Table
1. Nei’s (1978) unbiased genetic
distances (GST) among seven Flagstaff pinyon jay flocks. The East Flagstaff and
Southeast Doney Park flocks are least similar; the Herold Ranch and Country
Club flocks are most similar.
Population
Structure of a Metapopulation
of Pinyon Jays (Gymnorhinus cyanocephalus)
Nunes,
C., Benford, R., Shuster, S.M., Keim, P., and Balda, R.P.
Avian Cognition Laboratory · Department of Biological Sciences
Northern Arizona University · Flagstaff, AZ
Pinyon jays are non-migratory, yet eruptive, and the local among-flock dispersal rate for juveniles and adults is reported to be low. A low dispersal rate implies a low level of gene flow and high levels of inbreeding and population structure. However, the rate of gene flow and the levels of inbreeding and population structure for this species have not yet been determined. To measure gene flow, inbreeding, and population structure, DNA was collected for four consecutive years from 652 wild pinyon jays in seven flocks in and around Flagstaff, AZ. Genetic fingerprints were derived by measuring allele frequencies at six variable number tandem repeat (VNTR) loci. Population structure was calculated using three methods: RST, FST and θP. R, an unbiased estimator of RST, was used to standardize variance among multiple markers. The genetic distance (GST) and number of migrants per generation (NM) were estimated. GST was diagrammed in an unweighted pair-group method with arithmetic mean (UPGMA) dendrogram. Results suggest that RST= -.5302, FST = 0.0070 and θP = 0.006460. NM is estimated at 35.57, or 1.42 individuals per flock per year. As expected, some inbreeding and a low level of population structure exists, but population structure is less than predicted. Alternative hypotheses that would explain this phenomenon are proposed.
Introduction
The pinyon jay is a social bird that lives in flocks of 200-500. Observations suggest that dispersal from natal flocks is low. This implies that gene flow among flocks is restricted, and would predict that inbreeding within flocks is high. High levels of inbreeding would result in genotypic and phenotypic differentiation among flocks. However, phenotypic differentiation among flocks is not obvious, and the level of genotypic differentiation is unknown. The goal of this study was to determine the level of genotypic differentiation within a metapopulation of seven pinyon jay flocks in and around Flagstaff, AZ.
Methods
In the winters of 2000-04, 652 wild pinyon jays from seven flocks in or around Flagstaff, AZ, USA, were live-trapped. Blood was extracted from each individual. Blood samples were suspended in TE buffer and stored at -80ºC. Blood samples were digested, and DNA was extracted using a Puregene™ kit. Samples were fluorescently labeled and amplified with PCR. Birds were genotyped at six VNTR loci using an ABI 3100 sequencer. Electrophoresis data were used to create individual fingerprints. Data were scored by multiple observers using Genescan® and Genotyper®. Inter-rater discrepancies were resolved; un-resolvable discrepancies were discarded. The inbreeding coefficient and population structure of flocks were determined by calculating RST (Slatkin 1995), FST (Wright 1951, Nei 1972, Nei 1978) and θP (Wier and Cockerham 1984). The among-flock dispersal rate was determined by calculating NM (Nei 1987). The genetic differentiation of flocks was determined by calculating GST (Nei 1978). RSTCalc Version 2.2 was used to calculate RST, and R. PopGene Version 1.31 (Yeh et al. 1997) was used to calculate FST, FIS, NM, and GST. Genetic Data Analysis (GDA) Version 1.1 (Lewis and Zaykin 2001) was used to calculate θP and f. PopGene was used to construct a UPGMA dendrogram.
Results
Slatkin’s R-statistics suggest that population structure is low (RST= -0.5302, R= 0.3952). Nei’s F-statistics suggest that inbreeding in the population is moderate (FIS = 0.0614) and population structure is low (FST = 0.0070). Weir and Cockerham’s θ-statistics suggest that inbreeding in the population is moderate (f = 0.084191) and population structure is low (θP = 0.006460). The average number of migrants for all four years and all seven flocks in the study is NM = 35.57. Not all flocks were sampled all years; data for only 25 of the possible 28 flock-years were available. Data for the 25 flock-years suggest that NM = 1.42 per flock per year. Nei’s genetic distances (GST) are reported in Table 1. These distances suggest that the Country Club and Herold Ranch flocks are the most closely related (GST = 0.0038), and the Southeast Doney Park and East Flagstaff flocks are the least closely related (GST = 0.0255).
Table
1. Nei’s (1978) unbiased genetic
distances (GST) among seven Flagstaff pinyon jay flocks. The East Flagstaff and
Southeast Doney Park flocks are least similar; the Herold Ranch and Country
Club flocks are most similar.
Figure
1. Illustration of genetic
relationships among flocks. Flock locations and band colors are reported.
Branch lengths do not correspond to genetic distances.
Discussion
All three methods used, R-statistics, F-statistics and θ-statistics, agree that pinyon jays in Flagstaff are moderately inbred, yet they have little population structure. The moderate inbreeding was expected because observational data suggest that among-flock dispersal is low. Surprising, however, was the lower than expected population structure. The low dispersal rates that have been reported predicted more structure than was observed. Moderate inbreeding and low population structure could be explained by three alternative hypotheses. The first (the “flock viscosity” hypothesis) proposes that the rate of gene flow among flocks is sufficient to reduce population structure. The second (the “migrant wave” hypothesis) proposes that influxes of migrant pinyon jays into the Flagstaff area disguise the actual population structure of the local metapopulation. The third hypothesis (the “population substructure” hypothesis) proposes that the flock is not the effective breeding unit. Instead, clans within the flocks are the actual breeding units, and expected population structure does exist at that hierarchical level. These hypotheses can be more thoroughly tested with field observation, mitochondrial DNA work, and mathematical modeling. Presently, some empirical and anecdotal evidence supports each of these three hypotheses. Additional empirical work and computer modeling will provide more thorough tests of these ideas.
Because Wright’s F-statistics and Wier and Cockerham’s θ-statistics were designed for allozymes and single-locus, low diversity, dominant markers, these metrics may not be entirely reflective of the actual inbreeding level and population structure. Calculating the level of inbreeding and population structure using Slatkin’s RST and R, which account for multi-locus, high diversity, co-dominant markers provides a more informative metric.
References
Lewis, P. O., and Zaykin, D. 2001. Genetic Data Analysis: Computer program for the analysis of allelic data. Version 1.0 (d16c).
Free program distributed by the authors over the internet from http://lewis.eeb.uconn.edu/lewishome/software.html
Nei, M. 1972. Genetic distance between populations. American Naturalist. 106:283-92.
Nei, M. 1978. Estimation of average heterozygosity and genetic distance from a small number of individuals. Genetics 89:583-590.
Nei, M. 1987. Molecular Evolutionary Genetics. Columbia University Press, New York.
Slatkin, M. 1995. A measure of population subdivision based on microsatellite allele frequencies. Genetics 139:157-162.
Weir, B.S., Cockerham, C.C. 1984. Estimating F-statistics for the analysis of population structure. Evolution. 38:1358-1370.
Wright, S. 1951. The genetical structure of populations. Annals of Eugenics. 15:323-354.
Yeh, F.C., Yang, R., Boyle, T. 1999. Popgene. Microsoft Window-based freeware for population genetic analysis. Version 1.31.
Free program distributed by the authors over the internet from http://www.ualberta.ca/~fyeh/pr01.htm
Acknowledgements
This work was funded by grant #IBN 9882883 from the National Science Foundation, and Northern Arizona University. The opinions and conclusions in this study are those of the study authors, and are not necessarily shared by the National Science Foundation or Northern Arizona University. We thank Northern Arizona University’s College of Engineering and Natural Sciences and the Department of Biological Sciences for their support of and ongoing commitment to undergraduate education and research. We would also like to express our gratitude to the Keim Genetics Laboratory for the use of its facilities and helpfulness of its staff, including Talima Pearson, Joseph Busch, and Sergey Kachur. We would like to acknowledge Bryce Marshall and Kate Behn for their sustained efforts in the field, and Michael Barber and Erin Strasser for their help with data management and analysis.
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