estimates of rate of loss of genetic variability. Keywords: effective population size, genetic variability, pedigree, inbreeding, demographic model, red-cock-.
Biological Conservation 71 (1995) 299 304 © 1995 Elsevier Science Limited Printed in Great Britain. All rights reserved 0006-3207/95/$09.50+.00
0006-3207(94)00050-6
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INBREEDING RATE A N D EFFECTIVE POPULATION SIZE: A COMPARISON OF ESTIMATES FROM PEDIGREE ANALYSIS A N D A DEMOGRAPHIC MODEL Bradley F. Blackwell,* P. D. Doerr Department of Zoology, Campus Box 7617, North Carolina State University, Raleigh, NC 27695-7617, USA
J. Michael Reed Eeology, Evolution, and Conservation Biology Program, 1000 Valley Rd, University of Nevada, Reno, Nevada 89512, USA
&
Jeffrey R. Waiters Department of Biology. 2119 Derring Hall, Virginia Polytechnic Institute and State Univ., Blacksburg, Virginia 24061. USA
(Received 12 September 1993; revised version received 11 May 1994; accepted 15 June 1994) (Gilpin & Soulr, 1986). In isolated, wild populations genetic variation is lost primarily through genetic drift (Franklin, 1980). Results from studies in both captive and wild populations often indicate that inbreeding is associated with decreased reproductive rates (Ralls et al., 1980; Rails & Ballou, 1983), disease resistance, growth rates, and developmental stability (Allendorf & Leary, 1986. Animal breeders advise a maximum rate of inbreeding of no more than 2 3% (Dickerson et al., 1954), and inbreeding rates of no more than 1% are suggested for maintaining wild populations for short periods of time (Franklin, 1980). Knowledge of the inbreeding rates of wild populations can aid managers in efforts to conserve genetic variability. There are several methods of estimating inbreeding, both directly and indirectly. One direct method involves sampling individuals from a population over time, then estimating inbreeding from loss of alleles (Waples, 1989). Also, rates of allelic loss can be simulated (Harris & Allendorf, 1989). A commonly used indirect method of estimating rate of loss of genetic variability involves calculating the effective population size from demographic traits (e.g. Hill, 1972; Emigh & Pollak, 1979). To date, however, comparisons of this commonly used method with direct measures of loss of genetic variability, such as using a pedigree (Wright, 1922), have not been made for wild populations (Kimura & Crow, 1963). Demographic and pedigree data were available from a long-term study of the endangered red-cockaded woodpecker, thus allowing a comparison of F calculated using a demographic model with an estimate of F from a pedigree. These data come from approximately 550 adult red-cockaded woodpeckers Picoides borealis in south-central North Carolina, USA that have been
Abstract
Demographic. models have been used to calculate effective population size, (Ne) which is a measure of the expected rate of loss of genetic variability'. However, accurately' calculating effective size for most populations of wild vertebrates is difficult because the required demographic or pedigree data are unavailable. We used data from a long-term study' of the endangered red-cockaded woodpecker Picoides borealis in south-central North Carolina to construct a pedigree, which we then used to calculate the realized rate of inbreeding (F). We compared our values, estimated via pedigree analy,sis, with published, expected values o f F calculated jrom a demographic mode{ The change in inbreeding coefficient per generation (AF) based on a demographic model fell below the 95% confidence limit around the pedigree value. Thus, AF, as calculated from a demographic model, significantly underestimated the AF estimated via pedigree analysis. We suggest that a multi-method approach can be useful to managers in increasing the accuracy of estimates of rate of loss of genetic variability. Keywords: effective population size, genetic variability, pedigree, inbreeding, demographic model, red-cockaded woodpecker.
INTRODCTION Habitat fragmentation can divide previously large, contiguous populations into smaller, isolated populations (Forsman et al., 1984; Rosenfield et al., 1992), disrupting gene flow and resulting in loss of genetic variability *Present address: Department of Wildlife, 240 Nutting Hall, University of Maine, Orono, ME 04469, USA. 299
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B. F. Blackwell, J. M. Reed, J. R. Waiters, P. D. Doerr
study area from two populations, which together contained approximately 550 individually banded adults. For further details regarding data collection see Carter et al. (1983) and Walters et al. (1988). Our analyses were restricted to two study areas, Southern Pines/Pinehurst (SOPI) and Fort Bragg (FB) (Fig. 1), which are in close proximity to each other and frequently exchange successful breeders (Wakers et al., 1988). The FB and SOPI study areas are geographically separate from the Sandhills Gamelands (SGL) study area (Fig. 1) and recent electrophoretic data provide evidence that red-cockaded woodpeckers from SGL are genetically distinct from the FB/SOPI population (Stangel et al., 1992). The area separating the FB/SOPI population and the SGL population (MIN) is made up of predominantly private lands (Waiters et al., 1988) that contain little habitat for red-cockaded woodpeckers. However, one aggregation of birds within the MIN study area has frequently exchanged successful breeders with the FB/SOPI population and, thus, these groups were included in the FB/SOPI population.
studied in detail for over 11 years, with emphasis on population dynamics and demography (Carter et al., 1983; Walters et al., 1988; Walters, 1990). This species is endemic to mature, fire-maintained, pine savannahs of the southeastern United States (Jackson, 1971). Logging, agriculture, development, and fire suppression have fragmented and reduced this plant community, causing populations of red-cockaded woodpeckers to decline in size and become more isolated (Jackson, 1971, 1978; Lennartz et al., 1983). Fire suppression reduces quality habitat for red-cockaded woodpeckers by allowing deciduous understory to develop (Van Balen & Doerr, 1978; USFWS, 1985). The increase in isolation due to habitat fragmentation has resulted in erosion of heterozygosity in some populations (Stangel et al., 1992). Reed et al. (1993) calculated the expected rate of loss of genetic variability in red-cockaded woodpeckers from the Sandhills of North Carolina using a demographic model (Emigh & Pollak, 1979). We compared the value of AF calculated by Reed et al. (1993) with a value estimated using a pedigree from the same population. Our objectives were (1) to estimate age-specific reproductive values for male and female red-cockaded woodpeckers (Appendix 1); (2) to determine AF over a period of 8 years from a pedigree of red-cockaded woodpeckers; and (3) to compare our results with those obtained by Reed et al. (1993) using a demographic model.
Pedigree eontruction A pedigree can be used to determine the realized rate of loss of genetic variability without making assumptio,~s regarding the mating pattern (Wright, 1922; Kempthorne, 1969). However, because we have no information prior to 1980, we assumed an initially outbred population for the first generation of our pedigree, an assumption supported by (1) observations that the mating pattern of the red-cockaded woodpecker indicates inbreeding avoidance (Waiters et al., 1988); and (2) our interest in incremental changes in the inbreed-
METHODS Defining populations Data used to develop Reed et al.'s (1993) life table were collected from 1980 through 1987 on a ll0000-ha
0 2 4 6 8
km
MIN
SOPI
FB
SGL
Fig. 1. Sandhills Gamelands (SGL), Minor (MIN), Southern Pines and Pinehurst (SOPI), and Fort Bragg (FB) study areas.
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Inbreeding rate and effective population size
ing coefficient per generation (AF), and not the actual inbreeding coefficient (F). Thus, the initial rate of inbreeding was not critical. By using (AF) in our calculation of N~ we examined the accumulation of inbreeding over time. Progeny of a closely related mating have a higher coefficient of inbreeding than those of less closely related matings, and their presence raises the average coefficient of inbreeding for the population at any time (Franklin, 1980). However, Franklin (1980) notes that periodic matings of closely related individuals will not severely affect the rate at which the coefficient of inbreeding for the population accumulates. Our assumption concerning the validity of the observed mating pattern for red-cockaded woodpeckers used in our pedigree (i.e. cuckoldry does not occur) was based on two findings. First, extra-pair copulations have not been observed (Walters et al., 1988). Second, Haig et al. (1993) report that DNA profiles of redcockaded woodpeckers in the Savannah River Site in South Carolina, USA revealed no cases of extra-pair matings. Likewise, DNA profiling of our population (Haig et al., in press) shows no significant differences in mean similarity indices when compared with our pedigree analysis (c~=0-05, R2=0-87, d.f.=14, p 2
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Fig. 2. Age and sex-specific reproductive value (V,.) for a population of red-cockaded woodpeckers in south-central North Carolina, USA.
