HETEROTHALLISM and SEX IN THE FUNGI
Authors: WHITEHOUSE H. L. K. 
Published: January 2008

Summary1. The term heterothallism was first used by Blakeslee in 1904 for the condition of sexual reproduction which he found in certain species of Mucorales, such that ‘conjugation is possible only through the interaction of two differing thalli’. In those species in which it can be shown that the thalli differ in sex, it is proposed that the term morphological heterothallism be applied, and that those species in which the unlike thalli differ by an incompatibility factor be considered to show physiological heterothallism. It is thought that the heterothallic species of Mucorales possess heterothallism of the latter type.2. Two main types of physiological heterothallism are recognized, distinguished as two‐allelomorph and multiple‐allelomorph respectively. In the two‐allelo‐morphic type, the condition is evidently determined primarily by two allelomorphs at one locus, and species possessing it are divided into strains of two kinds, commonly described as plus and minus. In the multiple‐allelomorphic type, the heterothallism appears to be determined by a multiple‐allelomorphic series at either one or two loci. If the latter, the two loci usually segregate independently at meiosis, and such species are described as tetrapolar, since each individual bears spores of four different mating types, in contradistinction to the bipolar condition of species with one locus for heterothallism.3. An outline is given of the known distribution of the occurrence of morphological heterothallism and the various types of physiological heterothallism within the fungi. Typical examples of each type are given below:I. Morphological heterothallism, e.g. Dictyuchns monosporus, Achlya bisexualis.II. Physiological heterothallism.(i) Two‐allelomorph, e.g. MucorMucedo, Ascobolusmagnificus, Sclerotinia Gladioli, Neurospora sitophila, Puccinia graminis, Ustilago Kolleri (syn. U. levis).(ii) Multiple‐allelomorph: (a) Bipolar, e.g. Coprinus comatus. (b) Tetrapolar, e.g. Coprinus fimetarius.4. Multiple‐allelomorph physiological heterothallism is shown to have advan tages over the two‐allelomorphic type in evolution, particularly if the number of allelomorphs in the population of the species at the loci for heterothallism is large. The advantages are (a) increased chance of compatible strains meeting, and (b) greater degree of outbreeding that results. The tetrapolar type of multiple‐allelomorph heterothallism gives an increased tendency for outbreeding to occur compared with the bipolar type, provided that the number of allelomorphs in the population is more than two at both loci.5. The term homothallic is applied to species in which sexual reproduction can occur in colonies derived from single spores. If such spores are uninucleate or contain nuclei of only one genotype, then the homothallism is primary. If nuclei of compatible mating types are included in each spore at the time of its formation, then the homothallism is secondary. Homothallism appears to be more frequent in Phycomycetes and Ascomycetes than in Basidiomycetes. Certain species appear to be intermediate in character between typical homothallic and heterothallic species; they may be described as showing partial heterothallism.6. In species of fungi which possess differentiated gametes or gametangia and which also show physiological heterothallism, the two phenomena are usually independent in their genetic determination and in most species have probably originated separately. Such species occasionally show unisexual strains. These appear to be mutant forms of normally monoecious species which are deficient or sterile in the organs of one or other sex.7. Heterokaryosis, or the occurrence of nuclei of more than one genotype within a single cell, is known to occur in many species of fungi and appears to be advantageous in haploid organisms. In some fungi with physiological heterothallism, heterokaryosis is restricted and can occur only between nuclei of the same mating type. In others, there is no restriction of this kind and the sex organs or gametangia are then not essential for bringing together the gamete nuclei. Herein lies a possible explanation for the degenerate condition of the sex organs or their complete absence in many species of fungi.8. Morphological and physiological heterothallism are considered to have evolved independently of one another, except in the lower Phycomycetes, and their occurrence for the most part in different groups of fungi suggests that they may have arisen comparatively rarely in evolution.9. In groups of fungi in which physiological heterothallism is manifest, it would appear on theoretical grounds that the following successive evolutionary steps must originally have taken place in the order given:(a) Homothallism is replaced by two‐allelomorph heterothallism.(b) Heterokaryosis, at first restricted to nuclei of one mating type, becomes unrestricted and the sex organs become inessential for bringing the gamete nuclei together, subsequently being partially or wholly lost.(c) Two‐allelomorph heterothallism is replaced by bipolar multiple‐allelomorph heterothallism.(d) Bipolar multiple‐allelomorph heterothallism is replaced by tetrapolar. Steps (a) and (d) are probably readily reversible, and, in consequence, existing homothallic species are probably mostly derived from heterothallic ancestors and, among species with multiple‐allelomorph heterothallism, bipolar species are probably mostly derived from tetrapolar. Secondary homothallism, which is clearly derived from a heterothallic condition, can be expected to appear at any stage after heterokaryosis has become unrestricted. The occurrence in a specific order of these various evolutionary steps provides valuable information relating to the course of evolution in the fungi.