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Inbreeding Depression in the Speke's Gazelle Captive Breeding Program

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Inbreeding Depression in the Speke's Gazelle Captive Breeding Program Contributed Papers Inbreeding Depression in the Speke’s Gazelle Captive Breeding Program STEVEN T. KALINOWSKI,*‡ PHILIP W. HEDRICK,* AND PHILIP S. MILLER† *Department of Biology, Arizona State University, Tempe, AZ 85287–1501, U.S.A. †Conservation Breeding Specialist Group, 12101 Johnny Cake Ridge Road, Apple Valley, MN 55124–8151, U.S.A. Abstract: The Speke’s gazelle (Gazella spekei) captive breeding program has been presented as one of the few examples of selection reducing the genetic load of a population and as a potential model for the captive breeding of endangered species founded from a small number of individuals. In this breeding program, three generations of mate selection apparently increased the viability of inbred individuals. We reanalyzed the Speke’s gazelle studbook and examined potential causes for the reduction of inbreeding depression. Our analysis indicates that the decrease in inbreeding depression is not consistent with any model of genetic im- provement in the herd. Instead, we found that the effect of inbreeding decreased from severe to moderate dur- ing the first generation of inbreeding, and that this change is responsible for almost all of the decline in in- breeding depression observed during the breeding program. This eliminates selection as a potential explanation for the decrease in inbreeding depression and suggests that inbreeding depression may be more sensitive to environmental influences than is usually thought. Depresión por Intracruza en el Programa de Reproducción en Cautiverio para la Gacela de Speke Resumen: El programa de reproducción en cautiverio para la gacela de Speke (Gazella spekei) ha sido pre- sentado como uno de los pocos ejemplos de selección que reducen la carga genética de una población y un modelo potencial para la reproducción en cautiverio de especies en peligro fundado a partir de un número pequeño de individuos. En este programa de reproducción, tres generaciones de selección de pareja incre- mentaron aparentemente la viabilidad de individuos con intracruza. Realizamos el registro genealógico de las gacelas de Speke y examinamos las causas potenciales de reducción de depresión por intracruza. Nuestro análisis indica que la disminución en la depresión no es consistente con ningún modelo de mejoramiento genético en el grupo. Sin embargo, encontramos que el efecto de intracruza disminuyó de severo a moderado durante la primera generación de intracruza, y que este cambio es responsable de casi todas las disminu- ciones de la depresión por intracruza observadas durante el programa de reproducción. Esto elimina a la se- lección como una explicación potencial de la disminución de la depresión, y sugiere que la depresión por in- tracruza puede ser más sensible a influencias ambientales de lo que actualmente se cree. Introduction Ralls et al. 1988). For example, Ralls et al. (1988) esti- mated that full-sib mating increased juvenile mortality by Starting in the late 1970s, inbreeding was documented 33%, on average, compared to noninbred births. This to cause a substantial reduction of fitness in captive pop- and subsequent research has shown that inbreeding af- ulations of endangered species (e.g., Ralls et al. 1979; fects many traits, although to different degrees in differ- ent species, populations, and lineages (e.g., Ralls et al. 1988; Pray & Goodnight 1995; Kärkkäinen et al. 1996; ‡Current address: Conservation Biology Division, Northwest Fisher- Lacy et al. 1996). Avoidance of inbreeding has become a ies Science Center, 2725 Montlake Boulevard East, Seattle, WA primary goal in the management of small populations. 98112, U.S.A. Paper submitted April 29, 1998; revised manuscript accepted Sep- Inbreeding is unavoidable, however, in populations tember 29, 1999. founded from a small number of individuals. This prob- 1375 Conservation Biology, Pages 1375–1384 Volume 14, No. 5, October 2000 1376 Speke’s Gazelle Inbreeding Depression Kalinowski et al. lem has motivated interest in eliminating the genetic ba- drick (1994) doubted that the limited amount of in- sis of inbreeding depression through carefully controlled breeding in the pedigree could have reduced inbreeding breeding and selection. Typically, a purging process is depression to the extent observed, and Frankham envisioned: recessive alleles are exposed to selection by (1995) suggested that the decline in inbreeding depres- inbreeding, and healthy animals are used for subsequent sion might have been caused by the establishment of a matings. The success of purging is expected to depend second population in a zoo with a more favorable cli- strongly on characteristics of the loci causing inbreeding mate. depression. For example, inbreeding depression caused These issues remained unresolved because alternative by increased homozyosity of deleterious recessive alleles explanations for the observations of Templeton and can, in theory, be purged, especially when such alleles Read have not been analyzed in detail and because the are few in number and have a large effect. In contrast, plausibility of the chosen hypothesis has not been thor- inbreeding depression caused by increased homozyosity oughly evaluated. We used a combination of data analy- at loci with heterozygote advantage cannot be purged. sis and visualization to show that previous analysis of the Soon after inbreeding was recognized as potentially Speke’s gazelle breeding program failed to reveal an im- harmful to captive populations, Templeton and Read portant characteristic of the data. We argue that this (1983) described a breeding program that appeared to lapse, along with the lack of alternative explanations, eliminate inbreeding depression from the captive popula- led to inappropriate biological conclusions. tion of the endangered Speke’s gazelle (Gazella spekei). Templeton and Read selected mating pairs for approxi- mately 3 years and claimed that this pedigree manage- Speke’s Gazelle in Captivity: 1970–1982 ment substantially increased the viability of inbred ga- zelles. They attributed this accomplishment to selection From 1970 to 1982, the captive population of Speke’s against deleterious alleles and selection for favorable al- gazelles in the United States was descended from four lele combinations made possible by inbreeding and re- wild-born individuals that were transferred to the St. combination (e.g., Templeton & Read 1994). Louis Zoo by 1972: one male (studbook number 6) and This breeding program received much attention in the three females (nos. 7, 8, 9). No additional founders were conservation biology community and has been followed added to the herd until 1992. By 1979 the herd had in- by extensive investigation of the relationships among ge- creased from the initial four founders to 19 animals netic variation, fitness, selection, and population size. In- (Templeton & Read 1983). breeding depression is present in many species, but its The breeding program of Templeton and Read began genetic basis and response to selection has proven com- in February 1980, although some of the previous mat- plex. Experimental attempts to reduce the effect of in- ings were also planned by Templeton and Read (A. Tem- breeding in small populations of outcrossing organisms pleton, personal communication). Two criteria were have not replicated the dramatic results of the Speke’s used to select individuals to breed (Templeton & Read gazelle captive breeding program. Also, the potential for 1983): (1) breeders were chosen to help equalize founder deliberate inbreeding to increase the probability of pop- representation in the herd, and (2) healthy inbred animals ulation extinction has been emphasized (Hedrick 1994). were used preferentially as parents. Two criteria were Modern captive breeding programs now seek to maxi- used to determine mating pairs among the individuals se- mize the retention of genetic variation (Ballou & Foose lected to breed (Templeton & Read 1983). Mating pairs 1996) using breeding strategies that are still being re- were chosen to produce offspring that descended from as fined (S.T.K., unpublished data). The less conventional many founders as possible and were inbred but not to ex- claims of Templeton and Read (1984) that recombina- cess. Because this breeding program differed from the tion decreased inbreeding depression have received less modern goal of retaining maximum genetic diversity in a attention. population, it probably retained less genetic variation Although the breeding methods of Templeton and than might have been possible. The difference, however, Read have not been adopted by modern population between the breeding program of Templeton and Read managers, the Speke’s gazelle breeding program has be- and that of maximum retention of genetic variation or come an important case study in the conservation biol- maximum avoidance of inbreeding was probably small. ogy literature and is often cited in conservation-oriented discussions of inbreeding depression (e.g., Pennisi 1999). Several authors have questioned both the plausibility of Modeling the Effect of Inbreeding on Viability Templeton and Read’s explanations and the validity of their analysis. Templeton and Read (1998) have success- The relationship between inbreeding and viability is usu- fully responded to critics of their statistical methods ally modeled as (Lacy 1997a; Willis & Wiese 1997), but other issues –Bf have not been explicitly examined. For example, He- SS= 0e (1) Conservation Biology Volume 14, No. 5, October 2000 Kalinowski et al. Speke’s Gazelle Inbreeding Depression
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