Journal of Ecology 42(2): 521-556 (Jul., 1954)

Studies on Growth and Development in Lolium IV. Genetic Control of Heading Responses in Local Populations
J. P. Cooper
Department of Agricultural Botany of Reading*
*The experimental work was started at the Welsh Plant Breeding Station, University College of Wales Aberystwyth.

Abstract:

  1. The study of outbreeding populations of Lolium from different ecological origins suggests that the flowering responses of each population are closely adapted to local conditions of temperature and photoperiod. Furthermore, while heading behaviour is uniform under the conditions for which the population has been selected, considerable genetic variability may be revealed under changed conditions of temperature and photoperiod. The present paper is concerned with the two genetic problems posed by this behaviour: (a) the genetic control of differences in heading responses between local populations, (b) the means by which sufficient genetic variability is maintained in these populations for adaptive response to future selection.
  2. The genetic control of heading responses was tested by crossing parents from extreme populations of the outbreeding group, Lolium rigidum, L. italicum, L. perenne, and growing parents, F1, F2 and backcross progenies in such a range of environments as would separate the two developmental responses, competence of the shoot apex and response to photoperiod.
  3. Both competence and response to photoperiod are polygenically controlled, no main gene differences being apparent. This makes possible continuous variation in both components of inflorescence development and hence close adaptation to local environment. The parent plants from all outbreeding populations are heterozygous for genes controlling heading responses. Both competence and response to photoperiod behave as threshold characters. For each genotype there may exist a critical photoperiod or critical low temperature without which no heading can occur. No invariable linkage can be detected between the marker genes, Cc and Rr, and genes controlling competence or response to photoperiod.
  4. The maintenance of genetic variability between individuals in a population was studied by exposing several outbreeding and inbreeding populations of Lolium spp. and Triticum spp. to low-temperature treatments, and afterwards testing for competence under continuous light. A similar method was used to reveal potential variation carried within individuals in the heterozygous state. One population of Lolium perenne, the early-flowering S.24, was studied, and progenies from crossing two parents, and selfing one, were grown at threshold photoperiods and low temperatures. Homozygous plants of the inbreeding L. temulentum were used for comparison.
  5. The breeding system evidently controls the amount of genetic variation carried within the population. In the outbreeding species, L. rigidum and L. perenne, considerable genetic variation in heading responses is carried within apparently uniform populations, both in the form of concealed genetic differences between individuals and also in the heterozygous condition within individuals. In the early-flowering strain of L. perenne (S. 24) one plant may carry as much potential variation as is revealed phenotypically in the whole population. No such genetic differences are revealed within single lines of the inbreeding species, L. temulentum, Triticum aegilopoides, T. monococcum and T. vulgare, although differences may exist between lines of the same population. The genetic variation exposed by altered environment is available for future response to selection. In Lolium rigidum, selection for early or late competence does not affect response to photoperiod, i.e. selection in one environment does not necessarily lead to divergence in another.
  6. The genetic control of heading responses in other species is discussed and the following conclusions drawn: (a) Although single gene differences controlling flowering responses have been reported, any main gene difference is usually modified by a polygenic background, and often no single gene difference can be detected. (b) Both dominance and progeny distributions may be influenced strongly by photoperiod and exposure to low temperature.
  7. The genetic structure of these outbreeding populations of Lolium is compared with that of other outbreeding organisms, such as species of Drosophila, which also contain considerable genetic diversity hidden beneath a uniform phenotype. Such a population can posses high immediate fitness for its present environment and yet maintain a reserve of variation for evolutionary change.

I. Introduction

Inflorescence development on the shoot apex and its corollary, the partition of energy in the plant between seed production and continued vegetative growth, form a developmental system of ecological and adaptive importance. A comparative study of genetic variation in the timing of this system, either within one species or between closely related species, is therefore of interest, not only from the ecological standpoint, but also as indicating possible lines of evolutionary change.

The genus Lolium has a geographical distribution from central Asia, through the Mediterranean region, to the north-west coast of Europe. It contains a wide range of ecological and agronomic forms, varying from annual, self-pollinating species, such as L. temulentum and L. remotum, found as weeds in arable crops, to the biennial and perennial outbreeding species, such as L. italicum and L. perenne, which are commonly used as herbage plants. The genus therefore provides useful material for combined ecological and genetical studies.

Inflorescence development in Lolium follows the same general plan as in other Gramineae (Cooper, 1951, 1952), and appears to involve three main stages, similar to those postulated by Klebs (1918) for Sempervivum, each stage showing different responses to environmental conditions:

  1. attainment of competence (Blühreife) of the shot apex,
  2. initiation of the inflorescence under appropriate photoperiod,
  3. elongation and differentiation of the inflorescence.

The level of environmental response at each stage is under genetic control and varies with species and population.

(i) Attainment of competence. In the summer annuals, Lolium remotum, L. temulentum and L. gaudini, the shoot apex is competent to respond to photoperiod very soon after germination (Cooper & Money-Kyrle, 1952). In the winter annuals, L. rigidum and L. italicum, competence is eventually attained without low temperature, but can be accelerated by cold treatment, either natural or artificial. In most of the perennial strains of L. perenne, the shoot apex never becomes competent without exposure to low temperature.

(ii) Initiation of the inflorescence. Once competence of the shoot apex has been attained, photoperiod is usually the limiting factor in spikelet initiation. Most species of Lolium are long-day plants, in the sense that spikelet initiation is most rapid in continuous light and is progressively retarded as photoperiod decreases. The critical photoperiod below which inflorescences fail to develop varies with species and population. In the Mediterranean annuals, L. temulentum, L. remotum and L. rigidum, ear initiation can occur in 9 hr. photoperiods, although ear emergence is delayed; but the herbage strains of L. perenne from north-west Europe have higher critical photoperiods (13-14 hr. in the late-flowering pasture strain, S.23).

(iii) Elongation and differentiation of the inflorescence. After ear initiation has occurred under appropriate photoperiod, the rate of inflorescence development is controlled mainly by temperature. Such temperature response accounts for most of the local and seasonal difference in ear emergence in the British Isles (Cooper, 1952).

The comparative study of populations from different geographical and ecological origins suggests that the flowering responses of each population are closely adapted to local conditions of temperature and photoperiod (Cooper, 1951). The Mediterranean annuals attain competence very quickly and will form heads in all photoperiods from 9 to 24 hr., whereas the herbage strains of L. perenne from north-west Europe require low-temperature exposure before heading and have higher critical photoperiods. Furthermore, in each outbreeding population of the L. rigidum-L. perenne group, heading behaviour is uniform under the conditions for which the population has been selected, but considerable genetic variability may be revealed under changed temperatures or photoperiods. No such genetic diversity is revealed within single lines of the self-pollinating species of Lolium.

This high degree of adaptation in local populations, common in widely ranging species (Turesson, 1930; Clausen, Keck & Hiesey, 1940, 1948), together with the exposure of genetic variability under changed environments, poses two genetic problems; the genetic control of such adaptive characters, in this case flowering behaviour based on the response of the shoot apex to temperature and photoperiod; and the means by which sufficient genetic variability is maintained in these populations for adaptive response to future selection.

These two problems form the subject of the present paper.

II. GENETIC CONTROL OF INFLORESCENCE DEVELOPMENT

The three outbreeding species, L. perenne, L. italicum and L. rigidum, can hybridize with ease, free gene exchange occurs between them, and all are diploids with 2n = 14 (Jenkin, 1931 b; Jenkin & Thomas, 1938). They may thus be regarded as one polymorphic species or 'coenospecies' in the sense of Turesson (1929). The genetic control of competence and response to photoperiod was therefore studied by crossing modal parents from different populations within this 'coenospecies' and growing the parents, F1, F2, and backcross generations in such environments as would separate the different components of inflorescence development.

Two types of cross were used:

  1. a study of genetic differences between populations showing extreme responses to photoperiod and low temperature,
  2. tests for the linkage of genes controlling inflorescence development with marker genes for anthocyanin production.