
stored them in uniquely labeled sealed plastic bags, and
froze them at 238C prior to analysis. Only successful
clutches (1 hatched egg) were used for genotyping and
analysis.
Laboratory Protocols
DNA was extracted using the Qiagen DNeasy Blood &
Tissue Kit (Qiagen, Valencia, California, USA) with
extraction protocols for adult contour feathers, eggshell
membranes, and embryonic tissue in unhatched eggshells
when available (Bush et al. 2005). An alteration was made
to the final step of extraction protocols for all feather
samples by using 100 lL of Buffer AE instead of 200 lL.
Genotyping was conducted using 11 species-specific
microsatellite loci for the Northern Bobwhite (Quail 3,
Quail 31, Quail 44, Quail 13, Quail 30, Quail 22, Quail 23
[Schable et al. 2004], CV-P1F3, CV-PCF5, CV-P1A7, and
CV-P1E6 [Faircloth et al. 2009]), and 11–12 species-
specific loci for the Scaled Quail (C023, A014, A110, C015,
C009, A114, A104, C022, A001, A022, B105, and A018
[Orange et al. 2014]). Hatched and unhatched Scaled Quail
814 Alternative reproductive strategies in two quail species
egg samples were genotyped at 12 loci, while all adult
Scaled Quail feather samples were genotyped at 11 loci.
Five percent of samples were randomly selected and
blindly regenotyped to estimate the genotyping error rate
with program PEDANT 1.0 (Johnson and Haydon 2007).
One primer for each microsatellite locus was labeled
with 1 of 3 fluorescent tags (HEX, 6-FAM, and NED) and
run either individually or multiplexed in a group of 2 or 3.
The working concentration for all primer stock solutions
was 10 lM. Individual Polymerase Chain Reactions (PCR)
were conducted in 15 lL reactions consisting of 0.5 lL
forward and reverse primers, 9.0 lL True Allele PCR
Premix (TA; Applied Biosystems, Foster City, California,
USA), 1.0 lL bovine serum albumin (BSA; 0.1 mg mL1),
1.0 lL dH2O, and 3.0 lL DNA (5–50 ng lL1). A 20 lL
reaction was used for all multiplexes of 2. These reactions
consisted of 0.5 lL of forward and reverse primer 1, 0.5 lL
forward and reverse primer 2, 14.0 lL TA, 1.0 lL BSA, and
3.0 lL DNA (5–50 ng lL1). The final 3-primer, 30 lL
multiplex reaction consisted of 0.5 lL of forward and
reverse primer 1, 0.5 lL forward and reverse primer 2, 0.5
lL forward and reverse primer 3, 20.0 lL TA, 1.0 lL BSA,
and 6.0 lL DNA (5–50 ng lL1).
The thermal profile for ‘‘Quail’’ primers (Quail 3, Quail
31, Quail 44, Quail 13, Quail 30, Quail 22, and Quail 23)
consisted of 1 cycle at 958C for 12 min and 35 cycles at
948C for 40 s, 578C for 40 s, and 728C for 30 s, followed by
a final incubation at 728C for 4 min. The thermal profile
for all ‘‘CV’’ primers (CV-P1F3, CV-PCF5, CV-P1A7, and
CV-P1E6) consisted of 1 cycle at 958C for 5 min, 35 cycles
at 958C for 40 s, 658C for 30 s, and 728C for 90 s, 35 cycles
of 958C for 20 s, 608C for 30 s, and 728C for 90 s, and a final
incubation at 728C for 10 min. The thermal profile for all
Scaled Quail primers (C023, A014, A110, C015, C009,
A114, A104, C022, A001, A022, B105, and A018) followed
protocols described by Orange et al. (2014).
PCR product (0.5 lL) was added to 9.5 lL Hi-Di
Formamide and 0.5 lL GeneScan 400HD Rox Dye Size
Standard (Applied Biosystems), and fragment analysis was
conducted with an ABI 3130 or ABI 3730 Genetic
Analyzer and scored using Genemapper 4.0 software
(Applied Biosystems). The number of alleles per locus,
deviations from Hardy-Weinberg equilibrium (HWE),
observed (Ho) and expected (He) heterozygosity, polymor-
phic information content (PIC), and frequency of null
alleles were calculated using Cervus 3.0.3 (Kalinowski et al.
2007). Allele frequencies were calculated using 129 adult
samples (89 Northern Bobwhite and 40 Scaled Quail).
Parentage Analysis
Program COLONY 2.0 (Jones and Wang 2009) was used to
estimate the number of sires for eggs within each nest and
the number of offspring that were a direct result of IBP.
Program COLONY uses a maximum-likelihood method to
The Auk: Ornithological Advances 134:811–820, Q 2017 American Ornithological Society
C. A. Davis, J. P. Orange, R. A. Van Den Bussche, et al.
simultaneously assign sibling relationships and parentage
of offspring while accommodating genotyping error (Jones
and Wang 2010). Using program COLONY, individuals
within clutches were assigned to distinct genetic groupings
(full sibling, half-sibling, or unrelated). The ‘‘polygamous’’
option was selected for both males and females. Each
clutch was entered as a distinct group along with the
genotype of the incubating adult. The genotype of the
putative mate was also included when available (n ¼ 3).
The full likelihood option with ‘‘high’’ likelihood precision
was chosen along with a ‘‘long’’ length of run. Allelic
dropout and genotyping error rates were conservatively set
Downloaded from https://academic.oup.com/auk/article/134/4/811/5149124 by guest on 05 July 2021
at 0.03 at all loci based on the maximum single locus
genotyping error rate estimated using PEDANT 1.0
(Johnson and Haydon 2007). We performed 5 replicate
runs with varying seeding numbers to verify result
consistency.
The presence of Northern Bobwhite eggs within Scaled
Quail nests was apparent due to distinct interspecific
differences in eggshell pigmentation, and individuals that
hatched from these eggs were assumed to be a result of
interspecific nest parasitism. An individual was assumed to
have resulted from IBP when it was genetically unrelated
(,0.80 probability) to the incubating adult (when the
incubating adult was a female) or the inferred maternal
genotype of the majority of the offspring within the nest
(when the incubating adult was a male). Program
COLONY was used to estimate the total number of sires
per clutch following the exclusion of young identified as
resulting from interspecific nest parasitism. All family
clusters had a probability .0.80.
Additionally, we used the single-locus minimum method
(Fiumera et al. 2001) to verify rates of multiple paternity in
female-incubated nests, to estimate the number of sires
contributing to clutches, and to identify the proportion of
nests with more than 1 sire, following the exclusion of
young identified as resulting from interspecific nest
parasitism. For the single-locus minimum method, mater-
nal alleles at the most informative locus were subtracted
from the gentoype of the offspring within the clutch and
the remaining paternal alleles were counted, divided by 2,
and rounded up to generate a conservative minimum
estimate of the number of sires contributing to the nest
(Fiumera et al. 2001, Hess et al. 2012). For male-incubated
Northern Bobwhite nests, following the exclusion of young
resulting from IBP, a clutch was assumed to have more
than 1 sire when 1 offspring within the clutch was
genetically unrelated (,0.8 probability) to the incubating
male.
Two-sample t-tests, or Welch’s t-tests when variances
were unequal (Welch 1947), were used to test for
interspecific differences (P  0.05) in the proportion of
young resulting from IBP and the number of sires per
clutch, and to compare the number of sires between male-
C. A. Davis, J. P. Orange, R. A. Van Den Bussche, et al. Alternative reproductive strategies in two quail species 815

TABLE 1. Number of samples, number of alleles, expected TABLE 2. Number of samples, number of alleles, expected
heterozygosity (He), observed heterozygosity (Ho), and polymor- heterozygosity (He), observed heterozygosity (Ho), and polymor-
phic information content (PIC) for 10 microsatellite loci used to phic information content (PIC) for 12 microsatellite loci used to
genotype Northern Bobwhites from western Oklahoma, USA. genotype Scaled Quail from western Oklahoma, USA.
No. of No. of No. of No. of
Locus samples alleles He Ho PIC Locus samples alleles He Ho PIC
Quail 3 87 24 0.929 0.851 0.919 C023 39 12 0.808 0.744 0.781
Quail 44 89 5 0.442 0.449 0.403 A014 35 7 0.774 0.600 0.730
Quail 13 89 20 0.893 0.820 0.878 A110 40 3 0.598 0.700 0.509
Quail 30 87 16 0.892 0.874 0.877 C015 39 7 0.678 0.718 0.645
Quail 22 87 12 0.889 0.908 0.873 C009 40 12 0.884 0.875 0.860
Quail 23 86 15 0.889 0.884 0.873 A114 38 12 0.829 0.895 0.801
CV-P1F3 86 12 0.827 0.837 0.805 A104 39 11 0.816 0.744 0.782
CV-PCF5 86 15 0.898 0.837 0.884 C022 39 8 0.788 0.795 0.747

Downloaded from https://academic.oup.com/auk/article/134/4/811/5149124 by guest on 05 July 2021

CV-P1A7 85 7 0.719 0.635 0.668 A001 39 8 0.873 0.923 0.846
CV-P1E6 82 10 0.770 0.463 0.736 A022 33 8 0.832 0.636 0.795
Mean 13.6 0.815 0.756 0.792 B105 39 5 0.751 0.846 0.699
A018 8 8 0.883 1.000 0.807
Mean 8.4 0.793 0.860 0.750

and female-incubated Northern Bobwhite nests. Only

females incubated Scaled Quail nests. Mean values are
reported 6 standard errors (SE).
RESULTS
During 2013–2014, we collected and genotyped 223 Scaled
Quail eggshells (214 hatched, 9 unhatched) from 22 nests,
420 Northern Bobwhite eggshells (388 hatched, 32
unhatched) from 34 Northern Bobwhite nests (BRWMA:
n ¼ 17; PSWMA: n ¼ 17), and 12 eggs from 2 parasitized
Scaled Quail nests. The number of genotyped samples
within clutches ranged from 3 to 17 for Northern
Bobwhites and from 3 to 21 for Scaled Quail. All
genotyped Scaled Quail nests were incubated by females,
whereas 25 (~74%) of the Northern Bobwhite nests were
female-incubated. A total of 89 adult Northern Bobwhite
and 40 adult Scaled Quail feathers were genotyped.
Parental genotypes were available for the incubating adult
of 53 (~95%) clutches as well as for the putative mate for 3
(~5%) clutches.
Microsatellites
Allelic diversity was 5–24 alleles per locus for Northern
Bobwhites and 3–12 alleles per locus for Scaled Quail
(Tables 1 and 2). Microsatellite markers for both species
had high levels of heterozygosity, with Ho ¼ 0.449–0.908
for Northern Bobwhites and Ho ¼ 0.600–0.923 for Scaled
Quail. The PIC was 0.403–0.919 for Northern Bobwhites
and 0.509–0.860 for Scaled Quail. One locus (Quail 31)
had a high rate of allelic drop out and was thus excluded
from further analysis. One locus (CV-P1E6) showed signs
of deviations from HWE. A high frequency of null alleles
was observed in 2 Northern Bobwhite loci (CV-P1A7 and
CV-P1E6) and 2 Scaled Quail loci (A014 and A022).
Nevertheless, these loci were used for subsequent analyses
because deviations from HWE and a high frequency of null
alleles in the Northern Bobwhite were likely a direct result
of the Wahlund effect (Wahlund 1928), due to the 2
geographically disjunct Northern Bobwhite populations
(BRWMA and PSWMA) being analyzed as 1 population.
Deviations from HWE were not observed when the 2
Northern Bobwhite populations were analyzed indepen-
dently. High null allelic frequencies, especially in Scaled
Quail, were also likely a result of sampling and capture
methodology because gregarious adults were captured in
potentially related social groups (coveys) in autumn and
winter.
Extrapair Paternity
The estimated number of sires per nest and number of
nests with .1 sire were identical using both the single-
locus minimum (MIN) method and the COLONY method
of analysis for Scaled Quail. Additionally, the MIN and
COLONY methods estimated that a similar proportion of
female-incubated Northern Bobwhite nests had 1 sire
(MIN: 22/25 [88%]; COLONY: 24/25 [96%]; Z ¼1.04, P ¼
0.30). For the 2 clutches for which results differed between
analysis method, COLONY estimated that there were 2
sires and not 1. A significant difference was observed in
the mean number of estimated sires per clutch between
the COLONY and MIN methods for female-incubated
Northern Bobwhite nests (MIN: x̄ ¼ 2.08 6 0.15 SE sires;
COLONY: x̄ ¼ 2.52 6 0.11 sires; t24 ¼ 3.38, P ¼ 0.002);
however, this was not unexpected as methods relying on
counts of paternal alleles can conservatively underesti-
mate the number of sires contributing to a clutch (Sefc
and Koblmüller 2009). Therefore, further statistical
comparisons were made using the estimates from
COLONY.

The Auk: Ornithological Advances 134:811–820, Q 2017 American Ornithological Society

816 Alternative reproductive strategies in two quail species
TABLE 3. Extrapair paternity in Northern Bobwhite and Scaled Quail clutches in western Oklahoma, USA.
No. of No. of offspring
Species clutches genotyped
Northern Bobwhite 34 420
Scaled Quail 22 223
No differences were observed between Northern Bob-
white populations at BRWMA and PSWMA in the
number of sires per clutch (BRWMA: 2.06 6 0.16 sires;
PSWMA: 2.53 6 0.23 sires; t32 ¼ 1.69, P ¼ 0.10), the
proportion of young per nest resulting from IBP
(BRWMA: ~2%; PSWMA: ~3%; Welch’s t21 ¼ 0.66, P ¼
0.52), or the proportion of nests with .1 sire (BRWMA:
82%; PSWMA: 88%; Z ¼ 0.48, P ¼ 0.63); therefore, these
samples were combined in all subsequent analyses. During
the study, Northern Bobwhites had considerably higher
rates (.9 times) of multiple paternity (.1 sire per nest) of
clutches than Scaled Quail (Z ¼ 5.60, P , 0.001; Table 3).
The mean number of sires per clutch (excluding young
resulting from interspecific nest parasitism) was greater for
Northern Bobwhites than for Scaled Quail (Welch’s t44 ¼
7.69, P , 0.001; Table 3); the number of sires per clutch
ranged from 1 to 4 for Northern Bobwhites, while the
number of sires per clutch for Scaled Quail ranged from 1
to 2. Fifteen percent of the 34 Northern Bobwhite nests
were sired by 1 male, 50% were sired by 2 males, 26% were
sired by 3 males, and 9% were sired by 4 males. In contrast,
most (91%) of the 22 Scaled Quail nests were sired by 1
male, with only 9% sired by 2 males. For Northern
Bobwhites, the number of sires per clutch was greater for
female-incubated nests (x̄ ¼ 2.52 6 0.15 sires) than for
male-incubated nests (x̄ ¼ 1.67 6 0.16 sires; t32 ¼ 2.91, P ¼
0.01). None of the genotyped Scaled Quail nests were
incubated by males.
Nest Parasitism
IBP was only recorded in Northern Bobwhite nests (21%;
Table 4). Northern Bobwhites also parasitized 2 Scaled
Quail nests (9% of total Scaled Quail nests). Overall, the
mean number of offspring resulting from IBP and
interspecific nest parasitism (Scaled Quail nests parasitized
by Northern Bobwhites) was 0.35 6 0.15 offspring per
clutch and 0.54 6 0.38 offspring per clutch, respectively.
However, the mean number of offspring produced from
parasitized nests was 1.71 6 0.47 from IBP and 6.00 6
1.27 from interspecific nest parasitism. Additionally, in
relation to the outcome of Northern Bobwhite parasitism,
proportionally more offspring were produced from the
parasitized Scaled Quail nests (interspecific nest parasit-
ism) than from the parasitized Northern Bobwhite nests
(IBP; Table 4).
The Auk: Ornithological Advances 134:811–820, Q 2017 American Ornithological Society
C. A. Davis, J. P. Orange, R. A. Van Den Bussche, et al.
Mean no. of
genotyped samples Mean no. of Clutches with
per clutch sires per clutch .1 sire
12.0 6 0.6 2.29 6 0.14 29 (85%)
10.7 6 2.3 1.09 6 0.23 2 (9%)
DISCUSSION
Extrapair Paternity
Our result that the Northern Bobwhite population
exhibited a different rate of EPP from the Scaled Quail
Downloaded from https://academic.oup.com/auk/article/134/4/811/5149124 by guest on 05 July 2021
population is consistent with our hypothesis that EPP rates
for the populations would differ. Interestingly, the EPP rate
for the Northern Bobwhite was considerably higher than
that for the Scaled Quail (85% vs. 9%). The disparity in EPP
rate between the Northern Bobwhite and Scaled Quail
suggests that differences in their evolutionary history or
differences in their responses to more contemporary
factors may be driving the variation in EPP rate between
them. In terms of evolutionary history, adult mortality and
male contribution to care of the young have received
considerable attention toward explaining interspecific
variation in rates of EPP (Arnold and Owens 2002, Griffith
et al. 2002). We hypothesized that EPP rates for both
species could be high, given that Northern Bobwhites and
Scaled Quail both typically experience high annual
mortality (Johnsgard 1973, 1988). During both years of
our study, adult mortality rates for Northern Bobwhites
and Scaled Quail exceeded 50%. Moreover, socially
monogamous bird species with annual mortality rates
50% frequently exhibit rates of EPP that exceed 40%,
with some rates as high as 95% (Wink and Drycz 1999,
Griffith et al. 2002). However, it appears that adult
mortality provides a potential explanation for EPP rate
only in the Northern Bobwhite. Although several studies
have shown a strong relationship between adult survival
and EPP, there is also considerable variation in EPP rates
(i.e. 0% to 95%) for species with high mortality, suggesting
that the pattern is inconsistent (Wink and Drycz 1999,
Arnold and Owens 2002, Griffith et al. 2002). This was
certainly the case for Scaled Quail, for which we observed a
low EPP rate although the species experienced high
mortality. This pattern in Scaled Quail may be explained
by male Scaled Quail actively guarding their mates from
other males. Scaled Quail and other species in the genus
Callipepla have been reported to frequently defend their
mates from males encountered during the breeding season
(Dabbert et al. 2009, Calkins et al. 2014). Additionally, the
fact that Scaled Quail in western Oklahoma occur at some
of the lowest densities throughout their distribution (Sauer
et al. 2014) may also allow mate guarding to be more
C. A. Davis, J. P. Orange, R. A. Van Den Bussche, et al.
TABLE 4. Occurrence of intraspecific and interspecific nest parasitism (NP) in Northern Bobwhite and Scaled Quail nests in western
Oklahoma, USA.
No. of nests parasitized
Species No. of nests Intraspecific Interspecific
Northern Bobwhite 34 7 (21%) 0 408
a
Scaled Quail 22 0 2 (9%)
a
Interspecific nest parasitism was from Northern Bobwhites parasitizing Scaled Quail nests.
effective against cuckoldry because putative mates will
likely encounter fewer other males.
Given that both Northern Bobwhite and Scaled Quail
males have been documented assisting with the care of
broods (Dabbert et al. 2009, Brennan et al. 2014), we
hypothesized that EPP rates could be low for both species.
Male participation in brood care is highly variable and
inconsistent among individuals and between the 2 species.
For example, the duration of the pair bond in Northern
Bobwhites can range from 2–3 weeks to several months,
and male participation in brood care can range from
limited involvement due to the male abandoning the
female for other breeding opportunities to the male
assuming sole responsibility for care (i.e. incubating the
eggs and brooding and protecting the young; Burger et al.
1995, DeMaso et al. 1997, Brennan et al. 2014). Male
Scaled Quail exhibit similar variation in participation in
care to male Northern Bobwhites, but they rarely incubate
eggs and are the sole parent less frequently (Dabbert et al.
2009). The fact that male contribution to care in both
species is similarly variable, yet EPP rates were quite
different between the 2 species during our study, is
somewhat perplexing. However, our results seem to
suggest that this relationship is complex and not easily
disentangled for Northern Bobwhites and Scaled Quail.
First, the variable levels of participation in care by male
Northern Bobwhites may have contributed to the high
levels of EPP. We found that the number of sires for male-
incubated Northern Bobwhite nests was significantly lower
than for female-incubated nests, which suggests that the
level of male participation (i.e. incubation vs. participation
in brood rearing) and investment influences EPP (Orange
2015). Second, other evolutionary mechanisms or con-
temporary factors may be more important contributors to
the variation in EPP than male contribution to care.
Within our study area, the breeding densities of
Northern Bobwhites and Scaled Quail differed consider-
ably. Scaled Quail densities in western Oklahoma are at
their lowest within their distribution, while Northern
Bobwhites occur at densities near their peak within their
distribution (Sauer et al. 2014). In fact, Northern Bobwhite
densities are as much as 5 to 10 times greater than Scaled
Quail densities in the region (Sauer et al. 2014).
Furthermore, based on whistle count data collected from
The Auk: Ornithological Advances 134:811–820, Q 2017 American Ornithological Society
Alternative reproductive strategies in two quail species 817
No. of offspring resulting from NP
No. of offspring
genotyped Intraspecific Interspecific
12 (3%) 0
235 0 12 (9%)
our study site, Northern Bobwhites are considerably more
abundant than Scaled Quail; 2.19 6 0.13 males per point
and 3.17 6 0.23 males per point were recorded for
Downloaded from https://academic.oup.com/auk/article/134/4/811/5149124 by guest on 05 July 2021
Northern Bobwhite in 2013 and 2014, respectively,
compared with 0.07 6 0.02 males per point and 0.10 6
0.02 males per point for Scaled Quail in 2013 and 2014,
respectively (K. Andersson personal communication).
Given the large disparity in breeding densities between
Northern Bobwhites and Scaled Quail, we would expect
breeding densities to potentially be an important contem-
porary factor explaining differences in EPP rates between
the species. During our study, the higher breeding densities
of Northern Bobwhites likely facilitated higher rates of EPP
in this species in our study area compared with Scaled
Quail, who likely had low encounter rates with other
congeners at their lower breeding densities, which likely
contributed to their lower EPP rates.
Intraspecific Brood Parasitism
IBP is not a common reproductive strategy in galliform
species; among all Galliformes, IBP has been documented
in just 11% of species (Geffen and Yom-Tov 2001). The
incidence of IBP has not been well documented for
Northern Bobwhites and Scaled Quail. In one of the few
studies to have examined IBP in the Northern Bobwhite,
Faircloth (2008) reported an overall IBP rate of 28%, and
noted that IBP rates varied from 5% to 35% over a 3-yr
period. Our results, which were similar to those of
Faircloth (2008), further confirm that Northern Bobwhite
engage in IBP. Additionally, we found that Northern
Bobwhites engage in interspecific brood parasitism as 2
Scaled Quail nests contained Northern Bobwhite eggs. No
observations of Scaled Quail engaging in IBP have been
documented (Dabbert et al. 2009), and our results also
suggest that Scaled Quail may not engage in this behavior.
Overall, IBP is more common in birds that have
precocial young (Rohwer and Freeman 1989, Geffen and
Tom-Tov 2001). Two factors that contribute to the high
incidence of IBP in precocial species are large clutch sizes,
which increase the period during which clutches are more
susceptible to parasitism, and high nest densities, which
increase the opportunity for nests to be discovered and
parasitized (Geffen and Tom-Tov 2001). For the Northern
Bobwhite, large clutch sizes and high nest densities likely
818 Alternative reproductive strategies in two quail species
facilitated the occurrence of IBP. The mean clutch size for
Northern Bobwhites during our study was 12 eggs, and
clutch size ranged from 6 to 18 eggs, which is typical for
Northern Bobwhites. A closer examination of clutch sizes
showed that 71% of IBP occurred in clutches that
contained .12 eggs and no IBP occurred in clutches that
contained ,11 eggs. Moreover, the 2 Scaled Quail nests
that were parasitized by Northern Bobwhites contained 18
and 21 eggs. Although we did not determine nest densities
or the spatial distribution of nests, the high breeding
population density of Northern Bobwhites also suggests
that nest densities were high.
The large difference in IBP rate (21% vs. 0%) between
the Northern Bobwhite and Scaled Quail can be explained
by differences in nest densities between the 2 species.
Specifically, female Northern Bobwhites likely had greater
opportunities to encounter nests to parasitize compared
with Scaled Quail. However, the fact that we did not
document IBP in Scaled Quail or Scaled Quail parasitizing
Northern Bobwhite nests suggests another explanation. It
is possible that, for a species that evolved in an arid
environment, the time and energetic costs and risks of
searching for host nests may be too high. The fact that
Scaled Quail have adopted a strategy of allocating more
resources to self-maintenance than to reproduction
(Giuliano et al. 1998) suggests that the costs of engaging
in IBP in an arid environment may be too high. Further
research needs to explore the relationship between Scaled
Quail reproductive strategies and life history strategies,
especially at the core of their distribution.
Conclusions
Despite being closely related, the Northern Bobwhite and
Scaled Quail rely upon completely different reproductive
strategies. EPP and IBP rates were 85% and 21% for the
Northern Bobwhite, respectively, and 9% and 0% for the
Scaled Quail, respectively. Based on our understanding of
each species’ life history attributes, it appears that
differences in EPP and IBP rates between the Northern
Bobwhite and Scaled Quail are a function of each species’
life history strategy (r-selection strategy for Northern
Bobwhite vs. K-selection strategy for Scaled Quail) to adapt
to mesic (Northern Bobwhite) and xeric (Scaled Quail)
shrublands. Because we were able to study sympatric
populations of Northern Bobwhite and Scaled Quail under
the same environmental conditions, we were also able to
explore the potential role of a contemporary factor
(breeding density) in driving interspecific variation in
EPP and IBP. Our results suggest that breeding population
density facilitated differences in EPP and IBP rates
between Northern Bobwhites and Scaled Quail. This
seems plausible, considering that variation in EPP and
IBP rates between closely related species is thought to be
more likely determined by contemporary than evolution-
The Auk: Ornithological Advances 134:811–820, Q 2017 American Ornithological Society
C. A. Davis, J. P. Orange, R. A. Van Den Bussche, et al.
ary factors (Arnold and Owens 2002). However, we also
recognize the difficulty of disentangling the role of a
species’ evolutionary history from the role of contemporary
factors in explaining differences in EPP and IBP, and
therefore have not made inferences beyond the scope of
our study.
ACKNOWLEDGMENTS
We thank J. Groendyke for providing the Groendyke graduate
fellowship. We also thank M. Judkins, E. Thacker, W. Storer, C.
Crisswell, S. Wayment, M. Richins, K. Schultz, and all of our
great technicians for their assistance with this project. Any use
Downloaded from https://academic.oup.com/auk/article/134/4/811/5149124 by guest on 05 July 2021
of trade, firm, or product names is for descriptive purposes
only and does not imply endorsement by the U.S. Govern-
ment.
Funding statement: Funding was provided by the Pittman-
Robertson Federal Aid to Wildlife Restoration Act under
project W-161-R (F11AF00069) of the Oklahoma Department
of Wildlife Conservation and Oklahoma State University,
administered through the Oklahoma Cooperative Fish and
Wildlife Research Unit (Oklahoma Department of Wildlife
Conservation, Oklahoma State University, U.S. Geological
Survey, U.S. Fish and Wildlife Service, and the Wildlife
Management Institute cooperating). Additional funding was
provided by the Bollenbach Endowed Chair in Wildlife
Management and Groendyke Chair in Wildlife Conservation.
None of the funders had any input into the content of this
manuscript nor required their approval of the manuscript
before submission or publication.
Ethics statement: Capture and sample collection protocols
were reviewed and approved by Oklahoma State University’s
Institutional Animal Care and Use Committee (ACUP #AG-
13-2 and ACUP #AG-11-22). The Oklahoma Department of
Wildlife Conservation provided permission to conduct
research in both study sites.
Author contributions: J.P.O., C.A.D., and R.A.V.D.B. con-
ceived, designed, and performed the experiments; J.P.O.
analyzed the data; J.M.C. and E.P.T. contributed materials;
and C.A.D., J.P.O., D.M.L., R.D.E., and S.D.F. wrote the paper.
LITERATURE CITED
Albrecht, T., J. Kreisinger, and J. Piálek (2006). The strength of
direct selection against female promiscuity is associated with
rates of extrapair fertilizations in socially monogamous
songbirds. The American Naturalist 167:739–744.
Arnold, K. E., and I. P. F. Owens (2002). Extra-pair paternity and
egg dumping in birds: Life history, parental care and the risk
of retaliation. Proceedings of the Royal Society of London,
Series B 269:1263–1269.
Bennett, P. M., and I. P. F. Owens (2002). Evolutionary Ecology of
Birds: Life Histories, Mating Systems and Extinction. Oxford
University Press, Oxford, UK.
Brennan, L. A., F. Hernandez, and D. Williford (2014). Northern
Bobwhite (Colinus virginianus). In The Birds of North America
(P. G. Rodewald, Editor). Cornell Lab of Ornithology, Ithaca,
C. A. Davis, J. P. Orange, R. A. Van Den Bussche, et al.
NY, USA. https://birdsna.org/Species-Account/bna/species/
norbob
Bridges, A. S., M. J. Peterson, N. J. Silvy, F. E. Smeins, and X. B. Wu
(2001). Differential influence of weather on regional quail
abundance in Texas. The Journal of Wildlife Management 65:
10–18.
Burger, L. W., M. R. Ryan, T. V. Dailey, and E. W. Kurzejeski (1995).
Reproductive strategies, success, and mating systems of
Northern Bobwhite in Missouri. The Journal of Wildlife
Management 59:417–426.
Bush, K. L., M. D. Vinsky, C. L. Aldridge, and C. A. Paszkowski
(2005). A comparison of sample types varying in invasiveness
for use in DNA sex determination in an endangered
population of Greater Sage-Grouse (Centrocercus urophasia-
nus). Conservation Genetics 6:867–870.
Calkins, J. D., J. Gee, J. C. Hagelin, and D. F. Lott (2014). California
Quail (Callipepla californica). In The Birds of North America (P.
G. Rodewald, Editor). Cornell Lab of Ornithology, Ithaca, NY,
USA. https://birdsna.org/Species-Account/bna/species/
calqua
Dabbert, C. B., G. Pleasant, and S. D. Schemnitz (2009). Scaled
Quail (Callipepla squamata). In The Birds of North America (P.
G. Rodewald, Editor). Cornell Lab of Ornithology, Ithaca, NY,
USA. https://birdsna.org/Species-Account/bna/species/scaqua
DeMaso, S. J., A. D. Peoples, S. A. Cox, and E. S. Parry (1997).
Survival of Northern Bobwhite chicks in western Oklahoma.
The Journal of Wildlife Management 61:846–853.
Eadie, J. M., F. P. Kehoe, and T. D. Nudds (1988). Pre-hatch and
post-hatch brood amalgamation in North American Anatidae:
A review of hypotheses. Canadian Journal of Zoology 66:
1709–1721.
Faircloth, B. C. (2008). An integrative study of social and
reproductive systems in Northern Bobwhite (Colinus virgin-
ianus): A non-migratory, avian species bearing precocial
young. Ph.D. dissertation, University of Georgia, Athens, GA,
USA.
Faircloth, B. C., T. M. Terhune, N. A. Schable, T. C. Glenn, W. E.
Palmer, and J. P. Carroll (2009). Ten microsatellite loci from
Northern Bobwhite (Colinus virginianus). Conservation Ge-
netics 10:535–538.
Fiumera, A. C., Y. D. DeWoody, M. A. Asmusen, and J. C. Avise
(2001). Accuracy and precision of methods to estimate the
number of parents contributing to a half-sib progeny array.
The Journal of Heredity 92:120–126.
Geffen, E., and Y. Yom-Tov (2001). Factors affecting the rates of
intraspecific nest parasitism among Anseriformes and Galli-
formes. Animal Behaviour 62:1027–1038.
Giuliano, W. M., R. Patiño, and R. S. Lutz (1998). Comparative
reproductive and physiological responses of Northern
Bobwhite and Scaled Quail to water deprivation. Compara-
tive Biochemistry and Physiology Part A 119:781–786.
Griffith, S. C., I. P. F. Owens, and K. A. Thuman (2002). Extra pair
paternity in birds: A review of interspecific variation and
adaptive function. Molecular Ecology 11:2195–2212.
Gutiérrez, R. J. (1993). Taxonomy and biogeography of new
world quail. In Quail III: National Quail Symposium (K. E.
Church and T. V. Daley, Editors). Kansas Department of
Wildlife and Parks, Pratt, KS, USA. pp. 8–15.
Hess, B. D., P. O. Dunn, and L. A. Whittingham (2012). Females
choose multiple mates in the lekking Greater Prairie-Chicken
(Tympanuchus cupido). The Auk 129:133–139.
The Auk: Ornithological Advances 134:811–820, Q 2017 American Ornithological Society
Alternative reproductive strategies in two quail species 819
Hosner, P. A., E. L. Braun, and R. T. Kimball (2015). Land
connectivity changes and global cooling shaped the
colonization history and diversification of New World quail
(Aves: Galliformes: Odontophoridae). Journal of Biogeogra-
phy 42:1883–1895.
Johnsgard, P. A. (1973). Grouse and Quails of North America.
University of Nebraska Press, Lincoln, NE, USA.
Johnsgard, P. A. (1988). The Quails, Partridges, and Francolins of
the World. Oxford University Press, New York, NY, USA.
Johnson, P. C. D., and D. T. Haydon (2007). Maximum likelihood
estimation of allelic dropout and false allele error rates from
microsatellite genotypes in the absence of reference data.
Genetics 175:827–842.
Jones, O. R., and J. Wang (2010). COLONY: A program for
Downloaded from https://academic.oup.com/auk/article/134/4/811/5149124 by guest on 05 July 2021
parentage and sibship inference for multilocus genotype
data. Molecular Ecology Resources 10:551–555.
Kalinowski, S. T., M. L. Taper, and T. C. Marshall (2007). Revising
how the computer program CERVUS accommodates geno-
typing error increases success in paternity assignment.
Molecular Ecology 16:1099–1106.
Lusk, J. J., F. S. Guthery, and S. J. DeMaso (2001). Northern
Bobwhite (Colinus virginianus) abundance in relation to yearly
weather and long-term climate patterns. Ecological Modeling
146:3–15.
Mulder, R. A., P. O. Dunn, A. Cockburn, K. A. Lazenby-Cohen, and
M. J. Howell (1994). Helpers liberate female fairy-wrens from
constraints on extra-pair mate choice. Proceedings of the
Royal Society of London, Series B 255:223–229.
Orange, J. P. (2015). Breeding behavior, brood habitat use, and
chick survival of two quail species at the periphery of their
distributions. M.S. thesis, Oklahoma State University, Still-
water, OK, USA.
Orange, J. P., C. A. Davis, R. A. Van Den Bussche, S. D. Fuhlendorf,
R. D. Elmore, E. T. Thacker, and M. E. Judkins (2014).
Development and characterization of 23 microsatellite loci
for Scaled Quail (Callipepla squamata). Conservation Genetics
Resources 6:929–931.
Perez, R. M., J. F. Gallagher, and M. C. Frisbie (2002). Fine scale
influence of weather on Northern Bobwhite abundance,
breeding success, and harvest. In Quail V: Proceedings of the
Fifth National Quail Symposium (S. J. DeMaso, W. P. Kuvleksy,
Jr., F. Hernández, and M. E. Berger, Editors). Texas Parks and
Wildlife Department, Austin, TX, USA. pp. 106–110.
Petrie, M., and A. P. Møller (1991). Laying eggs in others’ nests:
Intraspecific brood parasitism in birds. Trends in Ecology &
Evolution 6:315–320.
Robertson, G. J., M. D. Watson, and F. Cooke (1992). Frequency,
timing and costs of intraspecific nest parasitism in the
Common Eider. The Condor 94:871–879.
Rohwer, F. C., and S. Freeman (1989). The distribution of
conspecific nest parasitism in birds. Canadian Journal of
Zoology 67:239–253.
Sauer, J. R., J. E. Hines, J. E. Fallon, K. L. Pardieck, D. J. Ziolkowski,
Jr., and W. A. Link (2014). The North American Breeding Bird
Survey, Results and Analysis 1966–2012, Version 02.19.2014.
USGS Patuxent Wildlife Research Center, Laurel, MD, USA.
Schable, N. A., B. C. Faircloth, W. E. Palmer, J. P. Carroll, L. W.
Burger, L. A. Brennan, C. Hagen, and T. C. Glenn (2004).
Tetranucleotide and dinucleotide microsatellite loci from the
Northern Bobwhite (Colinus virginianus). Molecular Ecology
Notes 4:415–419.
820 Alternative reproductive strategies in two quail species
Sefc, K. M., and S. Koblmüller (2009). Assessing parent numbers
from offspring genotypes: The importance of marker
polymorphism. Journal of Heredity 100:197–205.
Sorenson, M. D. (1992). Why is conspecific nest parasitism more
frequent in waterfowl than in other birds? Canadian Journal
of Zoology 70:1856–1858.
Stoddard, H. L. (1931). The Bobwhite Quail: Its Habits,
Preservation, and Increase. Charles Scribner’s Sons, New
York, NY, USA.
Wahlund, S. (1928). Zusammensetzung von Populationen und
Korrelationserscheinungen vom Standpunkt der Vererbung-
slehre aus betrachtet. Hereditas 11:65–106.
The Auk: Ornithological Advances 134:811–820, Q 2017 American Ornithological Society
C. A. Davis, J. P. Orange, R. A. Van Den Bussche, et al.
Webster, M. S., K. A. Tarvin, E. M. Tuttle, and S. Pruett-Jones
(2007). Promiscuity drives sexual selection in a socially
monogamous bird. Evolution 61:2205–2211.
Welch, B. L. (1947). The generalization of ‘Student’s’ problem
when several different population variances are involved.
Biometrika 34:28–35.
Westneat, D. F., and P. W. Sherman (1997). Density and extra-pair
fertilizations in birds: A comparative analysis. Behavioral
Ecology and Sociobiology 41:205–215.
Wink, M., and A. Dyrcz (1999). Mating systems in birds: A review
of molecular studies. Acta Ornithologica 34:91–109.
Yom-Tov, Y. (1980). Intraspecific nest parasitism in birds.
Biological Reviews 55:93–108.
Downloaded from https://academic.oup.com/auk/article/134/4/811/5149124 by guest on 05 July 2021