David Haig

Genomic imprinting in mammalian development: a parental tug-of-war

Genomic imprinting in mammals is increasingly being implicated in developmental and pathological processes, but without a clear understanding of its function in normal development. We believe that imprinting has evolved in mammals because of the conflicting interests of maternal and paternal genes in relation to the transfer of nutrients from the mother to her offspring. We present an hypothesis that accounts for many of the observed effects of imprinting in mammals and relates them to similar observations in plants. This hypothesis has implications for studies of X-chromosome inactivation and a range of human diseases.

A quantitative measure of error minimization in the genetic code

SummaryWe have calculated the average effect of changing a codon by a single base for all possible single-base changes in the genetic code and for changes in the first, second, and third codon positions separately. Such values were calculated for an amino acids polar requirement, hydropathy, molecular volume, and isoelectric point. For each attribute the average effect of single-base changes was also calculated for a large number of randomly generated codes that retained the same level of redundancy as the natural code. Amino acids whose codons differed by a single base in the first and third codon positions were very similar with respect to polar requirement and hydropathy. The major differences between amino acids were specified by the second codon position. Codons with U in the second position are hydrophobic, whereas most codons with A in the second position are hydrophilic. This accounts for the observation of complementary hydropathy. Single-base changes in the natural code had a smaller average effect on polar requirement than all but 0.02% of random codes. This result is most easily explained by selection to minimize deleterious effects of translation errors during the early evolution of the code.

Genetic scrambling as a defence against meiotic drive

Genetic recombination has important consequences, including the familiar rules of Mendelian genetics. Here we present a new argument for the evolutionary function of recombination based on the hypothesis that meiotic drive systems continually arise to threaten the fairness of meiosis. These drive systems act at the expense of the fitness of the organism as a whole for the benefit of the genes involved. We show that genes increasing crossing over are favoured, in the process of breaking up drive systems and reducing the fitness loss to organisms.

New perspectives on the angiosperm female gametophyte

This review builds upon previous classifications of angiosperm female gametophytes but offers two new perspectives. Firstly, the course of development is compared to an algorithm: a predetermined set of rules that produces a mature female gametophyte. This analogy allows hypotheses to be developed as to what changes in the “developmental program” are responsible for variant forms of development. Secondly, the review recognizes that the four meiotic products of a megaspore mother cell have different genetic constitutions and may have conflicting interests. In most cases, only one member of a megaspore tetrad gives rise to a functional egg. This megaspore is called the germinal spore. The other members of the tetrad are called somatic spores. Somatic spores do not give rise to functional eggs and, therefore, cannot leave direct genetic descendants.Non-monosporic embryo sacs are genetic chimeras containing derivatives of more than one megaspore nucleus. Conflict may arise within such embryo sacs between the derivatives of the germinal megaspore nucleus and the derivatives of somatic megaspore nuclei. “Antipodal eggs” and chalazal “strike” are interpreted as evidence of this conflict. The behavior of somatic spores and their derivatives is often variable for different embryo sacs produced by the same sporophyte. This has created difficulties for existing classifications of embryo sac “types” because more than one type is sometimes recognized within a species. A new classification of developmental algorithms is presented that emphasizes the fate of the germinal spore and its derivatives.ZusammenfassungDieser Überblick baut sich auf vorangehende Klassifizierungen des weiblichen Gametophyten der Angiospermen auf, zeigt aber zwei neue Perspektiven auf. Erstens wird der Entwicklungsverlauf vergleichen mit einem Algorithmus: eine vorbestimmte Reihe von Regeln, die den entwickelten weiblichen Gametophyten hervorbringen. Diese Analogie erlaubt, die Hypothese aufzustellen, daß eine Änderung im “Entwicklungs-Programm” verantwortlich ist für verschiedene Formen der Entwicklung. Zweitens zeigt dieser Überblick, daß die vier meiotischen Produkte der Megasporenmutterzelle unterschiedliche genetische Zusammensetzung und vielleicht widersprüchliche Interessen haben. Meistens entwickelt sich nur aus einer Zelle der Megasporentetrade eine funktionsfähige Eizelle. Diese Megaspore wird “Keimspore” gennant. Die übrigen drei Megasporen werden als “somalische Sporen” bezeichnet. Aus den somatischen Sporen können sich keine funktionsfähigen Eizellen und somit keine direkten genetischen Nachkommen bilden.Nicht-monospore Embryosäcke sind genetische Chimären, die Derivate von mehr als einem Megasporennukleus enthalten. Konflikte können innerhalb dieser Embryosäcke entstehen zwischen Derivaten des Keim-Megasporennukleus und Derivaten des somatischen Sporennukleus. Die “Antipodialeizellen” und der “Teilungsstreik” der chalazalen Kerne werden als Beweis für diesen Konflikt interpretiert. Das Verhalten der somatischen Sporen und ihrer Derivate ist oft variable für verschiedene Embryosäcke, die vom gleichen Sporophyten produziert wurden. Dies verursachte Schwierigkeiten in der bestehende Klassifizierung der Embryosack-Typen, weil manchmal mehr als ein Typus innerhalb einer Art auftreten kann. Eine neue Klassifizierung auf Grund des algorithmischen Entwicklungsverlaufes wird hier vorgestellt, der die Entwicklung der Keimspore und ihrer Derivate hervorhebt.

The evolution of unusual chromosomal systems in coccoids: extraordinary sex ratios revisited

Coccoids (scale insects) exhibit a wide variety of chromosomal systems. In many species, paternal chromosomes are eliminated from the male germline such that all of a males sperm transmit an identical set of maternal chromosomes. In such species, an offsprings sex is determined by whether or not paternal chromosomes are inactivated in the eggs cytoplasm after fertilization. This paper presents a model of the evolution of paternal genome loss in coccoids from an ancestral system of XX‐XO sex determination. The model is based on Hamiltons (1967) theory that different genetic elements within the genome have different unbeatable sex ratios. In this model (1) meiotic drive by the X chromosome in XO males causes female‐biased sex ratios; (2) the maternal set of autosomes in males evolves effective sex linkage to exploit X‐drive; and (3) genes expressed in mothers are selected to convert some of their XX daughters into sons. A similar model may explain the evolution of haplodiploidy.

Plants’ use of ants for dispersal at West Head, New South Wales

Of the world’s known species of myrmecochores, plants which provide food bodies to induce ants to disperse their seeds, many are found in the dry sclerophyll vegetation of Australia. Here we present data and observations on myrmecochory on the West Head, and area of dry sclerophyll vegetation near Sydney, and in the light of these we discuss possible explanations for the distribution of myrmecochory. In most stands myrmecochores made up about 30% of the overall plant species complement, but few of the dominant species were myrmecochores. Myrmecochores tended to occur in a wider range of stands than non-myrmecochores. Within a stand, they tended to occur more of their own diameters from their nearest conspecific neighbours, but otherwise did not occupy detectably different microsites. Many proposed explanations for myrmecochory could explain either its commonness in Australia, or why it should be adaptive in sclerophyll shrubs, but none explain why it should be adaptive in sclerophyll shrubs in Australia but not in California or the Mediterranean. Australian dry sclerophyll vegetation, unlike that of California or the Mediterranean, is delimited by low-phosphorus soils; empirically, the correlation of myrmecochory with low-phosphorus soils is good. Evidence is given to suggest that in the vegetation of the West Head the limiting currency for seed production is phosphorus. Food bodies cost little phosphorus, so that myrmecochory is cheap in terms of the effective currency. However, wings and hairs are also cheap in terms of phosphorus.

Seed size, pollination costs and angiosperm success

SummarySeed plants capture pollen before seeds are dispersed and abort unpollinated ovules. As a result, each seed is associated with an accessory cost that represents the costs of pollen capture and the costs of aborted ovules. Accessory costs may explain the minimum seed size among species, because these costs are likely to comprise a greater proportion of total reproductive allocation in species with smaller seeds. For very small propagules, the costs of pollination may not be worth the benefits, perhaps explaining the persistence of pteridophytic reproduction at small propagule sizes. The smallest angiosperm seeds are much smaller than the smallest gymnosperm seeds, both in the fossil record and in the modern flora. This suggests that angiosperms can produce pollinated ovules more cheaply than gymnosperms. Pollination becomes less efficient as a species decreases in abundance, and this loss of efficiency is greater for species with a higher accessory cost per seed. We propose that the greater reproductive efficiency of angiosperms when rare can explain why angiosperm-dominated floras were more speciose than the gymnosperm-dominated floras they replaced.

Conflicts among megaspores

At meiosis in angiosperms a diploid megaspore mother cell produces four haploid megaspores. Usually only one, the germinal spore, produces a functional egg. The theory of kin conflict predicts that megaspores should compete to become the germinal spore or that the germinal spore should be determined by action of the maternal genome. Once the germinal spore is determined alleles present in the other (somatic) spores may be more likely to be present in the germinal spore of another ovule on the same mother than in the germinal spore of their own ovule. The theory predicts natural selection may favour alleles expressed in somatic spores that interfere with the development of their own ovule if this benefits other ovules. Therefore, bisporic and tetrasporic development are expected to be less evolutionarily stable than monosporic development in which the female gametophyte is the product of the germinal spore alone. In support of this theory evidence is presented that the germinal spore is usually determined by the maternal genome and that in non-monosporic forms of development the derivatives of somatic spores are often non-functional.

Kin conflict in seed plants

Kin selection theory proposes that individuals value the reproductive success of relatives at a rate determined by their probability of shared alleles. The theory predicts when the interests of relatives are in accord and when they conflict. Though kin selection arguments have revolutionized the study of animal behavior, they have only recently been applied to plants. Kin selection has already been claimed to explain the formation of endosperm by double fertilization. This is the character that distinguishes angiosperms from gymnosperms. Plant life cycles involve interactions among kinds of relatives not encountered in animals. These interactions should be a fertile field for new applications of theory and the testing of ideas originally developed elsewhere.

A model for the origin of heterospory

Sporophytes are predicted to produce spores of a size that maximizes the return in gametophyte fitness per unit investment. Larger spores are predicted for those species in which gametophytes depend on stored food reserves for successful reproduction. A model for the origin of heterospory is proposed, in which an initially homosporous population is subject to natural selection for increased spore size. Because the minimum costs of male reproduction are less than the minimum costs of female reproduction, larger food reserves evolve principally for the use of female reproduction. Above some critical spore size, the population can be invaded by sporophytes producing smaller spores, which reproduce predominantly as males. This model for the origin of heterospory has three phases: (1) a gradual increase of spore size in a homosporous population; (2) the sudden introduction of smaller microspores; (3) the subsequent divergence in size and specialization of the two spore types. The model explains haploid dioecy as a consequence of pre-existing mechanisms of sex determination, and endosporic development as a consequence of an increased dependence on spore food reserves for reproduction.