genealogical analysis of a closed herd of black hairless iberian pigs

1843

Conservation Biology, Pages 1843–1851Volume 14, No. 6, December 2000

Genealogical Analysis of a Closed Herd ofBlack Hairless Iberian Pigs

MIGUEL A. TORO,* JAIME RODRIGAÑEZ, LUIS SILIO, AND CARMEN RODRIGUEZ

Departamento de Mejora Genética y Biotecnología, Instituto Nacional de Investigación y Tecnología Agraria y Alimentaria, Carretera La Coruña km. 7, 28040-Madrid, Spain

Abstract:

Livestock breeds are recognized as important components of world biodiversity. The Iberian pig is aswine breed well adapted to the Mediterranean forest ecosystem and provides cured products of high quality.The ancient population of Iberian pigs (

Sus scrofa meridionalis

) was differentiated in several local types, theblack hairless pigs representing the fattest genetic type. The conservation program of the Guadyerbas strainhas maintained this germplasm isolated since 1945 as a closed population in an experimental herd. The com-plete pedigree, with 1000 breeding animals descending from 24 founders, has been used to measure along thesuccessive cohorts of breeding animals the effective number of founders, effective number of nonfounders,founder genome equivalents, and expected number of founders’ surviving alleles. For the last cohort, the val-ues were 10.34, 1.42, 1.25, and 4.06, respectively. The evolution of inbreeding and coancestry and its compo-nents attributable to each founder were also studied. The rate of increase in inbreeding and coancestry was2.21% per cohort, or 0.906% per year. Finally, the effect of family structure and mating tactics on the evolutionof coancestry was also analyzed. The greatest rates of coancestry per cohort were attributable to unbalancedfamily sizes, and the use of minimum coancestry matings effectively delayed the increase in inbreeding.

Análisis Genealógico de una Manada Aislada del Cerdo Ibérico Lampiño Negro

Resumen:

Las razas de ganado son consideradas como un componente importante de la biodiversidad mun-dial. El cerdo Ibérico es una raza de cerdos bien adaptada al ecosistema forestal del Mediterráneo y proveeproductos encurtidos de alta calidad. La población ancestral del cerdo Ibérico (


) eradiferenciada en diversos tipos locales, siendo los cerdos lampiños negros los representantes del tipo genéticomás gordo. El programa de conservación de la variedad Guadyerbas ha mantenido su germoplasma aisladodesde 1945 como una población cerrada en una manada experimental. El pedigrí completo con 1000 ani-males reproductores descendientes de 24 fundadores ha sido usado para medir a lo largo de cohortes sucesi-vas de animales reproductores el número efectivo de fundadores, el número efectivo de no-fundadores, elgenoma fundador equivalente y el número esperado de alelos fundadores sobrevivientes. Para la última co-horte, los valores fueron 10.34, 1.42, 1.25 y 4.06, respectivamente. También estudiamos la evolución de endo-gamia y codescendencia y sus componentes debidos a cada fundador. La tasa de incremento en endogamia ycodescendencia fue del 2.21% por cohorte, o el equivalente a 0.906 % por año. Finalmente, analizamos elefecto de la estructura familiar y las tácticas de apareamiento en la evolución de la codescendencia. Las tasasmás grandes de codescendencia por cohorte fueron atribuibles a tamaños familiares desbalanceados y al uso

mínimo de apareamientos de codescendientes, retardando efectivamente el incremento de la endogamia.

Introduction

Along with species and ecosystems, the World Conser-vation Union (1994) has designated genetic diversity as a

level of diversity requiring conservation. Livestock breedsare important components of world biodiversity be-cause of the unique genes and gene combinations theycarry as a consequence of adaptation to different envi-

*

email [email protected] submitted July 6, 1999; revised manuscript accepted March 1, 2000.

1844

Pedigree Analysis of Iberian Pig Strain Toro et al.

Conservation BiologyVolume 14, No. 6, December 2000

ronments, and several authors have put forward argu-ments in favor of breed conservation (reviews by Wool-liams et al. 1998; Oldenbroek 1999).

Several factors can result in a numerical reduction of abreed; most are associated with economic pressures, in-cluding changes in the production system. The twogreatest causes of genetic erosion are the growing trendtoward global reliance on a limited number of highlyproductive breeds that are used in intensive animal pro-duction systems, and the indiscriminate crossbreedingof local populations with improved breeds.

The Iberian pig is a racial grouping of native pigs origi-nating from


which has beenmaintained for centuries in large areas of the southwest-ern Iberian Peninsula. They constitute the largest of thesurviving populations of the Mediterranean type, whichis one of the three ancient types of domestic pigs (theothers are the European/Celtic and Asian types). Thecharacteristic habitat of the Iberian pig is the Dehesa,which are sparse Mediterranean woodlands composedmainly of evergreen oaks (

Quercus ilex

), cork oaks(

Quercus suber

), and other

Quercus

species. The eco-system has been maintained in the past for several re-sources such as firewood, cork, grass, hunting, somecultivation of cereals, and extensive livestock grazing(cattle, sheep, and Iberian pigs). The use of most ofthese resources has declined, and the persistence of theecosystem now depends mainly on extensive exploita-tion of the Iberian pig.

The morphology of the Iberian pig—dark skin andhair, pointed snout, long and strong legs—makes it re-sistent to high summer temperatures and enables it totravel far in search of food. It can endure long periods ofhunger and a poor diet from grazing because of its lowbasal metabolism and early formation of fatty tissues.The Iberian pig fattens quickly in a process known asmontanera, which occurs when it consumes acorns,grass, small roots, and bulbs of the Dehesa from Novem-ber to February. Not only is the Iberian pig unusual in itscapacity for pasturing, it is also skillful at selecting fruitand peeling off the husk.

Those who raise Iberian pigs do so to produce meatfor dry-cured products. Iberian pig meat has a high pro-portion of intramuscular fat, and the fat has a high con-tent of unsaturated fatty acid (oleic and linoleic) result-ing from high acorn intake. These characteristics producehams with extraordinary flavor. Consequently, Iberiandry-cured products are considered of the highest qualityby consumers (López-Bote 1998).

The 1960s marked the start of a long period of declinefor both Iberian pigs and Dehesa (Dohao et al. 1988).The outbreak of African swine fever, depreciation of ani-mal fats, and massive entry into Spain of more efficientbreeds selected for intensive meat production resultedin a drastic population reduction. Fortunately, the hardtimes passed once consumers began to recognize the

high quality of the Iberian products (especially hams),and a high-price market was established. This revival ofthe Iberian pig bodes well for survival of the exception-ally valuable ecosystem of Dehesa because extensiveproduction of the pig maintains the basic features of thetraditional production system.

Although the production of Iberian pigs has increased,crossbreeding with the Duroc breed is common, andthere is a strong dependence on a small number of eliteherds supplying purebred Iberian animals. Under thesecircumstances, some varieties, especially the ancestralones, are not out of danger, and a plan of genetic controlof these Iberian populations is necessary. We sought todescribe the conservation program of an ancestral strainof Iberian pig, the black hairless Guadyerbas, which ischaracterized by an extremely high body-fat content(Serra et al. 1998), and to monitor the evolution of thegenetic variability of this herd from 1945 to 1998.

Methods

The Closed Herd

An early conservation program conducted from 1944 to1945 at El Dehesón del Encinar (Oropesa, Toledo) com-bined the objective of conservation of the Iberian pigand its diffusion to farmers. The herd was formed fromfour populations that descended from populations rep-resentative of the different types of Iberian pigs in Portu-gal and Spain. Each population was isolated geneticallyuntil 1963. Then the four groups were slowly blended,resulting in a composite strain (Torbiscal) that is consid-ered the main genetic reservoir of the Iberian breed.One of the founder populations (Guadyerbas), whichoriginated from four sires and 20 dams, represented theancient earliest-maturing black hairless type. Because ofthese features, it was also maintained as a separated,closed line. Since then, full pedigrees have been recorded,and no new blood has been introduced. Although theconservation of genetic resources was considered in thegenetic strategy of the program, a moderate empiricalselection in favor of weaning weight was applied ini-tially (Béjar et al. 1993).

More strict rules of conservation in the choice andmating of breeding animals were not introduced until1982. The first rule was to maintain a balanced breedingstructure so that each sire left one son and one daughterand each dam left one daughter, giving every dam thesame probability of leaving a son. The second rule wasto impose minimum coancestry matings in which mat-ings occurred among the least-related animals and corre-sponded to the system of maximum avoidance of in-breeding (Wright 1921). The best combination can befound using linear programing techniques. If there are

S

sires and

D

dams, an

S

3

D

matrix of coancestries (

f

ij

)


Toro et al. Pedigree Analysis of Iberian Pig Strain

1845

between the

i

th sire and the

j

th dam can be set up, andthe problem is reduced to the calculation of the matrixof matings (

x

ij

) such that

is the minimum and subject to the restrictions, where

(Toro et al. 1988).The complete pedigree of the strain from 1945 to

1998 includes 248 boars and 776 sows. We considered18 cohorts of breeding animals born in successive peri-ods of 3 years (Table 1).

Founder and Nonfounder Genetic Contributions

The basic concepts in the analysis of genealogies are theinbreeding coefficient of an individual

F

x

, the probabil-ity of identity by descent of the two genes carried bythis individual at a given locus, and the coancestry (kin-ship) coefficient between two individuals

f

xy

, the proba-bility of identity by descent of two genes taken at ran-dom from each individual at the locus. These conceptsare related closely to the classical concept of geneticcontributions defined by James and MacBride (1958) asthe proportion of all distinct genealogical pathways thattravel from a given ancestor to a group of descendents.In a pedigree with a total of

M

individuals, where

N

0

arefounders (animal with unknown parents), the averagepairwise coancestry including reciprocals and self-coances-

xij fij

j 1=

D

∑i 1=

S

∑

xij 0 or xij 1, xij

i 1=

S

∑ 1, and xij

j 1=

D

∑ D S⁄= = = =

tries of a given group of

N

individuals (for example, thecurrent cohort of individuals in the pedigree) is

where

c

i

is the classical genetic contribution of the ani-mal

i

to the current cohort (Caballero & Toro 2000). Itcan be calculated for each founder

i

as

and for the nonfounders a computational algorithm canbe implemented by setting along the pedigree the con-tribution of each individual to itself equal to 1 and to anydescendent the mean of the contribuitons to its parents.Effective contribution (

d

i

) is equal to

c

i

if

i

is a founder;it is equal to

if it is a nonfounder and is corrected to avoid redundan-cies due to the coancestry among nonfounders.

From these concepts several parameters have been de-fined. The effective number of founders

is the number of equally contributing founders expectedto produce the same genetic diversity as the population

f 0.50 ci2

i 1=

N0

∑ 0.25 ci2

1FSi FDi+

2---------------------–

i N0 1+=

M

∑

0.50 di2,

i 1=

M

∑

=+=

ci 2fij,j 1=

N

∑=

12--- 1

FSi FDi+

2---------------------–

ci

Nef 1 di2

i 1=

N0

∑⁄=

Table 1. Analysis of breeding Iberian pig cohorts.

Cohort Time period (year)

S D L

σ

2sk

σ

2dk

N

3y

N

3y

/N

3yMAX

1 45/47 4 26 2.48 0.51 8.88 10.49 0.752 48/50 12 35 3.17 9.19 5.10 15.71 0.253 51/53 4 45 2.72 1.02 89.57 4.72 0.284 54/56 14 54 2.03 5.42 8.01 10.23 0.335 57/59 14 43 2.32 12.75 5.67 7.75 0.196 60/62 12 43 2.33 7.29 10.78 9.01 0.257 63/65 16 56 1.72 2.86 5.34 12.06 0.478 66/68 17 49 2.30 9.08 11.61 10.14 0.219 69/71 13 31 2.29 15.35 20.21 4.55 0.13

10 72/74 30 87 2.00 9.26 7.99 14.57 0.2311 75/77 19 55 2.68 5.91 2.80 25.38 0.3512 78/80 8 32 2.83 6.99 21.94 7.60 0.2213 81/83 12 45 2.93 4.00 8.97 20.56 0.3714 84/86 14 33 2.69 2.07 5.34 25.14 0.4815 87/89 9 16 2.97 4.38 5.48 13.34 0.3416 90/92 12 32 2.37 4.00 8.44 12.07 0.3417 93/95 21 36 2.31 5.06 1.80 21.40 0.3918 96/98 13 38 1.92 0.62 0.83 21.6 0.93

Average 13.56 42.00 2.45 5.88 12.71 13.80 0.36

*S

, number of male parents;

D

, number of female parents;

L

, generation interval;

σ

2sk

and

σ

2dk

, variances of family sizes;

N

3y

, effective size per3-year period; and

N

3y

/

N

3yMAX

, proportion of maximum effective size with balanced family structure.

1846

Pedigree Analysis of Iberian Pig Strain Toro et al.


under study (Lacy 1989; de Rochambeau et al. 1989).The effective number of nonfounders is

(effective contributions) (Caballero & Toro 2000). Thefounder genome equivalent

N

ge

5

1/2

f (Lacy 1989,1995) is the number of equally contributing founders ex-pected to produce the same genetic diversity as in thepopulation under study if no founder genes are lost bygenetic drift. The relationship between the three parame-ters is

To examine whether the alleles contributing to inbreed-ing are descended from specific founders, we can alsopartition the coancestry (or inbreeding) of a cohort intocomponents attributable to each founder. Partial coances-try (or inbreeding) coefficients refer to identity by descentof alleles descended from each specified founder. Thesum, across all founders, of the partial inbreeding coeffi-cient for an individual is equal to the overall coancestry.Partial coancesty (or inbreeding) coefficients have beencalculated through a modification of the additive matrixmethod for calculating inbreeding coefficients (Lacy etal. 1996; Lacy 1997; Rodrigañez et al. 1998).

Changes in Family Structure

The concept of effective population size (Ne) is usedmore frequently for predictive purposes than for analyz-ing realized genealogies. The classical formula for over-lapping generations is

where L is the mean generation interval in the four path-ways (sire-son [ss], sire-daughter [sd], dam-son [ds],dam-daughter [dd], sss and ssd are the variances in thenumber of males and females progenies from male par-ents, and sss,sd is the corresponding covariance (Hill1979). For female parents, the equivalent terms are s2

dd,s2

ds, and sds,dd. Although this formula is valid only whenthe number of parents is large, when the population hasconstant size and a stable age structure, when the varia-tion in family size is due to non-inherited causes, andwhen there is random mating over age groups, it can beused to illustrate the changes that have occurred in fam-ily structure over time in a conservation program.

Allele Survival

The gene-dropping method was proposed (MacCluer etal. 1986) as a simulation procedure to analyze the evolu-

Nenf 1 di2

i N0 1+=

M

∑⁄=

1 2Nge 1 2⁄ Nef 1 2Nenf.⁄+=⁄

1 Ne⁄ 2 σss2 2 S D⁄( )σss,sd S D⁄( )2σsd

2+ + +{ }16SL 2 σdd

2 2 D S⁄( )σds,dd D S⁄( )2σds2+ + +{ }+

⁄

16DL,

⁄=

tion of gene diversity in a realized pedigree. Two distinctalleles (founder genes) are assigned to every founder, andthe genotypes of all descendants along the actual pedi-gree are generated through Monte-Carlo simulation fol-lowing Mendelian segregation rules. The entire processis repeated 250,000 times, and the information from thegenotypes of different cohorts is summarized over repli-cates. The effective number of founders can be mea-sured as

where qk is the frequency of the founder gene k aver-aged over N individuals and over replicates of a given co-hort and the average pairwise coancestry

where qjk is the frequency for replicate j of the foundergene k in a given cohort. The obtained values should co-incide, within the Monte-Carlo error, with those previ-ously calculated by pedigree analysis. Unlike these param-eters, other parameters can be calculated only throughdropping genes, such as the expected number of surviv-ing alleles both from each founder (2ri) and from allfounders

Effect of the Mating System

Under random mating, inbreeding (F ) is delayed with re-spect to coancestry ( f ) for one generation, the averageinbreeding in a generation being the average coancestryof previous generations. The departure from randommating can be measured with the coefficient a, whichindicates the degree of deviation from Hardy-Weinbergproportions and is related to the previous coefficients by

The parameter (1 2 a) measures the ratio of observedto expected heterozygosity in the population. A nega-tive value of a reflects that matings between relativeshave been avoided. In the context of subdivided popula-tions, these coefficients are equivalent to the Wright(1951) statistics FIT, FST, and FIS.

Results

Changes in Family Structure

To evaluate changes in family structure during the his-tory of the strain, we considered cohorts of breeding an-imals born in successive periods of 3 years. The average

Nef 1 2 qk2

k 1=

2N0

∑

⁄ ,=

f qjk2

i 1=

2N0

∑

j 1=

n

∑ n,⁄=

2 ri.i 1=

N0

∑

1 F–( ) 1 f–( ) 1 α–( ).=


Toro et al. Pedigree Analysis of Iberian Pig Strain 1847

family sizes for the four pathways were 1.04 (sire-son),3.28 (sire-daughter), 0.33 (dam-son), 1.03 (dam-daugh-ter). The variance of sire and dam family sizes for eachcohort

and

(Table 1) indicated an unequal contribution of differentsires and dams to the stud of the breeding population,even in the last period (since 1982) when more strictconservation criteria to maximize effective size were in-troduced. The application of such criteria was subject topractical restrictions such as mortality or infertility ofsome individuals before the planned number of progenyhad been obtained. The generation intervals, defined asthe age of parents at the birth of the breeding offspringand averaged over the periods and for each of the fourpathways, were 2.25 (sire-son), 2.22 (sire-daughter), 2.60(dam-son), and 2.70 (dam-daughter).

The 3-year effective size (N3y) corresponded to thesize of an idealized population with a generation intervalof 3 years, leading to the same increase of inbreeding ob-served in the current population in the same time. Wecalculated it as N3y 5 NeL / 3, where L is the generationinterval and Ne is the value obtained using the previouslyquoted expression of Hill (1979). The mean for the stud-ied periods was 13.80, implying annual rates of inbreed-ing of 1.21%. The quotient between the 3-year effectivesize and the maximum effective size assuming a bal-anced family structure was calculated for the successivecohorts (Table 1). These values also measure the dis-tance from planned ideal conditions and ranged be-

σ( sk2 σss

22 S D⁄( )σss,sd S D⁄( )2σ2

sd+ +=

σdk2 σdd

22 D S⁄( )σdd,ds D S⁄( )2σ2

ds )+ +=

tween 0.13 and 0.93, although in the last six cohorts thevalues were more uniform.

Analysis of Contributions

We calculated the contribution of each one of thefounder and nonfounder individuals to the average pair-wise coancestry of successive cohorts (Fig. 1). The valueof f in the last cohort was 0.401, and the contributionsof founders and nonfounders were 0.048 and 0.353, re-spectively. The contributions of founders stabilize withtime, and the stabilization was complete at cohort seven.From there, the increase in coancestry must be attrib-uted to the differential contributions of nonfounders.Only 14 founders survived to leave genes in the last co-hort, and most of the losses occurred in the initial pe-riod of the program. The founder individual that mostcontributed to the last cohort (1.61%) was sow number6, and the founder that contributed least (0.00011%)was sow number 5.

Another way to summarize the information is throughthe parameters Nge, Nef , and Nenf. The first one is relateddirectly to the average coancestry and decreased overthe studied period from 9.68 to 1.25. The value of Nef inthe last cohort was 10.34, but it had a stable value sincecohort seven. The average value of the last 12 cohortswas 10.28. When stabilized it estimates half of the effec-tive population size Ne and therefore provides an esti-mate of the rate of inbreeding of DF 5 2.43%. The Nenf

decreased continuously from 60 to 1.42, reflecting theaccumulated effect of genetic drift.

The sum of the genetic contributions of all foundersand nonfounders to the last cohort was 21.35 and couldbe called the number of discrete generation equivalents

Figure 1. Evolution over the suc-cessive cohorts of the contribution to coancestry ( f) of founder and nonfounder animals of the Guadyerbas strain.

1848 Pedigree Analysis of Iberian Pig Strain Toro et al.


(Woolliams & Mantysaari 1995; Woolliams et al. 1998).An estimate of the generation interval is provided by thetotal number of years considered, divided by the num-ber of generations. A different method would be to cal-culate the reciprocal of the slope of the regression oflog2 P on year, where P is the total number of stepsalong distinct paths leading to a founder in the pedigreefor each animal. The two respective estimates of thegeneration interval were 2.53 and 2.36, close to thevalue of L 5 2.45 (Table 1).

Allele Survival

The mean number of founder genes was 31.04 (SD 1.28,range 26–34) in the first cohort and 4.06 (SD 1.06, range1–8) in the last cohort. These values correspond to64.6% and 8.5%, respectively, of alleles present amongthe 24 founders, and most of this reduction took placein the initial period of the herd. The expected numberof alleles surviving from each founder for each cohortare presented in Fig. 2. Alleles of only 14 founders wererepresented in the last cohort, and the number of allelesper founder ranged from 0.10 to 0.70. The values of al-lele survival along the successive cohorts allowed us todate this virtual extinction. Ten founder lineages wereextinct from the second to the fifth cohort, and 5, 1, 3,and 1 were the respective numbers of lost lineages.

The differences in survival probabilities of the foundergenes suggest the unequal contributions of differentfounders to inbreeding. We calculated the mean value ofthe partial inbreeding coefficients for the breeding ani-mals born in each cohort (Fig. 3). For the last cohort, thecontribuitons to the inbreeding coefficient of the four

founder sites were 3.41%, 2.18%, 3.33%, and 3.20%,whereas the contribution of the 10 surviving founderdams ranged from 6.68% (sow 6) to 0.04% (sow 5).These partial coefficients can be used to find out whetherthere is variation among founder lineages in inbreedingdepression (i.e., whether alleles contributing to inbreed-ing depression descended from specific founder lineages)(Rodrigañez et al. 1998).

Mating System

With an unequal number of males and females, the in-breeding and coancestry coefficients can be calculatedas an unweighted or weighted average of the two sexes.In our case, the two values in the last cohort wereclosed: 35.96 versus 35.91% for F and 39.95 versus40.20% for f (unweighted values for 18 cohorts in Fig.4). The value of F increased from 0 in the first cohort to35.96% in the last cohort for f 5 5.17% and 39.95%, re-spectively. The rate of advance in inbreeding andcoancestry per cohort was DF 5 2.21 and Df 5 2.21%,which corresponds to a effective population size of22.62, close to the value of 20.56 obtained from the ef-fective number of founders.

The values of a (Fig. 4) reflect the three different tac-tics used to avoid mating among relatives. Until the year1972 (cohort 9, a 5 20.0574), matings were plannedconsidering the coancestry coefficients among the breed-ing animals, although without a formal solution to theminimization of inbreeding. From 1973 to 1981 (cohort10 to 13, a 5 20.0498), the coancesty coefficients werenot available to the mating design; breeders avoided

Figure 2. Expected number of al-leles coming from each founder in each one of the cohorts of the Guadyerbas strain.



matings only between animals with common grandpar-ents. After 1982 (cohort 14 onwards, a 5 20.0764), thebest mating combination was calculated with updatedcoancestry coefficients and was solved by linear pro-graming techniques.

Discussion

In conservation of animal genetic resources, it is impor-tant to counteract the process of breed decline beforethe population becomes too small. One effective way to

do this is to develop links between a local breed or breedenvironment and products with high market value thatimprove a breed’s profitability. The Iberian pig is a goodexample of a local breed that suffered a drastic reductionin numbers and then experienced a rise associated withthe establishment of a high-price market for its products.

Despite the present favorable situation, some variet-ies, especially the ancestral ones, are not out of danger.One such variety, the Guadyerbas strain, has been theobject of a conservation program since 1944. This strainhas been traditionally rejected by farmers because of itspoor growth and extremely fat carcasses. It serves, how-

Figure 3. Mean values by cohorts of the partial components of in-breeding of the Guadyerbas strain.

Figure 4. Changes in coancestry (f ), inbreeding (F), and coeffi-cient of deviation from Hardy-Weinberg proportions (a).

1850 Pedigree Analysis of Iberian Pig Strain Toro et al.


ever, as a good example of the practical importance ofconservation activities: boars from this strain are now indemand for crossbreeding with Duroc sows to produceanimals with good growth, good carcass performance,and high-quality cured products.

The objective of genetic management is the preserva-tion of genetic variation of the population from whichfounders were drawn. Conservation schemes rely on thekey concept of population effective size (Wright 1931),defined as the size of an idealized population that wouldgive rise to the rate of inbreeding (inbreeding effectivesize) or the rate of coancestry (variance effective size)observed in the population under consideration. Exceptin cases where a population is subdivided permanentlyin independent sublines or where the population is in-creasing or decreasing, the two rates converge and thereis no need to distinguish between the two parameters.For the Guadyerbas population, the rate value was2.21% per cohort (Ne 5 22.62), or 0.906% per year.

Several simple, widely accepted rules are applied tothe conservation of genetic variation in animal species,such as equalization of sex ratio and family sizes, avoid-ance of fluctuations in population size, and prolongedgeneration interval. More recently it has become clearthat the general criterion guiding selection of animalsthat contribute gametes to the next generation is basedon minimizing the average coancestry among reproduc-tive individuals weighted by the contributions to thenext generation (reviewed by Caballero & Toro 2000;Oldenbroek 1999). If the individuals are unrelated, therule minimizes the variation in family size (Gowe et al.1959; Wang 1997), but in other circumstances it takesinto account the possibility that individuals of the paren-tal generation could be related; therefore, their contribu-tions could be redundant.

In practical schemes, the application of conservationcriteria is subject to restrictions such as mortality or in-fertility of some individuals before planned progeny areobtained. In spite of these limitations, the average of theratios of N3y/N3yMAX increased from 0.30 in 1945–1980to 0.48 in 1981–1998. The mean generation interval alsoincreased between both periods from 2.41 to 2.53. Inthe future, the combination of an in situ live and cryo-conservation scheme could be advisible to reduce ge-netic drift and allow the population to evolve and pro-vide animals to farmers.

The theory of genetic contributions ( James & MacBride1958) is useful as a tool for analyzing pedigrees. Whereasthe distribution of progeny size reflects the applicationof the rule of equalizing family sizes, the analysis of ge-netic contributions gives a more complete description ofthe evolution of genetic variability over generations. Theeffective number of founders is related to the contribu-tions of founders to a given cohort, and it is useful in theinitial stages of the program as a measure of the possiblelosses of founder lineages. After a few generations, all the

descendants will have the same contribution from a par-ticular ancestor, although it will differ among ancestors.

When this stabilization is reached in a regular system,the Nef equals half of the asymptotic effective popula-tion size. Despite the survey, generation intervals andfamily sizes of the analyzed population changed over thecohorts. The corresponding values of these parameterswere 10.28 and 22.62, respectively. The effective num-ber of nonfounders depends on the contributions ofnonfounders, and it takes the drift process into account.It therefore decreases as time proceeds, expressing theaccumulated loss of genetic variability by drift. Thefounder genome equivalents summarize both processes,and it can be shown that it is approximately related tothe effective size by Nge 5 Ne / t, t being the number ofgenerations (Lacy 1995; Caballero & Toro 2000). Thisapproximate relation holds for the asymptotic Ne (22.62)and the correspondent values in the last cohort of Nge

(1.25) and t (18). Allele survival also showed an impor-tant early decay, although it can be partially explainedby the fact that all alleles in the base population were as-sumed to be different.

The choice of mating system in a conservation pro-gram is not simple because it depends on the time scaleand on the capacity of species to cope with inbreedingdepression. In the short term, the avoidance of matingsbetween relatives will decrease the average inbreedingof the population and the associated inbreeding depres-sion and therefore is the advisable mating tactic. The ef-fects in the long term, however, can be the same or op-posite, depending on circumstances (Caballero 1994;Caballero & Toro 2000). The effectiveness of minimumcoancesty matings was manifested by the a parameter,which always showed a negative value and a mean value of20.061. The parameter a is related to G (G 5 [1 1 a]/2),the proportion of variability between individuals (1 2 Gis the proportion within individuals). With random mat-ing, G 5 1/2. Lower values indicate that variability isstored preferentially as variability within individuals. Inthe last five cohorts, over 53.82% of the variability wasestimated to be stored within individuals.

The effectiveness of the tactics of controlling familysizes and of performing minimum coancestry mating canbe evaluated approximately by carrying out a computersimulation in which the number of breeding individualsis kept as in the real scheme but the parents of each indi-vidual are taken at random among all possible candi-dates of the previous cohort. In that case, the values ofNef and the expected number of surviving alleles were7.2 and 3.21, respectively, values considerably lowerthan the actual values attained in the herd. The futuregenetic management of the Guadyerbas strain must bebased on the selection of the group of breeding animalswith lower average coancestry, although the implemen-tation of this method in a population with overlappinggenerations will require further research.



Acknowledgments

The authors acknowledge the efforts of the late M. Odri-ozola and J. Zuzuárregui, who organized and preservedthis closed herd for four decades. Financial support forthe conservation program is provided by Junta de Comu-nidades de Castilla-La Mancha and Instituto Nacional deInvestigación y Tecnología Agraria y Alimentaria grants.This work is funded by Comisión Interministerial de Ci-encia y Tecnología grant 1FD97–0772.

Literature Cited

Béjar, F., C. Rodriguez, and M. A. Toro. 1993. Estimation of genetic trendsfor weaning weight and teat number in Iberian pigs using mixedmodel methodology. Livestock Production Science 33:239–251.

Caballero, A. 1994. Developments in the prediction of effective popu-lation size. Heredity 73:657–679.

Caballero, A., and M. A. Toro. 2000. Interrelations between effective-population size and other pedigree tools for the management ofconserved populations. Genetical Research 75:331–343.

de Rochambeau, H., L. F. de La Fuente, R. Rouvier, and J. Ouhayoun.1989. Sélection sur la vitesse de croissance post-sevrage chez lelapin. Genetics, Selection, Evolution 21:527–546.

Dohao, M. T., J. Rodrigañez, L. Silió, and M. A. Toro. 1988. Iberian pigproduction in Spain. Pig News and Information 9:277–282.

Gowe, R. S., A. Robertson, and B. D. H. Latter. 1959. Environment andpoultry breeding problems. 5. The design of poultry controlstrains. Poultry Science 38:462–471.

Hill, W. G. 1979. A note on effective size with overlapping genera-tions. Genetics 92:317–322.

James, J. W., and G. MacBride. 1958. The spread of genes by naturaland artificial selection in a closed poultry flock. Journal of Genetics56:55–62.

Lacy, R. C. 1989. Analysis of founder representation in pedigrees: founderequivalents and founder genome equivalents. Zoo Biology 8:111–124.

Lacy, R. C. 1995. Clarification of genetic terms and their use in themanagement of captive populations. Zoo Biology 14:565–578.

Lacy, R. C. 1997. Errata. Evolution 51:1025.Lacy, R. C., G. Alaks, and A. Walsh. 1996. Hierarchical analysis of in-

breeding depression in Peromyscus popionotus. Evolution 50:2187–2200.

López-Bote, C. 1998. Sustained utilization of Iberian pig breed. MeatScience 49:(supplement 1):S17–S27.

MacCluer, J. W., J. L. Van der Berg, B. Read, and O. A. Ryder. 1986.Pedigree analysis by computer simulation. Zoo Biology 5:147–160.

Oldenbroek, J. K. 1999. Genebanks and the conservation of farm ani-mal genetic resources. DLO Institute for Animal Sciences andHealth, Lelystad, The Netherlands.

Rodrigañez, J., M. A. Toro, C. Rodriguez, and L. Silió. 1998. Effect offounder allele survival and inbreeding depression on litter size in aclosed line of large white pigs. Animal Science 67:573–582.

Serra, X., F. Gil, M. Pérez-Enciso, M. A. Oliver, J. M. Vázquez, M.Gispert, Y. Díaz, F. Moreno, R. Latorre, and J. L. Noguera. 1998. Acomparison of carcass, meat quality and histochemical characteris-tics of Iberian (Guadyerbas line) and Landrace pigs. Livestock Pro-duction Science 56:215–223.

Toro, M. A., B. Nieto, and C. Salgado. 1988. A note on minimisation ofinbreeding in small scale breeding experiments. Livestock Produc-tion Science 20:317–323.

Wang, J. 1997. More efficient breeding systems for controlling inbreed-ing and effective size in animal populations. Heredity 79:591–599.

Woolliams, J. A., and E. A. Mantysaari. 1995. Genetic contributions of Finn-ish Aysrhire bulls over four generations. Animal Science 61:177–187.

Woolliams, J. A., D. P. Gwaze, T. H. E. Meuwissen, D. Planchenault, J. P.Reanard, M. Thibier, and H. Wagner. 1998. Secondary guidelines fordevelopment of national farm animal genetic resources managementplans: management of small populations at risk. Initiative for domesticanimal diversity (IDAD). Food and Agriculture Organization, Rome.

World Conservation Union (IUCN). 1994. IUCN red list of threatenedanimals. Gland, Switzerland.

Wright, S. 1921. Systems of mating. Genetics 6:111–178.Wright, S. 1931. Evolution in Mendelian populations. Genetics 16:97–159.Wright, S. 1951. The genetical structure of populations. Annals of Eu-

genics 15:323–354.

genealogical analysis of a closed herd of black hairless iberian pigs

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