Genetic diversity in Ethiopian barley in relation to altitude
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1 Genetic Resources and Crop Evolution 41 : , Kluwer Academic Publishers. Printed in The Netherlands. Genetic diversity in Ethiopian barley in relation to altitude J. M. M. Engels' Plant Genetic Resources Centre/Ethiopia (PGRC/E), P.O. Box 30726, Addis Ababa, Ethiopia; 'Present address : IBPGR, Via delle Sette Chiese 142, Rome, Italy Received 20 April 1993 ; accepted I September 1993 Key words : barley, characters, diversity index, genetic diversity, genetic resources, Hordeum vulgare Summary A representative sample of the Ethiopian barley collection, maintained at the Ethiopian Plant Genetic Resources Centre (PGRC/E), was studied for its phenotypic diversity for some agronomic characters, i.e. kernel row number, spike density, spikelets per spike, caryopsis type, kernel colour, thousand grain weight, days to maturity and plant height. The diversity was estimated by using the Shannon-Weaver diversity index (H') for each of the characters to examine overall genetic divergence between accessions on the basis of administrative regions, ecogeographical zones as well as altitudinal ranges within Ethiopia. Most of the variation was due to differences among characters and only a relatively small fraction due to differences between regions. However, almost all characters are considerably influenced by altitude within the regions. The mean diversity index for all characters increases with altitude, reaches a maximum between 2,400 and 2,800 m, and decreases beyond that altitude. Introduction Barley (Hordeum vulgare L.) is one of the oldest food crops and has been cultivated in Ethiopia since ancient times. Harlan (1969) and Doggett (1970) indicated that barley was brought to the Ethiopian Highlands at least 5000 years ago. Since then considerable diversity has been built up, and Ethiopia is generally considered as a secondary gene centre or a centre of diversity for barley and not as a centre of origin (Tolbert et al., 1979). The diversity in Ethiopian barley has been studied in a number of cases (Vavilov, 1926 ; Giessen et al., 1956 ; Ward, 1962 ; Tolbert et al., 1979; Bekele, 1983a, 1983b, 1983c ; Negassa, 1985 ; Zemede, 1988) using mainly discrete (noncontinuous) characters. Disease resistance genes found in Ethiopian barley landraces (Moseman, 1971 ; Qualset, 1975 ; Lehmann et al., 1976) and the identification of high protein and lysine contents in some accessions (Munck et al., 1971) further increased the interest of plant breeders in Ethiopian barley. In an earlier study Engels (1991) presented results of diversity analyses conducted with a much larger number of accessions from Ethiopia, than were ever used for one single country in earlier studies (Ward, 1962 ; Tolbert et al., 1979). The diversity was estimated by the Shannon-Weaver diversity index. The results of the analyses did not show significant differences between the administrative regions or provinces, which were arbitrarily grouped into four ecogeographic regions, i.e. the northern administrative regions (high altitude, relatively dry), the western administrative regions (higher rainfall), the southern administrative regions (highest rainfall), and the central and eastern administrative regions (high altitude, diverse).
2 6 8 However, since the actual growing conditions vary significantly from one locality to the other, even within regions, it was expected that the genetic diversity might be strongly influenced by altitude. Therefore, diversity indices were calculated for the various altitudinal zones as well as for the characters, and then analysed to measure the effect of altitude on the genetic diversity of barley landraces. The results of these analyses are presented in this paper. Materials and methods In the calculation of diversity indices for the ecogeographic and administrative regions the data of 3,765 barley accessions were used. The accessions represent an approximately random sample from a total of over 8,000 Ethiopian barley samples which are maintained by the Plant Genetic Resources Centre Ethiopia (PGRC/E) and which have been collected since 1977 throughout Ethiopia. The passport data were recorded during the germplasm collecting missions and the morphological data were taken during the routine characterisation activities of PGRC/E. This characterisation work was carried out at Holetta (at approximately 2,400 m above sea level, about 30 kms west of Addis Ababa), and the data were recorded from unreplicated small plots (+2m' each), each representing an accession, planted in ascending order of the accession number and generally calculated as the mean of five randomly chosen plants or ears per accession. The majority of the accessions are morphologically rather uniform since they were selections from heterogeneous landraces. Data were analysed for seven characters, presented in Table 1. The choice of the characters was based on their use in earlier studies, their consistency of expression over the years, and their reliability in scoring, as well as their relevance to plant breeders. Several of the selected characters which show continuous variation needed to be converted into "discrete" characters. In order not to bias the contribution of the individual character to the mean diversity index each phenotypic range was arbitrarily divided into five classes. Furthermore, these quantitative characters had shown their usefulness in earlier studies (Ward, 1962 ; Engels, 1991), proved to be consistent over the Table 1. Characters examined, their respective classes, range or frequencies Character Character state Code 1. row 6 rowed number 2 rowed** irregular irr Spike density lax intermediate dense Range* or frequency (%) 3. Spikelets per < 15 1 mean 22 spike*** 15 to 20 2 min to 25 3 max to 30 4 = or > Caryopsis type covered covered 96.5 naked naked colour white-brown purple-black Days to maturity < 100 days I mean days 2 min days 3 max days 4 = or > 145 days 5 7. Plant height I mean 94 < 60 cm 2 min cm 3 max cm cm = or > 150 cm 5 *Range data are non-weighted means. **Both categories, sterile and rudimentary lateral florets, are combined. ***Only the fertile spikelets of entire spikes have been counted. years in characterisation work and their scoring turned out to be reliable. The phenotypic frequencies of the characters were analysed by the Shannon-Weaver information index (H') in order to estimate the diversity of each character within each administrative and ecogeographic region. The latter regions were arbitrarily chosen by dividing the country into four similar ecoregional zones as described in the introduction, and are presented in Table 2. For the estimation of diversity indices within altitudinal classes, only those accessions could be
3 Gojam Welega Ilubabor Kefa Western Region Gamo Gofa Sidamo Bale Southern Region Shewa Arsi Harerge Central & Eastern Region Unknown Ethiopia Table 2. Frequencies calculated as percentages of the phenotypic classes of the seven characters used for each administrative region. The frequencies of the four geographic regions and Ethiopia as a whole are calculated as weighted mean percentages Region Number of entries' row number Spike density Spikelets per spike Caryopsis type colour Days to maturity Plant height 6 2 irr covered naked Eritrea Tigray Gonder Welo Northern Region 'These numbers vary insignificantly from character to character.
4 7 0 used for which specific data on the altitude of their original collecting site were available. Although this resulted in a total number of only about 1,000 accessions, they can be treated as a random sample of the total barley diversity in Ethiopia since their variation for the characters used was not significantly different from the overall variation of the 3,765 accessions. The actual sample sizes per altitudinal class are included in Table 4. For the comparative analyses of the diversity indices the altitude classes were arbitrarily grouped into the following altitudinal zones : "lower elevation zone"-a (< 2,400 m) ; "medium elevation zone"-b (2,400-3,000 m) ; and "higher elevation zone"-c (> 3,000 m), termed A, B and C respectively. The diversity index was calculated for these zones by using the Shannon-Weaver equation as presented by Poole (1974) : H'= Y p+ loge p ; where s represents the number of phenotypic classes of a given character, and p ; the proportion of the total number of accessions consisting the i" class. In order to keep the values of H' in the range of 0-1, each value of H' was divided by its maximum value, i.e. loge s. Normalized data for each character were used in the analysis of variance to determine whether the diversity indices for a given character differ significantly between altitude zones. The critical difference (C.D.) between mean diversity indices for altitude zones for a given character was calculated as described by Panse & Sukhatme (1985). Results and discussion Distribution of phenotypic frequencies Frequencies of the various characters for each administrative region and the weighted means for the ecogeographical regions are presented in Table 2. A preliminary analysis of some of the results presented here was described in Engels (1991). In general, the mean frequencies per ecogeographic region do not show marked variation and the same holds true for the frequencies per administrative regions for almost all the characters. The latter was expected since the administrative regions are political/administrative sub-divisions not based on ecological aspects. One exception is the high frequencies (>72%) of tworowed barley accessions found in Eritrea, Tigray, Welega, Ilubabor and Kefa. There is an increase of the spike density from north to south and from west to east, showing clinal variation. The purple to black coloured kernels are more frequent in the south-west (Welega, Ilubabor, Kefa, Sidamo and Arsi). In the administrative regions of Eritrea, Tigray, Welo, Welega, Ilubabor, Kefa, Gamo Gofa and Harerge the average days to maturity are lower than the Ethiopian average. In the drought prone northern administrative regions (Eritrea, Tigray and Welo) this might be caused by a combination of natural selection as well as human selection for early maturity to provide the crop with an escape mechanism. In the more humid southern regions human selection alone seems to have produced earlier types. The barleys from the southern region and from Eritrea have a higher average straw length than the accessions of the rest of Ethiopia, whereas straw length and days to maturity are not strongly correlated (r = 0.21 at a significancy level of 1 %). Zemede (1989) concluded that morphological traits are under direct influence of both human and natural selections and that some morphological features are significantly associated with altitude. Phenotypic diversity indices over regions The estimates of H', individually and pooled over characters and regions, show relatively wide variations between characters (Table 3). The caryopsis type (covered or naked) and plant height were the characters with the lowest diversity indices and spike density had the highest overall index. The pooled indices over characters within administrative and ecogeographic regions are relatively uniform. Eritrea and Ilubabor had the lowest values and this might be explained by a possible greater degree of selection pressure since both regions somehow represent the extremes of the production conditions in Ethiopia, for instance lowest rainfall in Eritrea, and highest rainfall as well as lowest average altitude of collecting sites in Ilubabor. Another possible factor could be the relatively small number of accessions which were available from both regions. Bekele (1983b) found different
5 7 1 Table 3. Estimates of the diversity indices (H') for the various Administrative Regions, four geographic regions, and mean diversity (H') and its standard error over all characters Administrative and ecogeographic region row no. Spike density Spikelets per spike Caryopsis type colour Days to maturity Plant height H' + SE Eritrea Tigray Gonder Welo (North) Gojam Welega Ilubabor Kefa (West) Gamo Gofa Sidamo Bale (South) Shewa Arsi Harerge (Central & East) Ethiopia levels of genotypic diversity for different regions, based on allozyme analyses. The analysis of variance among and within ecogeographic and administrative regions did not reveal any significant difference. By far the highest variance is due to "among characters within administrative regions", 92.4% of the total variance was contributed to this source as was calculated from the sum of squares of an ANOVA for all observations. Comparing the overall diversity index for Ethiopian barley of this study with results from other studies (i.e. Qualset & Moseman, 1966 ; Qualset, 1975 ; Tolbert et al., 1979; Bekele, 1983c ; Negassa, 1985) it can be concluded that the results are, in general, very similar despite the use of different characters, different number of characters and different sample sizes. Phenotypic diversity indices over altitudes The estimates of H' for each of the characters and the altitude classes as well as the mean H' per altitude class are presented in Table 4. For all characters, except caryopsis type and kernel colour, an increase of the diversity index can be observed by increasing altitude from 1,800 till ±3,200m and thereafter a decrease occurs. These observations are supported by the analyses of variance (Table 5) "between" (F5 4 = 2.70 ; s ign. at 5% level) and "within" altitude classes (F54 = ; s ign. a t 1 % level). The results of a "split" ANOVA to analyze the influence of the altitude on the diversity indices for all characters are presented in Table 6. This shows that H' for the altitude classes 2,400-3,000 m are significantly bigger than the mean diversity indices for the lower altitudes (at the I % level) and significantly greater than the higher altitude classes (at the 10% level). The latter results would have been significant at a much lower percentage level had the medium altitude zone been chosen from 2,400-3,200 m. This was not done in order to have more or less comparable ranges in altitude for each zone. The
6 72 Table 4. Estimates of H' for the ten altitude classes and the seven characters, and mean diversity (H') over all characters and altitude classes and their corresponding critical differences (CD) Altitude classes Number of accessions' row Spike density Spikelets per spike Caryopsis type colour Days to maturity Plant height < 1800 m m m m m m m m m = or > 3400 m Number of Accessions ' (CD = 0.12) Altitude range 1 1 A B C H' Ethiopia H' (CD = 0.10) 'Numbers of accessions varied from character to character within the range presented. Critical Differences between the low and medium altitude ranges is 0.12 and between the medium and the high ranges The analyses of the H' for the separate characters and altitude ranges revealed that significant differences were found between the IT of the different altitude ranges only for "days to maturity" and for "plant height" (in the latter case only between medium and high altitude ranges). The above results indicate that the mean diversity indices indeed vary with altitude and that the indices are significantly highest for altitudes between 2,400 and 3,200m. On a single character basis such significant differences were only found for "days to maturity" and for "plant height". For both characters the phenotypic expression does depend on altitude, i.e. for days to maturity in altitude range A days, in B days and in C days and for plant height in altitude range A cm, in B 99.1 cm and in C 95.6 cm. In the latter case there exists a very strong negative correlation (r = -0.89) between plant height and Table 5. Analysis of variance of diversity indices "between" and "within" altitude classes for seven characters Source df SS MS % F Between altitude classes * Between characters within altitude classes ** Error *Significant at the 5% level ; **Significant at the 1% level. Table 6. Analysis of variance of the pooled diversity indices (H') over character for (a) the altitude ranges A and B and (b) for ranges B and C Source df SS MS F a) Among altitude ranges A and B ** Within altitude ranges, between classes b) Among altitude ranges B and C ' Within altitude ranges, between classes **Significant at the 1% level ; 'Significant at the 10% level.
7 73 altitude, indicating that the natural selection pressure for short plant stature increases with increasing altitude, perhaps as a result of harsher growing conditions. Conclusions The overall diversity index of Ethiopian barley accessions used in this study and similar results from other studies made earlier, support the conclusion that Ethiopia is an important centre of diversity for barley. This diversity is rather evenly distributed over the barley producing regions in the country. However, the study revealed decreasing diversity indices towards lower as well as higher altitudes. This means that to capture the most genetic diversity one should concentrate on the medium altitudes between 2,400 and 3,200 m, which correspond with the best growing conditions for barley in Ethiopia. Because of presumed stronger natural selection pressure towards the extremes of the altitudinal distribution range, one might expect certain desirable genotypes, for instance for abiotic stress tolerance, such as frost resistance or drought, to be found at higher frequencies in these areas. Acknowledgements The author would like to thank all colleagues involved in the collecting and characterisation work at PGRC/E and Dr. Melaku Worede, Director, for permission to use the data in this study and Drs. Masa Iwanaga, Toby Hodgkin and Mr. Mike Bolton for their critical review of the manuscript. References Bekele, E., 1983a. Some measures of gene diversity analysis on landrace populations of Ethiopian barley. Hereditas 98 : Bekele, E., 1983b. Allozyme genotypic composition and genetic distance between the Ethiopian landrace populations of barley. Hereditas 98 : Bekele, E., 1983c. A differential rate of regional distribution of barley flavonoid patterns in Ethiopia, and review on the centre of origin of barley. Hereditas 98 : Doggett, H Sorghum. Longmans, London. Engels, J. M. M., A diversity study in Ethiopian barley. In : J. M. M. Engels, J. G. Hawkes & Melaku Worede (Eds.) "Plant Genetic Resources of Ethiopia". Cambridge University Press, Cambridge Giessen, J. E., W. Hoffmann & R. Schottenloher, Die Gersten Athiopiens and Erythraas. Z. Pflanzenziichtg 35 : Harlan, J. R., Ethiopia : a centre of diversity. Econ. Bot. 23 : Lehmann, Chr., O. I. Nover & F. Scholz, The Gatersleben barley collection and its evaluation. In : "Barley Genetics", Vol. III. Proc. 3rd Int. Barley Genetics Symp., Garching, pp , Karl Thiemig Verlag, Miinchen. Moseman, J. G., Co-evolution of host resistance and pathogen virulence, In "Barley Genetics" Vol. II. Proc. 2nd Int. Barley Genetics Symp., 1969, pp , Washington State University Press, Pullman, Washington. Munck, L., K. E. Karlsson & A. Hagberg, Selection and characterization of a high protein, high-lysine variety from the world barley collection. In "Barley Genetics", Vol. II. Proc. 2nd Int. Barley Genetics Symp., 1969, pp , Washington State University Press, Pullman, Washington. Negassa, M., Patterns of phenotypic diversity in an Ethiopian barley collection and the Arusi-Bale Highland as a centre of origin of barley. Hereditas 102 : Panse, V. G. and P. V. Sukhatme, Statistical methods for agricultural workers. ICAR, New Delhi. Poole, R. W., An introduction to quantitative ecology. McGraw-Hill, New York. Qualset, C. O. & J. G. Moseman, Disease reactions of 654 barley introductions from Ethiopia. USDA, ARS CR Qualset, C. 0., Sampling germplasm in a centre of diversity : an example of disease resistance in Ethiopian barley. In : O. H. Frankel & J. G. Hawkes (Eds.) "Crop Genetic Resources for Today and Tomorrow". Cambridge University Press, Cambridge Tolbert, D. M., C. O. Qualset, S. K. Jain & J. C. Craddock, A diversity analysis of a world collection of barley. Crop Sci. 19 : Vavilov, N. I., Studies on the origin of cultivated plants. Bull. Appl. Bot. Plant Breed. 16 : Ward, D. J., Some evolutionary aspects of certain morphological characters in a world collection of barley. USDA Techn. Bull Zemede Asfaw, Variation in the morphology of the spike within Ethiopian barley, Hordeum vulgare L. (Poaceae). Acta Agric. Scand. 38 : Zemede Asfaw, Relationships between spike morphology, hordeins and altitude within Ethiopian barley, Hordeum vulgare, L. (Poaceae). Hereditas 110 :
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