FEATURE ARTICLES The Condor 106:215-228 ? The Cooper Ornithological Society 2004 GENETIC STATUS AND MANAGEMENT OF CALIFORNIA CONDORS KATHERINE RALLS1 AND JONATHAN D. BALLOU Department of Conservation Biology, Conservation and Research Center, National Zoological Park, Smithsonian Institution, Washington, DC 20008 Abstract. The last wild California Condor (Gymnogyps californianus) was brought into captivity in 1987. Captive breeding was successful and reintroduction efforts began in 1992. The current population is descended from 14 individuals belonging to three genetic "clans." This population bottleneck led to the loss of genetic variation and changes in allele fre- quencies, including a probable increase in the frequency of the putative allele for chondro- dystrophy, a lethal form of dwarfism. We use studbook data to analyze the current genetic and demographic status of the population and explain how it is managed to meet specific goals. In August 2002 the population consisted of 206 individuals distributed among three captive-breeding facilities and three reintroduction sites. The population is managed to pre- serve genetic diversity using the concept of mean kinship. Growth of the total population has been between 10% and 15% per year since 1987, but the growth of the captive popu- lation has been only about 5% per year since 1992 due to the removal of chicks for rein- troduction. Assuming that founding birds within clans were half-siblings, the birds used to found the captive population theoretically contained 92% of the heterozygosity present in the hypothetical wild base population. About 99.5% of this heterozygosity has been retained in the current population. Alleles from most founders are well represented across captive- breeding facilities and reintroduction sites. The genetic status of this population compares favorably with other species that have been rescued from extinction by captive breeding. Key words: California Condor, captive breeding, genetic management, Gymnogyps cal- ifornianus, reintroduction. Situacion Genetica y Manejo de Gymnogyps californianus Resumen. El ultimo condor californiano (Gymnogyps californianus) silvestre fue puesto en cautiverio en 1987. La reproduccion en cautiverio fue exitosa y las reintroducciones comenzaron en 1992. La poblacion actual desciende de 14 individuos pertenecientes a tres "clanes" geneticos. Este cuello de botella poblacional dio lugar a la perdida de variabilidad genetica y a cambios en la frecuencia de alelos, incluyendo un probable incremento en la frecuencia del alelo para condrodistrofia, una forma letal de enanismo. En este estudio, utilizamos datos del libro genealogico para analizar la situacion genetica y demografica actual de la poblacion y para explicar como se esta manejando la poblacion para cumplir con metas especificas. En agosto del 2002 la poblacion consistia de 206 individuos distri- buidos en tres instalaciones de reproduccion en cautiverio y tres sitios de reintroduccion. La poblacion fue manejada con el proposito de conservar la diversidad genetica usando el concepto de parentesco medio. El crecimiento de la poblacion ha sido de entre 10% y 15% por ano desde 1987, pero el crecimiento de la poblacion en cautiverio ha sido unicamente de aproximadamente un 5% por ano desde 1992 debido a la remocion de los polios para su reintroduccion. Suponiendo que los condores fundadores dentro de cada clan eran medio- hermanos, las aves que fueron utilizadas para fundar la poblacion en cautiverio teoricamente Manuscript received 6 May 2003; accepted 30 November 2003. 1 E-mail: rallsk@thegrid.net [215] 216 CATHERINE RALES AND JONATHAN D. BALLOU contienen un 92% de la heterocigosidad presente en la poblacion silvestre base hipotetica. Cerca de un 99.5% de esta heterocigosidad ha sido retenida en la poblacion actual. Alelos de la mayoria de los fundadores estan bien representados en las diversas instalaciones de reproduction en cautiverio y sitios de reintroduccion. La situation de esta poblacion parece ser mejor que la de otras especies silvestres que han sido rescatadas por medio de la repro- duccion en cautiverio. INTRODUCTION California Condors (Gymnogyps californianus) once ranged over much of southern North Amer- ica. After the end of the Pleistocene, the range of the species contracted toward the West Coast (Emslie 1987). After Europeans arrived, the population began a precipitous decline due to a variety of human impacts (Snyder and Snyder 2000). A small wild population persisted in Cal- ifornia until the 1980s. However, high mortality continued and the last wild California Condor was brought into captivity in 1987 to avoid ex- tinction of the species. The total population then consisted of 27 captive birds (Wallace and Too- ne 1992). Reproduction in captivity was highly successful and by August 2002 the population consisted of 206 individuals divided into four subpopulations: the captive population and re- introduced populations in California, Arizona, and Mexico. Because of this population's history, pedi- grees are available for every individual, regard- less of its location. Thus, California Condors are one of the few species where management rec- ommendations for both captive and wild popu- lations can be based on pedigree analyses (Haig and Ballou 2002). Pedigree analyses provide powerful methods for describing current popu- lation structure, determining the genetic impor- tance of specific individuals to current and fu- ture populations, and monitoring loss of genetic diversity over time (Haig and Ballou 2002). While pedigree analyses are routinely used for management of captive populations, they are un- fortunately often unavailable for wild popula- tions. The California Condor population belongs to one of over 100 Species Survival Plans spon- sored by the American Zoo and Aquarium As- sociation (2003). These populations of threat- ened and endangered species are managed across the participating breeding facilities to re- tain, as far as possible, the genetic diversity pre- sent in the wild source population (Rails and Ballou 1992, Frankham et al. 2002). Managing to maintain genetic diversity helps counter ad- aptation to the captive environment, minimizes possible deleterious effects of inbreeding, and preserves the population's capacity for genetic adaptation to environmental changes (Rails and Ballou 1992). Specific goals for the California Condor pop- ulation include maximizing the growth of the captive population under the constraint of pro- ducing as many chicks as possible for reintro- duction; ensuring that genetic diversity is well represented at each captive-breeding facility; minimizing the expression of chondrodystrophy (Thorp 1994), a lethal form of dwarhsm (Rails et al. 2002); transferring all the genetic diversity available in the captive population to the wild; and ensuring that each reintroduction site has the full genetic representation of the captive popu- lation. Decisions must be considered carefully, because it is often not possible to simultaneously maximize progress toward these multiple man- agement goals. Here, we use pedigree analyses to analyze the current demographic and genetic status of the condor population and illustrate how manage- ment decisions, such as choosing new pairs and deciding whether to reintroduce individual chicks to the wild, are made. Our specific ob- jectives were to (1) determine the growth rate and age structure of the population; (2) deter- mine the current genetic structure of the total population; (3) compare the genetic structure of the various subpopulations; and (4) conduct analyses to assist with 2002 management needs. These management needs included a genetic evaluation of existing pairs, recommendations for new pairings, identification of genetically less valuable birds that could be used for pur- poses other than breeding (e.g., as exhibit birds), selection of pairs to begin a new captive sub- population at the Oregon Zoo, and recommen- dations for appropriate placement of the chicks hatched in 2002 in the various subpopulations. METHODS PEDIGREE ANALYSIS AND TERMINOLOGY Pedigree analyses measure genetic parameters relative to a base population, which is assumed STATUS AND MANAGEMENT OF CALIFORNIA CONDORS 217 to be a wild source population from which ran- domly captured individuals (founders) would be unrelated (i.e., the kinship coefficients among founders are 0.0; Falconer and Mackay 1996). Thus measures of genetic diversity determined by pedigree analyses estimate losses or changes relative to this hypothetical wild base or source population. Here we use the pedigree analysis software PM2000 (Pollak et al. 2002) to calcu- late changes in heterozygosity, levels of inbreed- ing, mean kinship among individuals, and sur- vival and loss of founder alleles in the condor population. Because of extensive work with domesticated, laboratory, and captive populations, software needed to carry out various pedigree calcula- tions is widely available. Although some param- eters such as inbreeding and kinship coefficients can be calculated directly (Ballou 1983), direct calculation of other parameters, such as survival probabilities for individual founder alleles, is be- yond the capabilities of most desktop computers (Thompson 1983). Therefore, such probabilities are estimated with "gene drop" simulations (Mace 1986, MacCluer et al. 1986, Lacy 1989). Gene drop analyses begin by giving each found- er two unique alleles. These unique alleles are then "dropped" down through the pedigree ev- ery generation, assuming Mendelian inheritance, so that each descendant receives one allele se- lected randomly from its mother and one from its father. Many iterations (typically 10 000) are performed to simulate sampling broadly throughout each individual's genome. (Each it- eration can be thought of as representing sto- chastic Mendelian events at a different locus.) Gene drop models assume independence be- tween model runs, thus no linkage, and no se- lection (Haig and Ballou 2002). These assump- tions are untrue to whatever extent linkage and selection occur in particular genetic systems in real organisms. Heterozygosity. Heterozygosity (H) is calcu- lated from gene drop models by counting the allele frequencies of the founder alleles in the living extant population each simulation, aver- aging frequencies over simulations to obtain av- erage allele frequencies (pj and estimating H us- ing the formula for expected heterozygosity: H = 1 ? X/>i2. Thus, heterozygosity is interpreted as the proportion of the base population's het- erozygosity retained in the extant captive pop- ulation. This relative or proportional heterozy- gosity is often referred to as gene diversity in the captive-breeding literature (Lacy 1989). H as calculated in pedigree analysis is not directly re- latable to molecular estimates of heterozygosity because it is proportional to expected heterozy- gosity in the base population (i.e., if H = 0.90, then the population has 90% of the base popu- lation's heterozygosity, whatever that might have been). Founder genome equivalents. A useful con- cept related to retained heterozygosity is founder genome equivalents (fg). This is the number of unrelated founders needed to establish a new population with the same levels of heterozygos- ity as that in the present population and is cal- culated as 1/[2(1 ? H)]. Thus, for example, a population with H = 0.9 has 5 founder genome equivalents; only five unrelated founders would be needed to establish a population with an ini- tial H = 0.9 (Lacy 1989, 1995). Founder allele survival. The proportion of a founder's genome that survives to the extant population ("allele retention," or r) is also cal- culated using gene drop models (Thompson 1986, Lacy 1989). A founder that produces only one offspring in the extant population has 50% allele retention because only one-half of its genes have been passed on to the single off- spring. Founders with more complex descendant pedigrees will show more or less retention de- pending on the exact structure of their descen- dant's pedigrees. Founder allele survival is cal- culated as the proportion of a founder's two al- leles that are present in the extant population. There are only three possibilities for a founder in any given simulation: neither allele present = 0%, only one present = 50%, both present = 100%; these are averaged over all simulations (Lacy 1989, Thompson 1986). Mean kinship and inbreeding. Mean kinship is used to identify genetically important individ- uals. Mean kinship (mk;) is calculated for every living animal in the population as the average kinship between that individual and all individ- uals in the population, including itself (Ballou and Lacy 1995). Individuals with low mean kin- ship have fewer or less-closely related relatives than those with high mean kinships. Ballou and Lacy (1995) showed that breeding strategies that preferentially select animals with low mean kin- ships are the best at retaining expected hetero- zygosity in the population, since average mean kinship is directly related to expected heterozy- 21!< CATHERINE RALES AND JONATHAN D. BALLOU gosity (H = 1 ? mk). Thus, minimizing average mean kinship in the population maximizes het- erozygosity. Most, if not all, captive-breeding programs now use mean kinship when selecting animals to breed (Ballou and Foose 1996). Inbreeding coefficients (F) measure the de- gree of kinship between the parents of an indi- vidual and are calculated as the probability that an individual will receive two alleles that are identical by descent from the base population (i.e., two copies of the same founder allele; Fal- coner and Mackay 1996). Unrelated parents pro- duce offspring with F = 0, while brother-sister, mother-son or father-daughter pairs produce off- spring with F = 0.25. Both mean kinships and inbreeding coefficients are calculated directly from the pedigree using an additive relatedness matrix (Ballou 1983) rather than gene drop. DATA The data needed for population management, in- cluding births, deaths, parentage, and location of each individual, are recorded in the California Condor Studbook, currently maintained by Mi- chael Mace at the San Diego Wild Animal Park (Mace 2002). Studbook data change constantly as individuals hatch, die, are moved between captive locations, or are reintroduced to the wild. We analyzed studbook data as of 21 Au- gust 2002, but modified those data by assuming scheduled transfers to new locations had already taken place. In general, we refer to individual condors by their studbook numbers. In some cases, we also provide names to facilitate com- parisons with other sources on the population (e.g., Snyder and Snyder 2000). INCORPORATING CLAN STRUCTURE INTO THE PEDIGREE The relationships among some of the first 27 California Condors in the captive-breeding pro- gram were known from observations in the wild (Fig. 1). Birds identified as studbook numbers 2, 3, 4, 8, 9, and 10 were never brought into cap- tivity but were known to be the parents of some that were (e.g., as eggs) and are therefore in- cluded in the studbook. The known pedigree re- lationships suggested that the population de- scended from 14 individuals (Fig. 1). We call these 14 individuals the "apparent founders" (marked by asterisks in Fig. 1). However, DNA fingerprinting indicated that the captive condors fell into three basic groups or clans (Geyer et al. 1993). Birds within clans were more closely re- lated to each other than birds belonging to dif- ferent clans. Although Geyer et al. (1993) could not determine the absolute level of relatedness among clan members with high accuracy, it was clear from their analysis that any captive-breed- ing strategy designed to maintain genetic diver- sity would need to incorporate the information on clan structure. To incorporate the clan structure into the ped- igree prior to analysis, we modified some stud- book data to create an analytical studbook that we used for all analyses (Geyer et al. 1993; Fig. 1). For analytical purposes, we therefore as- sumed that birds within a clan had a coefficient of kinship of 0.125 (half-sibs), unless known otherwise from recorded pedigree information, and that kinship coefficients were 0 for individ- uals belonging to different clans. Assuming half- sib relationships among clan members is not un- realistic, given the California Condor's known history of small population size before the last birds were brought into captivity. To establish these levels of relationships among the apparent founder birds in the stud- book, we created hypothetical parents for them (Fig. 1). Each wild-caught bird within a clan was given a common hypothetical sire (i.e., HA, HB, or HC) and a unique hypothetical dam (e.g., HI, H2, etc, where the number was the same as the studbook number of the wild-caught individual). This structure achieved the desired result of members within a clan having kinships of 0.125, but kinships between clans being 0. By adding these hypothetical parentages, we increased the number of founders that contributed to the cap- tive population. The population now had 17 founders (a unique dam for each apparent found- er plus three added sires; Fig. 1). We call these 17 individuals the "analytical" founders. ANALYSES Analyses were conducted using SPARKS Stud- book Management software (ISIS 1994); PM2000 version 1.16 (Pollak et al. 2002), MateRx version 1.9 (Ballou et al. 2001) and METAMK (Ballou 1999). PM2000 was used to evaluate the current demographic and genetic status of the total population. The probability that individuals carried the putative chondrodys- trophy allele was calculated based on the pedi- gree for this trait given in Rails et al. (2000). STATUS AND MANAGEMENT OF CALIFORNIA CONDORS 219 "HB"' H13 H20 FIGURE 1. Pedigree of the 33 California Condors at the beginning of the captive breeding program. The 14 "apparent founders" are marked with an asterisk. The 17 "analytical founders," added to define the hypothesized clan relationships among condors based on molecular analysis, are shown with dotted lines. Birds that died in the wild before being brought into the captive-breeding program are shaded. PM2000 was also used to compare the genetic structure of various subpopulations. The propor- tion of founders' alleles remaining in each sub- population was estimated by conducting a gene drop analysis for each subpopulation. The max- imum proportion of each founder's alleles re- tained (rmax) is determined by the number of off- spring produced (n): rmax = 1 - 0.5". Since the hypothetical dams (HI, H2, H3, . . . , H20) pro- duced only one offspring each (the actual found- ers 1, 2, 3, ... , 20), their maximum is 0.5. Since the hypothetical sires (HA, HB, HC) produced two, four and eight F, offspring, respectively, their maximum potentials are 0.75, 0.94 and 0.99. Several other programs were used for the analyses to assist with 2002 management needs. We used MateRx to evaluate the genetic value of existing pairs. This program calculates a sin- gle numeric index for every male-female pair in the population that indicates the relative genetic benefit or detriment to the population of breed- ing that particular pair (Ballou et al. 2001). This index, the mate suitability index, is calculated from considering the pair's mean kinship, the difference in the male's and female's mean kin- ship, the inbreeding coefficient of the offspring that would be produced, and the amount of un- known ancestry in the pair. (At present, the con- dor population does not contain living individ- uals with unknown ancestry.) MateRx is de- signed to simplify the decisions about which pairs should be bred by condensing all that is known about the genetics of a pair into a single number. Mate suitability indices are labeled as beneficial (1, 2, or 3) indicating most to margin- 220 CATHERINE RALES AND JONATHAN D. BALLOU ally beneficial, or detrimental (4, 5, or 6, indi- cating slightly to highly detrimental) to the pop- ulation, while "?" indicates that the pairing should not be considered in any case as the kin- ship of the pair, and the inbreeding coefficient of any offspring produced, is greater than 0.125. Beneficial mate suitability indices denote no det- rimental effects relative to the genetic values of that pair, and 4, 5, or 6 indicate at least one detrimental effect. MateRx was used with the default settings ex- cept for the definitions of bins used to evaluate the effect of differences in mean kinship be- tween males and females. Initial modeling sug- gested that the default settings in MateRx might overcompensate for differences in mean kinship and label as detrimental pairs that would other- wise be considered suitable (R. Lacy, pers. comm.), particularly when all females are being bred, as is the case here. We therefore recali- brated MateRx so that pairs with differences in mean kinship less than 1.5% were defined as suitable (with differences less than 0.5%, less than 1.0% and less than 1.5% given ranks 1, 2, and 3 respectively) and differences greater than 1.5% as detrimental (with differences greater than 1.5%, 2.0%, and 2.5% receiving ranks 4, 5, and 6 respectively). We also used MateRx to choose new pairs. First, we ranked the females available for pair- ing in order from lowest (most genetically valu- able) to highest (least genetically valuable) mean kinship. For each female, we then listed four or more males that would be suitable mates in terms of producing the lowest possible mate suitability indices for the resulting pair. Many males were suitable mates for more than one fe- male, so we noted their current location as well. We then chose the best mate available for each female, beginning with the most genetically valuable female at the top of the list. If pairing with more than one male would produce the same mate suitability index, we chose a male at the same location as the female to minimize the number of individuals that would have to be moved from one institution to another. We avoided choosing pairs that likely would be be- haviorally incompatible, for example a very dominant female with a young, sexually inex- perienced male, in the opinion of those familiar with the individual birds. We also avoided pai- rings that would have a high probability of pro- ducing a chick with chondrodystrophy (Rails et al. 2000). Once we had selected a male for a given female, we crossed that male off as a pos- sibility for all other females lower down on the mean kinship list. We selected pairs to be sent to the new facility at the Oregon Zoo based partly on availability and partly on genetic background. METAMK (Ballou 1997) was used to select a genetically diverse set of pairs. METAMK uses changes in mean kinships to calculate the increase or de- crease in heterozygosity for both a source and destination population when a specific individ- ual is moved from one to the other (Ballou 1997). In this case, the source population is the entire captive population and the destination population is Oregon Zoo. The first pair was chosen on the basis of minimizing genetic loss to the existing captive population and subse- quent pairs were selected iteratively partly on the basis of their low level of relatedness to birds already chosen to go to Oregon, and partly on availability (i.e., not already paired up). "Mentors" are adult or nearly adult birds that are placed with groups of captive-born chicks to help them develop appropriate social behavior and fear of humans. Mentors were evaluated on the basis of mean kinship as calculated by PM 2000 (Pollak et al. 2002). Because mentors are not used for breeding, they should be selected from the less genetically valuable individuals, that is, those with high mean kinship. METAMK was also used to make recommen- dations regarding which chicks should be re- tained in the captive (source) population and which should be reintroduced to the wild (the destination population). Haig and Ballou (2002) illustrated this procedure using data for golden lion tamarins (Leontopithecus rosalia). ME- TAMK was again used to recommend which of the chicks to be reintroduced should be released in California and which should be released in Arizona. First, we assumed that all chicks to be reintroduced were part of the wild California population. METAMK then provided data on the genetic costs and benefits (i.e., increase or de- crease in heterozygosity) of either keeping that chick in the wild California population, or trans- ferring it to Arizona. Placement of chicks was determined by the effect on overall heterozy- gosity (average change in H in California and Arizona caused by transferring the chick). STATUS AND MANAGEMENT OF CALIFORNIA CONDORS 221 250 ? 200 o 150 ra 100 Q. O a. bO Annual growth overall - Annual growth captive 10-15% - 3-6% _c^*^ o-o-?"'? -*- Total o Captive Year FIGURE 2. Growth of the California Condor popu- lation since captive breeding began in 1987 showing both the total number of birds at the end of each year and the number in captivity. RESULTS STATUS OF THE POPULATION AND ITS SUBPOPULATIONS Demography. There were 206 birds in the pop- ulation on 21 August 2002, with 113 in captivity and 93 in the wild. The captive birds were dis- tributed among three facilities: 32 at the Los An- geles Zoo, 35 at the San Diego Wild Animal Park, and 46 at the World Center for Birds of Prey in Boise, Idaho. The wild birds were divid- ed into three subpopulations: 50 in California, 37 in Arizona, and 6 in Baja California, Mexico. Growth of the total population has been between 10% and 15% per year since 1987 (Fig. 2), when the last wild birds were brought into captivity. Since 1992, the growth of the captive population has been only about 5% per year due to the re- moval of chicks for reintroduction each year. The age structure of the current population is relatively young because the captive population has been in existence only since the late 1980s. Most birds older than about 14 years are wild- caught birds and their ages are estimates. Over- all, there is a balance between males and fe- males, and the age structure is typical of a rap- idly growing population (Fig. 3a). The wild pop- ulation consists mostly of young birds and a few adults that have recently attained sexual maturity (at 5-6 years of age; Fig. 3b). The age structure of the captive population (Fig. 3c) shows a def- icit of animals in age classes 1-4 years because almost all chicks for the last 5 years have been reintroduced. Given management goals and the current de- mography of the population, it is still appropri- ate to breed all adult females in captivity to in- crease the size of the population as rapidly as 0 < 30 20 10 (a) Total Females 20 15 10 5 0 5 10 15 30 -i (b) Wil - =? 20 - 10 - - 0 20 15 10 10 15 (c) Captive 20 15 10 5 0 5 10 No. of condors 15 FIGURE 3. Age structures of the (a) total, (b) wild and (c) captive California Condor populations. possible and provide chicks for reintroduction. There is also a need to begin retaining some chicks in captivity to rectify the deficit of youn- ger individuals in the captive population. Genetic analyses. Any assumption that the 14 apparent founders are related in some way will result in an immediate loss of heterozygosity in the captive population compared to the amount that would have been present if the founders had been unrelated. Our assumption that the birds within clans were half-sibs resulted in an aver- age kinship of 8% among the 14 apparent found- ers, meaning that on average they were slightly more related to each other than cousins (Table 222 CATHERINE RALES AND JONATHAN D. BALLOU TABLE 1. Summary of California Condor population genetics. Retained heterozygosity is the estimated pro- portion of the heterozygosity of the wild California Condor population prior to its bottleneck that is retained in the present-day population. Founder genome equivalents are the number of unrelated founders that would be needed to establish a population with the same level of retained heterozygosity as shown in the population. Apparent founders Captive population Genetic population Arizona California Total characteristics (n = 14) (n = 206) (n = 113) (? = 37) (n = 50) 0 = 93)* No. analytical founders represented 17 17 17 16 16 17 Proportion heterozygosity retained 0.920 0.914 0.915 0.897 0.901 0.901 Founder genome equivalents 6.2 5.8 5.9 4.9 5.0 5.4 Mean inbreeding 0.00 0.03 0.04 0.01 0.02 0.02 a Includes six condors in Baja California. 1). Under this assumption, the birds used to found the captive population contained only 92% of the heterozygosity contained in the hy- pothetical wild base population prior to its bot- tleneck (Table 1). This equates to 6.2 founder genome equivalents. In the current population, (wild and captive combined) heterozygosity is 91.4%, down only slightly from the 92.0% of the founders (Table 1). Thus about 99.5% of the heterozygosity that the founders brought into the population has been retained in the current pop- ulation. This is because condors are long-lived and the captive population has been under ge- netic management since its inception. The average mean kinship for the total pop- ulation is 0.086 with individual mean kinships ranging from 0.067 to 0.108 (Fig. 4). A mean kinship of 0.063 is equivalent to an individual being related to the population on average at the Average = 0.086 1 (Topa) 5 (ACS) 33 (Sequoia) a 21 (AC96) 44 (Nojoqui 0.060 0.070 0.080 0.090 0.100 0.110 Mean kinship FIGURE 4. Frequency distribution of mean kinship values in the living population of California Condors. Average mean kinship is 0.086. The three birds with the lowest mean kinship (most valuable) and the two with the highest (least genetically valuable) are iden- tified. level of first cousin; a mean kinship of 0.125 is comparable to half-sibs. While all birds should be bred, birds with mean kinships below the av- erage should be given the highest breeding pri- ority. This applies, in particular, to the three birds with the lowest mean kinships (birds 1,5, and 33; Fig. 4). The frequency distribution of the probability of carrying the putative chondrodystrophy allele (Rails et al. 2000) for the total population is shown in Figure 5. The average probability of being a carrier is 18%, although there are only two living birds that are known to be carriers (27 and 31; the parents of four of the five chon- drodystrophic chicks produced so far). However, there are many birds with at least a one-in-three chance of being a carrier. Genetic structure in the subpopulations. Re- tained heterozygosity is somewhat lower in the wild than in captivity (Table 1), which is not surprising since some of the more genetically valuable animals and their descendants have not 80 60 3 40 20 0 I 0.0 0.1 0.2 0.3 0.4 0.5 0.6 0.7 0.8 0.9 1.0 Chondrodystrophy carrier (P) FIGURE 5. Frequency distribution of the probability of an individual California Condor carrying the lethal chondrodystrophy allele. All 206 living birds are in- cluded. Two birds are known carriers (P = 1.0). STATUS AND MANAGEMENT OF CALIFORNIA CONDORS 223 1.0 n Wild Arizona 0.5- nnnnnnn.nnnnn 1.0 0.5 0.0 Wild California m "m tn (5 c 3 ? c o '?e o o 1.0 0.5 0.0 1.0 0.5 0.0 1.0 0.5 0.0 1.0 0.5 0.0 Captive (total) Los Angeles Zoo nnnllllnnnPHii San Diego World Center Oregon Zoo n,n,n,n,n,n,n,n,n,n,f1,n,n,n,n H1 H2 H3 H4 H5 H6 H7 H8 H9 H10 H11 H12 H13 H20 HA HB HC FIGURE 6. Proportion of founders' alleles present in subdivisions of the California Condor population. San Diego refers to the San Diego Wild Animal Park and World Center refers to the World Center for Birds of Prey in Boise, Idaho. Alleles from analytical founder HI are missing in Arizona and alleles from founder H9 are missing in California and the World Center. yet been reintroduced. The level of inbreeding is less in the wild because only non-inbred birds have been reintroduced and wild birds have yet to breed. There are only small to moderate differences between the wild populations in California and Arizona based on heterozygosity (Table 1). FST, a common measure of genetic differences be- tween populations (Frankham et al. 2002), is only 0.009, indicating only minor differences in the frequency of founder alleles in the two pop- ulations. We did not evaluate the wild popula- tion in Baja California because it was estab- lished with only six birds in 2002. A more detailed genetic comparison of the wild populations in California and Arizona is provided by estimates of the proportion of each analytical founder's alleles that are present in each population (Fig. 6). The most obvious dif- ference between these two subpopulations is that alleles from bird number 1 ("Topa") are missing from the Arizona population, and alleles from bird 9 are missing from the California popula- tion. Number 1 is still alive and reproducing but 9 is dead. Its alleles are represented in the pop- ulation through its offspring, 33 ("Sequoia"). Condor number 7 ("AC5") is also underrepre- sented in the Arizona population. The founders' alleles also are fairly well dis- tributed between the three current breeding fa- cilities (Los Angeles, San Diego Wild Animal Park, and World Center for Birds of Prey; Fig. 6), although the World Center for Birds of Prey lacks alleles from condor 9. Genetic deficits in specific wild or captive populations can be rec- tified by moving individuals carrying alleles from the underrepresented founders to the ap- propriate location. MANAGEMENT RECOMMENDATIONS FOR 2002 Genetic evaluation of existing pairs. We evalu- ated the genetic value of all current pairs in the population by calculating mate suitability indi- 12 3 4 5 6- Mate suitability index FIGURE 7. Frequency distribution of the mate suit- ability indices for the 34 condor pairings prior to the 2002 genetic management recommendations. Mate suitability index scores of 1, 2, or 3 indicate mostly to marginally beneficial pairs. Scores of 4, 5, or 6, indi- cate slightly to highly detrimental pairs for maintaining genetic diversity in the population. Pairs receiving a "?" should not be considered in any case because the kinship of the pair, and the inbreeding coefficient of any offspring produced, would be greater than 0.125. The three highly undesirable pairings (with scores of 6) were broken up and the individuals re- paired with other birds. 224 CATHERINE RALES AND JONATHAN D. BALLOU re 3 Q. o a. i 0.0012 0.0008 0.0004 % 0.0000 B -0.0004 ? #280 ? * ? ? + Wild - Captive ? + Wild ? ? a + Captive < # #264 a i' - Wild - Captive ? - Wild + Captive -0.0008 -0.0003 -0.0002 -0.0001 0.0000 0.0001 0.0002 Change in H in captive population FIGURE 8. Expected changes in heterozygosity in the captive and wild California Condor populations resulting from reintroducing individual captive chicks into the wild. Each point shows the negative or positive change in heterozygosity in the captive and wild population if that individual were to be reintroduced. ces for each pair (Fig. 7). Three existing pairs were judged genetically detrimental, with a mate suitability index of 6: individuals 20 and 29, 44 and 45, and 33 and 79. These pairs were detri- mental because a bird with a very low mean kinship was paired with a bird with a very high mean kinship. Such matings are undesirable be- cause they link rare alleles with overrepresented alleles in any offspring (Ballou and Foose 1996). Choosing new pairs. The pool of individuals available for pairing included those from the three pairs with high mate suitability indices that needed to be re-paired, those from four pairs that appeared incompatible based on poor reproduc- tive performance and behavioral observations, and all unpaired captive birds of breeding age except for mentors. The pairing procedure based on mean kinship resulted in 11 new pairs for a total of 39 potentially breeding pairs. No males were available for the remaining five females, all of which had high mean kinships and thus were judged suitable for uses other than breed- ing, such as placement in exhibits or use as men- tors. Genetic evaluation of mentors. Genetic re- view of the existing mentors indicated that two birds, 63 and 64, had mean kinships that fell in the high end of the distribution and were appro- priate for long-term use as mentors (as opposed to breeders). However three others, 138, 140, and 141, had lower mean kinships (in the low end of the distribution) and should be used in the captive-breeding program sometime in the future once replacement mentors are developed. Three less genetically valuable birds, 36, 59, and 79, were identified as possible new mentors. Creating a new captive population. We se- lected six pairs to begin the new captive popu- lation at the Oregon Zoo. While all founders are represented (Fig. 6), less than 25% of the ge- nome is represented for the majority of founders. This is to be expected given this small number of individuals and can be improved by the ad- dition of pairs as they become available. Placing the 2002 chicks. 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