GENETIC VARIATION AND INTER-TRAIT CORRELATIONS IN EUCALYPTUS GLOBULUS BASE POPULATION TRIALS I S ARGENTINA

Gustavo A. Lopez I.', Bradley hl. Polts I , Gregorl 11'. Dutkowski I , Luis A. Apiolaza ' Sr Pedro E. Gelid2.'

I ' Cooperative Research Ccntl-c for Sustainable PI-oduction Forestry and School of Plant Science. Uni\trsit! of Tasmmia. GPO Box 252-55. Hobart. 7001. Tasmania, Australia.

'' Permanent address: Institute Nac~onal dc Tecnologicl Agropccuaria (INTA) CIRN. Los Rcscros 5 Las Cubalias sin. 171 2, Ca5telar (B.A.). Argentina.

" Proyecto Forestal dc Desarrollo. (SAGPyA-HIRF). c/o Los Rescros y Las CabaRas sin, 1712. Cn<tcla~- (13.A.) Arpcntina. Corrcspondinp author: 13radlcy b1. Potts. Cooperative Rcscarcli Centre for Sustainable Production Foresty? and Scliool of

Plant Scicncc, U~liversity of Taslnania, GPO Box 252-55. Hobart. 7001. Twnania. ,\ustral~:i. E-llnil: H.h4.PottsO'utas.cdt1.:111

Gcnctic \ariation and intcr-trait correlations nerc es;irnincd in 3 base population of E~lc,ir!\.l)iilr g / o / ~ i l / i i t

e~tablishcd on b u r sites in At-sy~tin:~. The gtnctic matcrial included 323 opcn pollinatcd seed lots I'rorn I 1 Aust~aliaii localities and 52 opcn pollinated and contl-ol pollinated seed lots from EUI-opcan m d South American land races. Survival, p n t l i , hark rhickncss, tree lorni, transition ro adult foliage arid Pilodyn pcneirntion net-c assessed. at diffcfcrcnt ages up to 4-years. Awl-age s~nplc site individual narrow-sene lieritahilit~c \\.ere low lor forking (0.03), survi\.al10.05) and form (0.10): intcrmcdiaie Ibr growth (0.27) and rclativc bark t l~ick~icss (0 .33) : and liipli for Pilodyn penctratlon (0.18) and transition to adult foliage (0.60). There \\as strong positiw genetic correlation between the s:imc trait ~neasurcd at diffcrcnt sites (> 0.70) and ages (> 0.61). In general, the genetic correlations between growth and other traits were not stat~sticnlly signilicanl Pilodyn penetration -0.01. fork 0.06. proportion ofadult I'oliage0.05, bark thickness-0.02). Corrclntiorls aniongst subrace effects \\crc generally consistent w i h the family ~vithin subrace genctic correlations. hut to wme extent Ion'cr and less sign~i'icant. Other estimates of gcnctic par:ime(ers rt:portcd fbl- FI, g/ohii/ir.s wcrc get~erally consistcr~t with the prescnr srutly. The liniiiations on parameter es~imatcs from open poll~natcd progeny trials are discussed.

interaction. tree brccdin~.

INTRODUCTION

Elc~nl!,ptirs g/ohit/ir.\ is a forest tree native to south- eastern Australia and variously given specific (Bi<oot i - EI< 2000) o r sub-specific status (E. g1ohulu.s SSP.

globiilr~s; KIRKI?ATRICK 1975). It is the premier pulp- wood Elrcril>pt~r.s species and is grown in plantations in many temperate countries around the wor ld (ELIIIIIIIGE er (11. 1993). It is in various stages of domestication in many countries such as Australia (TIBB~TS et 01. 1997) . Chi le (SAYI-~UEZA & GRIFFIN 2001 : GUTIERREZ et (11. 2001) , Ch ina (ZANG et ril. 1995). Portugal ( A K A ~ ~ J O et al. 1997) , Spain (SOIIIA & BORRALHO 1998) and Uruguay ( B A L ~ I E L L I et rd. 2001) . Genet ic parameters are required to opti lnise breeding and deployment strategies. as well as e s t i m a k breeding values and gains f rom selection (WHITE 1996: BOIIRALHO 2001 ). T o d c t c r n i n e the response to selection. it is important to know h o w much o f the phenotypic variation in a given

trait is under gcnclic control (heritability). It is also important to understand the extent to u ,h ich the espl-cs- sion of the gcnctic vx ia t iou is stable across different agcs iagc to age genetic corrclations) and diffcrcnt sites (;IS an indication o f genotype x cn1.i:-onmcnt intcrac- t ion), as well as the gcnctic correlations exist ing amongst different traits to predict the response to selection in a multivariate sense (F..ILCONER Kr MACK- AY 1996).

Mos t studies of genetic parameters in E. glohllllrs have focused o n growth (e.g. PUTTS & J O I ~ I I A N 199413; BOIIRALHO et nl. 1995; H o n c ; ~ et (11. 1996; BALMELLI er (11. 2001) and its association with a f e w key traits such as survival (CH.?MUERS ct (11. 19%). \ ~ o o d density (BOIIKALHO et I / / . 1992b; M.-\cDoN,AL~I ef r i l . 1997; MUNERI & RAYMOND 2000) , f lowering precocity (CHAMBERS ci 01. 1997). form (VOLKER pi (11. 1990) and vegetative phase change (IPIKz.-\ et 01. 1994: J O R I ) A K cr (11. 2000). Thcsc studies difl'c:. in anal)t ical

G. A. LOPEZ ETAI..: GENETIC VARIATION IN ECCALYPTL~S G1,OBLZU.S

technique. statistical moc!el, genetic material studied andlor test e~~\, ironment.

The present study reports the genetic parameters I'or the first pedigreed E. glohul~cs trials grown i n Argeti- tina. These trials combine both native stand seed lots I'rom Australia and land race material from around the ~vorld to construct a large base population for breeding this specics in Argentina (LOPEZ et trl. 2001 b). We examined the Icvcl of genetic control and genetic correlations for eight traits covering growth. wood density, for~n, bark thickness and vegetati\;c phase chnngc. The expression of gcnctic variation in thew traits is examined across four sites, as well as the changc v, ith age up to 4-yeas.

RIATGRIIALS AND RIETHODS

Plant n~aterial and trials

The four sites studied are lacakd in the Buenos Aires Province. Argentina, within the traditional E. g1obdrf.s planting ;/.one (defined in LOPEZ etul. 200 1 c). The trials arc identified as B A I L (lat. 37"45' S long. 58" 17' W). BOSG (lat 38" 39' S long. 59" 04' W), hlANU (Iat. 37" 53' S IClng. 59" 56' W? and VOCA (lat. 38" 28' S long. 59" 06' W) arid vary in average annual rainfall from 850 to 1008 mm and average annual minimum tempera- ture from -5.8" to -3.3 "C (scc LOPEZ et til. 2001b). The trials included a total of 14.925 trees from 276 seed lots. Two hundred and twenty three open pollinated (OP) families and one bulk collection were from 11 native stand localities in A~strillia and 52 seed lots w c ~ from land races from Portugal. Spain. Chile and Argen- tina. The land race seed lots includcd 37 OP families and 10 control pollinatcd (CP) families, as well as 5 bulk collections of varying levels of genetic improve- ment. 'The number of families (i.e. seed lots) per trial ranged from 220 to 275. Full details of the distribution of families across collection localities are given in LOPEZ et ill. (200 I b).

Tlic trials comprised I5 replicates per family of single-tree-plots. Families were arranged in sets of 20 to 25, based on their geographic provenance. Sets w c r ~ randomly allocated to a position in thc trial and families within each set were randomly arranged in each repli- catc of the set. Spacing was 3 m x 3 m in all trials.

Measurements

Measurements were made of growth, adult foliage. Pilodyn penetration, bark thickness. form and survival. Stern diameter (cm) over bark was assessed at breast

height (1.3 ~ n ) at 2 (DBH2), 3 (DBH3) and 4 (DBH4) years after planting. Total height (cm) was measured at 1 (HTI ) and 2 (HT2) years. The proportion of adult foliage was assessed at age 2 (ADFO). while tree form (FORM: 1 worst - 4 best) was assessed at age 3 (MANU and VOCA) or 4 (BALC and BOSC). These last two variables were mcas~~red on an ordcred 4-point scale (details in LOPEZ rt 01. 2001h). Bark thickness (BTHI) and Pilodyn penetration (PILO) wcrc mcasurcd ( ~ n ~ n ) only in BALC and BOSC at age 4. The variable BARK used for analysis is the percentage of DBH1 that was effectively bark for each indi\,idual tree. The presence of forks at age 2 (FORK) was assessed in the same 2 trials approxi~natcly 2 months after light hail damage. Survivai (SURV) was determined baaed o n thc oldest assessment for each trial (i.c. age 1 for BALC and BOSC and age 3 for MANU and VOCA).

The general set of' data used for analysis was from all those trees that were alive at measurement; houc \w . isolated outliers (usually runts) were rejcctcd. At MANU approximately 25 % of trees sufl'cred damage by cows at an early age and were excluded froni thc analysis.

Analyses

For each trial, an inco~nplctc block design was imposed rr posteriori (see EKICSSON 1997: Fu et c d . 1999). Thc incomplctc block size used I'or cach trial was that which maxilniscd the model likelihood for the oldest diamc~cr measurement (DUTKOLVSKI rt t i / . 2 0 0 2 ) . Vxiancc components for each trait were ~ < i ~ ~ ~ l a t c d with an individual tree mixed ~nodcl. uung rcstricrd maximum likelihood implemented with ASRe1n1 ( G I L ~ I O U I I et (11.

2001'). The model fitted was:

where: y is the vector of indi\,idual tree data: b is the vector fur all the fixed effects (overall mean, subrace as d-l'incd by the classification of DLTKOWSKI 8r POTTS (1999) or lalid race (~APEZ et al. 2001 b). and pollina- tion type -open pollinated or control pollinated): a is the vcctor of unobservable additive gcnctic effects of individual trees; c is the vector for the random cfl'ccts of the incomplete blocks and e i.; the vector ol'rcsidu- als. X. %, and Z,. are incidence matrices relating the observations to the fixed and random effects in the model. Model 1 was fitted for both univariatc and hivariate analyses and in both cases, the expected mean and variances of the parameters are:

tions wcre significantly differcnt from zero or not was determined with a likelihood ratio test.

whcrc V = Z , G,, Z ' , + Z, G, Z', + R , G, = A B Go whcrc A is the numerator rclationship matrix, G, is the additive genetic covariance matrix, and o is the Kronecker product, Gc= I e G,,, where I is an idcntity matrix, Gc, is the incomplete block covariance matrix and R= R, 8 I where R, is the trait residual covariance matrix. For the univarialc case, some of these rnatrices

1 7 (e.g. G,,. R,) collapsc to scalars (e.g. 0;;. 0 ; ) . Thc additivc rclationship matrix A was modificd to account for an assumcd 30%' selfing ratc, which increases the sib additivc coefficient of relatedncss (r) from 0.25 to 0 . 3 and the parent-offspring relatedncss from 0.25 to 0 . 3 as well (DUTKOWSKI et al . 2001). Thc few bulk sced samples werc included in the rclationship matrix ~v i th missing male and femalc pedigree information. A binomial model was fittcd to presencelabsence traits (SURV, FORK) with a probit transformation. The significance of random effccts was tested using a likelihood ratio tcsl (SEARLE 1971).

To compare the absolute levels of additive genetic variation across traits, the cocfficients of additive genetic variance wcre calculated as:

whcrc: o(i is the within subracc additivc gcnctic stan- dard deviation calculated from the univariatemodel and ,? is the population mcan ( a f e r HOULE 1992). Single site. narrow-sensc hcsitabilities (I?) were calculated as:

- ~ b '

0

0

0

Z:\G., 'cGc

0 0 G,Z,i G.\

GcZc 0 G , 0

R 0 0 R

a

c

e

wherc: o: is !lie additive genetic variance within subraccs and 0; is the error variance component i n 121. The error term includes the specific combining effcct from the few controlled crossed families. The standard errors of estimates werc calculated by ASReml from the avcrage information matrix. using a standard truncated Taylor series approximation (GILMOUR et (rl. 2001). Genctic differences between subraccs wcrc tcstcd with thc F-statistics using an error degree offreedom dcrivcd from the family within subraces term. Subracc least squarc means and their standard crrors werc also csti~natcd in ASReml. Pearson's corrclation coefficients amongst these subraces lcast squarc incans wcre cstirnatcd using the PROC CORR proccdurc in SAS

(version 8). Pairwise gsnetic con-clations and their standard

crrors were cstimatcd using a bivariate model that was extcnded from the univilristc niodcl \Vlicthcr correla-

iv

RESULTS AND DISCUSSION

Expression of genetic effects

The genetic variation was partitioncd into I'ixcd subsacc effects and random additive genetic variation within subracc. The estimates presented in this study arc dominated by open pollinated native stand families (82 %) but also integrated information from opcn pol l i~l i l t~d (14%) and control pollinated (4%) land race families. All traits shoucd significant subrace differentiation, exccpt survival at MANU (Table 1). The patterns of differentiation at the subrace level are discussed by LOPEZ et (11. (2001 b). therefore this paper focuses on the genetic variation ol'i'amilies within subraccs.

Statistically significant levels of additive genctic variation within subraces wcrc dctcctcd for all traits except surviml, where significant variation n x s only dctcctcd at VOCA (Tablc I). However the magnituclc of the additive variance was scale dependent and in the casc of growth. incrcascd with LIE mcasurclncnt mean. The ability of traits to respond to selection can be compared by thc coefficient of additive genetic \miance (CV,,) that rncasures levels of additivc genetic variation while accounting for scale and size effects (HOULE 1992). The CV, was close to 10% for most traits. except for the proportion of adult I'oliagc, n,hich was greater than 40% at all sites (Table I). In a re\ iew of the magnitude of the cocl'l'icicnt of additivc: genetic \,ariation across a largc number of quant i ta t i~e traits in a variety of forcst tree species. CORNELIUS (19931 reported median values for height ant1 dia~ncter growth of 9%, consistent with the average obtained in the present study.

The magnitude of the genotype x environment interaction on trait cxprcssion can be gaugcd by the gcnctic correlation between the same trait mcasurcd at differcnt sitcs. Such correlations could be partitioned into the corrclation of subrace effccts (r,) and thc correlation of additive genetic ef'ects within subraces (r,). The subracc correlations across sitcs were strong add positive for most traits (Tahle 3), indicating stabil- ity of subraccs performance for the traits observed. Genctic correlations within subraces bvcre also high (Table 3). and in general slightly higher than the subrace correlations.

0 A I I R O I I A P U B L I S H E R S

G. A. LOPEZ ETAL.: GENETIC VARIATION IN EUCALYPTUS GLOBULUS

Table 1. The overall means with standard deviation (sd), additive genetic variance (x) with their significance (Sig.) and coefficient of additive genetic variation (CV,in 70 units), within subrace heritabilities (h') with their standard errors (s.e.) and the F values and significance of the subrace effects (F) for the 34 variables measured across the four trials. Significance of effects are noted as ns = not significant; * P < 0.05; ** P < 0.01 and *** P < 0.001; NT = could not be tested. "n" represents the number of data for each trait included in the analysis. The traits HT (height, cm), DBH (diameter a t breast height, cm), PILO (pilodyn penetration, mm), BARK (bark thickness, %), FORM (stem form), ADFO (adult foliage, proportion), FORK (presence of fork, binary) and SURV (survival, binary) are followed by a number which represents the age of measurement in years. Note that n in DBH3 at BALC and BOSC are smaller that DBH4 due to exclusion of data at age 3.

Trait

HT 1

HT2

DBH2

DBH3

DB H4

PILO

BARK

FORM

ADFO

FORK

SURV3

SURV4

Site

B ALC BOSC

BALC BOSC VOCA MANU

BALC BOSC VOCA MANU

BALC BOSC VOCA MANU

B ALC BOSC

BALC BOSC

BALC BOSC

BALC BOSC VOCA MANU

B ALC BOSC VOCA MANU

BALC BOSC

VOCA h'lANU

BALC BOSC

Mean Additive genetic Heritability Subrace effect

-

Sig.

*** * **

*** *** *** * :b *

*** *** *** ***

*** *** *** *:**

* *

*** * % *

*** X i *

* x *

*** *** ****

*** *** *** ***

*** ***

* ns

*** 1

Table 2. Individual narrow-sense heritability estimates (h2) for growth traits of Eucalyptus globrtlus open pollinated families from single sites or the sites average when multiple sites are reported. The coefficient of relationships (r) used in the estimation are given and the heritabilities have been standardised to a common basis of r = 0.4 (1z2,,,,) for comparison. b'here r is not given these are treated as r = 0.4. The traits dbh (diameter a t breast height), ht (height) and vol (volume) are followed by a number which represents the age of measurement in years. The group effect represents the inclusion (Yes) or not (No) in the statistical model of a fix effect to account for the provenance, subrace, race or other group effect. Number of families (No. of families) and number of sites (No. of sites) tested, and type of population (Pop. type) refers to whether land race (L) or dominantly Australian native stand (N) families have been tested.

Trait

dbh ? dbh2 dbh3 dbh3 dbh4 dbh4 dbh4 dbh4 dbh4 dbh4 dbh5 dbh5 dbh5 dbh6

Group KO. of effect families

K o 560 Yes 224 Yes 224 No 89 No 20 Ycs 224 No 589 Yes 594 Yes 569 Yes 474 Ycs 260 No 89 Yes 70 Ycs 45

Pop. type

L & N N N h' N N N N iY N N L N K

No. of sites

Country Source of reference and year

Portugal Chile Chile Uruguay Australia, VIC Chile Australia Australia, TAS Australia, TAS Australia, TAS Spain Uruguay Australia Australia, TAS

ARAUJO et 01. ( 1997) IPINZA et (11. ( 1 994) IPINZA et (11. (1 994) BALMELLI et a / . (200 1 ) WOOLASTON e f nl. (1 99 1) I I Y N Z A ~ ~ (11. (1994) BORRALHO or a/. ( 1 995) BORRALHO & POTTS ( 1996) M~cDox.ln1.11 et r i l . (1997) DUTKOWSKI ei nl. ( 1997) S o l w et a/. ( 1997) BALMELLI et a/ . (2001) MUNERI &RAYMOND (2001) VOLKEII ei nl. (1 990)

ht ? llt I IlL2 ht2 ht2 ht3 ht3 ht4 ht4 h t4 ht5 ht5 ht6 ht6 ht8 ht9

No h'o No Yes No Yes No Yes Ycs No Yes No Yes Ko No No

Portugal Portugal Australia. VIC Chilc Portugal Chile Uruguay Chilc Australia, TAS Portugal Spain Uruguay Australia, TAS Portugal Portugal Portugal

ARALUO ct a/ . ( 1997) BOIIRALHO et (11. (1 992) WOOLASTON et (11. (1 99 1 ) IPINZA er nl. ( I 994) BORRAI~HO et t i l . ( 1 992) IPlNZ/\ et a/ . ( 1 994) BAI.MELLI et cil. (200 1 ) IPINZA et tit. i 1994) ROI<RAl,HO ei (11. (1 996) BORRALHO c f trl. ( 1 992) SORIA et t i l . ( 1997) BALMLILI et trl. (2001 ) VOLKER ct 01. ( 1990) BOIII<ALHO et 01. ( 1992) BORIIALHO et i l l . ( 1 992) BORRALHO et ul. ( 1 992)

vol? vo12 vo12 vo13 vol4 vo14 vo14 vo15 vo16 yo19

No Yes Yes No

Yes Yes -

No Yes

Portugal Australia Australia Uruguay Chilc Australia, TAS Chile Lrruguay Australia. TAS Portugal

-

ARAIIJO e f ril. (1997) Honcrr ei (11. ( 1 996) HODGE et (11. (1 996) BAL~IELLI et ell. (2001) IPINZA el (11. ( 1 994) POTTS & JORDAN ( I 994) V E R G . . ~ , ~ & GRIITIN ( 1 997) RAI,~~[ ;LI . I et nl. (2001) V01,Kr;n el nl. (1 990) COTTI:IIIIL & RIIOLIN ( I 997)

"' Heritabilities estimated by the authors for Australian native stand families have not been included In the averasc presented here as these were highly inflatcd due to inclusion of large provenance effects in the difference between families.

0 A K B O R A P U B L I S H E R S

G. A. LOPEZ ETAL.: GENETIC VARIATION IN EUCALYPTC~ GLOBULUS

Table 3. Across site correlations between subrace least square means and their significance from zero. The significances are noted as ns = not significant; * P < 0.05; ** P < 0.01 and *** P < 0.001. The traits HT (height, cm), DBH (diameter at breast height, cm), PILO (pilodyn penetration, mm), BARK (bark thickness, proportion), FORM (stem form), ADFO (adult foliage proportion), FORK (presence of fork, binary) and SURV (survival, binary) are followed by a number which represents the age of measurement in years.

Trait Site BOSC VOCA

HT 1

HT2

DBH2

DBH3

DBH4

ADFO

FORM

PILO

BARK

FORK

B ALC

BALC BOSC VOCA

BALC BOSC

VOCA

BALC BOSC VOCA

B ALC

BALC BOSC VOCA

BALC BOSC VOC A

BALC

BALC

BALC

High intra-population genetic correlations (5) are often associated with high inter-population (c.g. y,) genetic correlations (ZENG 1987) as in the prcsent case. However, this is not always the case in E. g[obulus (POTTS & JORDAN 1994a; JORDAN et 01. 2000) and to some extent the patterns of subrace correlation will depend upon the pattern of subrace sampling. In contrast, the genetic correlations within subraces are likely to be more stable and reflect pleiotropy. The pooled estimates across different subraces would argue against an effect of linkage. In the present case, mea- surements of the same trait at different sites were genetically correlated at a level usually greater than 0.7 (Table 4) and, at least for most growth measurements, this was also the case at the subrace levcl. These results would argue that the same genes are being expressed at the different sites and that from a breeding perspective a single breeding population would bc suitable for the range of sites tested.

Growth

Fast growth is one of the major objectives of eucalypt breeding programs around the world (GREAVES et nl. 1997; BORRALHO 2001). Growth was under moderate genetic control in our trials. In general, single site heritability estimates for growth traits ranged from0.09 to 0.36 (Table 1). The average heritability of four single trial estimates for diameter across ages was 0.25. Estimates from MANU were atypically low (0.09 to 0.12), but this poor expression of genetic variation for growth within subraces at this site was not reflected in the expression of subrace differences. Heritabilities for height ranged from 0.11 to 0.36.

A comparison with heritability estimates reported in the literature is complicated by the differences in envi- ronment: methodology of analysis (e.g. whether group effects are excluded or not), age of evaiuation and the coefficient of relatedness (r) used. Table 2 lists thc heritability for growth traits reported in other OP

G. A. LOPEZ ETAL.: GEKETIC VARIATION IN EUCALYPTUS GLORULUS

Table 5. Subrace least square mean correlations between the different traits within sites. The significances are noted as ns = not significant; * P < 0.05; ** P < 0.01 and *** P < 0.001. The traits HT (height, cm), DBH (diameter at breast height, cm), PILO (pilodyn penetration, mm), BARK (bark thickness, proportion), FORM (stem form), ADFO (adult foliage, %), FORK (presence of fork, binary) and SURV (survival, binary) are followed hy a number which represents the age of measurement in years.

Site Trait

BALC HTI HT2 DBH2 DBH3 DB H4 PlLO BARK FORM ADFO

BOSC HTI HT2 DBH2 DBH3 DBH4 PILO BARK FORM ADFO

VOCA HT2 DBH2 DBH3 FORM SURV3

MANU HT2 DBH2 DBH3 FORM

HT2 DBH2 DBH3 DBH4 PILO BARK FORM ADFO

0.29 ns 0.20 ns

-0. I9 ns -0.24 ns -0.22 ns 0.00 ns

-0.26 ns 0.21 ns

at BALC, 0.33 and 0.35 and BOSC, 0.35 and 0.36, respective1 y).

There were very strong age-age correlations in the expression of genetic variation both within (r , ; Table

6) and between subraces (r,; Table 5). As would be expected, the magnitude of this genetic correlation declined with increasing age interval. However, even at the greatest interval, the correlations were still highly significant and the genetic correlations (r,?) between 1 year height and the 4 year diameter were greater than 0.6. While subrace effects were less strongly correlated across ages than the genetic effects within subraces, in most cases these correlations were high and statistically significant. While these trials are still relatively young, a strong genetic correlation (r, >0.7) between height at age 2 years and later age sectional area measurements (8-18 years) has been reported by BORRALHO et al. (1992a) for E. globulus. Sectional area estimates at age 4 years were also highly correlated (r, > 0.95) with later

FORK

0.18 ns -0.34 ns -0.13 ns

0.00 ns -0.02 ns

0.20 ns -0.05 ns -0.31 ns

0.26 ns

0.54 11s 0.49 ns 0.57 ns 0.33 ns

age measurements taken close to rotation age of be- tween 8 and 18 years. These results argue that selection for later age growth could occur as early as 2 years, but BORRALHO et al. (1992a) argue that the optimal age for selection is four years or, if expressed in terms or average tree size, 8m of height.

Despite the environmental differences between trials (LOPEZ et al. 2001b), growth was strongly corre- lated across sites for all pair-wise comparisons (r, > 0.78). Growth on the different sites can thus be consid- ered the same trait because family performance was stable and the genotype by environment interaction was very small (BURDON 1977). Comparable within race genetic correlations across sites were reported by MACDONALD et al. (1 997) for 4 year-old diameter of E. globidus across five sites in Tasmania (averaged 0.80 cf 0.91 for comparable ages in the present study). In another Australian study, MUNERI & RAYMOND (2000) reported similar genetic correlation between two sites

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0 A R B O R A P U B L I S H E R S

reported higher hcritability (0.22 + 0.07) for form from a trial assessed at age 8. Howevcr in both studies, tlic heritability of tree form was lower than estimates for growth. Despite tlic low heritability for forking and form, the gcnctic expression of these traits was highly correlated across sites, at lcast within subraces (Tublc 4; form 0.70; forking 0.77).

Vegetative phase change

In hcteroblastic species such as E ~ ~ c a l j , p t ~ ~ s glob~dus. thc timing of transition from juvenile to adult foliagc type is important as thc lcaf typcs differ in numerous physiological and anatomic characteristics. In the casc of E. g l o b ~ ~ l ~ ~ s , many pcsts are adapted to one or an- other type of foliage (e.g. LAWRENCE et al. 2002; STEINBAUER 2001), and variation in thc timing of thc transition may affcct performance (JORDAN etal. 2000). The proportio~i of adult foliagc was the most heritable of all traits in the present study, averaging 0.60. High hcritability estimates for this ontogenetic trait were similarly rcportcd in a base population trial of E. glob~tlrrs in Tasmania (height to phase change h' = 0.67 + 0.13; JOIWAN et 01. 1999) and for other eucalypt spccics (WILTSHIRE et (11. 1998). Despite the lowcr hcritability reportcd by IPINZA et al. (1994; height to phase change I? = 0.30), thc timing of thc transition to adult foliagc seems clearly to be undcr strong genctic control in eucalypts. In addition, the relative timing of this transition appcars to be cxtrcmcly stablc across envirorimcnts. The vcry high gcnctic correlations between (0.92) and within (0.99) subraces for the proportion of adult foliage in the canopy, implies there is no environment interaction affecting the cxprcssion of this ontogenctic trait jscc also JORDAN et nl. 2000).

Inter-trait correlations

The genetic corrclation between two traits will deter- mine how selection operating on one trait will affect genetic variation in another (i.e. correlated sclcction - FALCONER & MACKAY 1996). A positive genetic change in onc trait could affect other traits in the populatio~i In an adverse or favourable manner depend- ing upon the strength and dircction of thcir gcnctic correlations.

Within races, gcnctic variation in growth was cffcctivcly independent of genetic variation in the proportion of adult foliage in the canopy, the level of forking, Pilodyn penetration and relative bark thickness (Table 6). The only exceptions involved specific growth correlations with vegetative phase change. Therc was a low, but significant positive correlation of

early growth with the proportion of adult foliage at two sitcs. This is indicative of the general trend observed at the environmcntal and gcnctic I c x l by JORDAN et a/ . (2000) for fast growth to result in morc rapid transition to adult foliage. This trend was also evident in the gcnetic correlation with four-year diameter reported by IPINZA et a/ . (1994). but not for their carlier a, oe mea- surements. Thcrc was no significant association be- tween growth and thc transition to adult foliagc at thc subrace level in the present study, although such a corrclation was reported for a disease damaged site in Tasmania where early phase change resultcd in better growth (JORDAN et a/ . 2000).

Survival was genetically correlated with growth traits at VOCA (Tablc 5). VOCA was tlic only trial whcrc there was a significant genetic basis to variation in survival within subraccs (Tablc 1) and, as with growth, survival was also corrclatcd with thcproportion of adult foliage. but not with form. The corrclation estimates between survival and growth were within thc top range of those rcported previously ( C H A ~ I B E K S et 01. 1996) and indicate mortality was size dcpendcnt due to the dcath of genetically slower growing plants. However, these significant gcnctic correlations (r,) \vcrc not evident at the subrace level ( I - , ; Table 5).

There was a gcncral tcndcncy Ibr good form to be gcnctically correlated with fast growth at all sitcs (Table 6). This association was not detcctcd at the suhrace level (Table 5) but a similar trend was also rcportcd by VOLKER et 01. (1990) in E. g lob~r l~ ls where good tree form was wcakly genetically associatcd with fast growth ( r , for hcight 0.43, diameter 0.07 and volume 0.13). Regardless of whether this trend is a scoring artifact or a true biological tendency, thc genetic corrclation is clearly in a dircction favourable for breeders.

There was a tendency for trees with gencs for thicker bark to also have denser wood. The correlation between the relative bark thickness and Pilodyn pcne- tration was highly significant at both sitcs assessed (r,s = -0.46 to -0.42; Tablc 6). This trcnd was also evident at the subrace level (Tablc 5) and has also bcen ob- served in trials in Tasmania (DUTKOWSKI & POTTS 1999), wherc it was suggested to be a pleiotropic relationship rc1'1ccting from the joint origin of wood and bark in the cambium.

A knowledge of the genetic relationship betwccn growth and wood density is important for breeding programs. An adverse correlation, as obscrvcd in some P i t i ~ ~ s spccies (c.g. BuIIDON & LO\\.' 19921, can mark- edly retard progrcss in sclcction toward a fast growing. high density ideotype required to optimisc pulp yield per hcctare. Within sitcs in thc present study, Pilodyn pcnctration was genetically independent of diametcr

0 A R R O I I A P U B L I S H E R S

G. A. LOPEZ ETAL.: GENETIC VARIATION IN EUCALYPTUS CLOBULUS

within subraces (average r, - 0.00; Table 6) and slightly positive when across site correlations are also consid- ered (average r, - 0.09; LOPEZ et a/ . 2001a). Other studies reported positive genetic correlations between growth and Pilodyn penetration (0.04, 0.18 and 0.85 MUNERI & RAYMOND 2000; average of 5 sites 0.26 MACDONALD et al. 1997; 0.19 VOLKER unpubl. data) and slightly negative associations between growth and basic density (MUNERI & RAYMOND 2000), but rarely were these correlations significantly different from zero. At the subrace level, there was a tendency for faster growth to be associated with lower Pilodyn penetration (i.e. denser wood) in the present study (Table 5). At the race level this association was highly variable across sites in the study of MACDONALD et al. (1997), but the combined correlation was also slightly negative (-0.19). Regardless, the very low correlations between growth and Pilodyn penetration within the total population in Argentina when both genetic and sub-race effects are combined suggest that the traits can be improved independently (LOPEZ et al. 2001a).

Limitation of parameter estimates

As most eucalypt species are only in the early stages of domestication, the majority of the genetic parameters reported to date are derived from open pollinated progeny trials (ELDRIDGE et al. 1993; POTTS &WILT- SHIRE 1997) and E. globulw is no exception (Table 2). However, the accuracy of these parameter estimates has been questioned, particularly for growth (GRIFFIN & COTTERILL 1988; POTTS et al. 1995). Eucalypts have a mixed mating system (HARDNER & POTTS 1995; POTTS & WILTSHIRE 1997) and inbreeding depression for growth after selfing is severe (HARDNER &POTTS 1995; HARDNER et al. 1996; LOPEZ et al. 2000). Bi-parental inbreeding may also be significant in wild populations (HARDNER et al. 1998; SKABO et al. 1998). Variation in the levels of outcrossing in the open pollinated progeny may thus impact considerably on their growth perfor- mance (HARDNER & POTTS 1995; BORRALHO & POTTS 1996; BURGESS et al. 1996). Hence, heritability for growth estimated fromopen pollinated progenies can be inflated and not reflect the true additive genetic varia- tion amongst parents where the expression of inbreed- ing depression is variable (HODGE et al. 1996). It has also been argued that the stability of inbreeding depres- sion may result in overestimation of the strength of the additive genetic correlation in growth across ages and sites (POTTS et al. 1995; HODGE et al. 1996).

Varied results have been found when comparing estimates of heritability and breeding values derived from open pollinated and control pollinated progeny of the same E. globulus parents, even when adjusted as in

the present study. Breeding values derived from native stand open pollinated progeny have been shown to be significantly correlated with those derived from con- trolled crosses for traits such as susceptibility to Myosphaerella sp. fungus attack (DUNGEY et al. 1997), Pilodyn penetration (VOLKER unpublished) and height to vegetative phase change (JORDAN et nl. 1999). Heritability estimates derived for these traits havc been comparable in the both cross types. In contrast, herita- bility estimates derived from native stand open polli- nated progeny were highly inflated for growth traits, and breeding values derived from open and control pollination were poorly correlated (GRIFFIN & COTTE- RILL 1988; HODGE etal. 1996; P. VOLKER unpublished data). Such differences may be due to variation in inbreeding and not accounting for non-additive genetic effects (i.e. maternal or specific combining ability). Indeed, the specific combining effects for growth in E. globulus appear to be relatively high, at least compara- ble to additive genetic effects (HODGE et al. 1996; VAILLANCOURT et nl. 1995; P. VOLKER unpublished data). Non-randomoutcrossing with afew malc parents may thus also bias breeding values derived from open pollinated progeny.

Most E. globulus breeding programs are moving to controlled pollinated assessment after first generation improvement, stimulated by the development of new single-visit pollination procedures (HARBARD et al. 1999; WILLIAMS etal. 1999). Such full pedigree control will allow more accurate estimation of genetic parame- ters, the possibility of separating additive from non- additive genetic effects, and improved accuracy in the prediction of genetic merit for breeding and deploy- ment.

CONCLUSIONS

Heritabilities estimated for most traits were consistent with other studies. Survival, forking and form were poorly heritable. Growth and relative bark thickness were under moderate genetic control, whereas Pilodyn penetration and vegetative phase change were under strong genetic control. Genetic variation in most traits was strongly correlated across sites, indicating low genotype by environment interaction. Age-age genetic correlations for growth were also high. However. the possibility that these genetic parameters, particularly for growth, are inflated by inbreeding depression cannot be dismissed. Growth traits were in general genetically independent fromother key objective traits at the within and between subrace levels.

The significant genetic variation detected for both growth and Pilodyn, coupled with their genetic inde- pendence, would argue that considerable progress can

be made in improvement o f this base population fo r pulpwood production in Argentina. A strong genetic correlation across ages and sites suggests that early selection for growth and a single breeding population is possible with little loss of genetic gain.

ACKNOWLEDGMENTS

The authors thank INTA- SOPORCEL (Instituto Nacional de Tecnologia Agropecuaria. Argentina - Sociedad Portugucsa dc Papcl S. A,, Portugal) for I'acilitating the data, Dr. Greg Jordan for comments and assistance with analysis and Peter Volker for allowing us to use unpublished results. Trials and data collection were financially supported by the Proyecto Forcstal de Desarrollo. INTA, the Argentinian Government and University ofTasmania sponsored a postgraduate scholar- ship for tlie senior author

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