Each organism has its own phenotype. Epigenetic, genetic or genomic properties orchestrate the phenotypes in the organism. The nearly identical phenotypic difference can occur through epigenetic, genetic or genomic causes. Richard Goldschmidt, a German-American geneticist, noticed this about 80 years ago and discussed it in his book “The Material Bases of Evolution,” published in 1940. Through studying the polymorphism of moss and cytogenetics and mutant analysis of fruit flies, he noticed that very similar phenotypic differences were observed in seasonal polymorphism in a single species, in genetic mutants of a single species and between two different species.
A cell is a network of biochemical reactions with many detours encapsulated in the plasma membrane. The network maintains its inner equilibrated state. Andy Poss proposed this as the state of dynamic kinetic stability. (Imagine a water wheel on a creek. The scenery looks static, but the water and wheel constantly move. Thus, life is not precisely an equilibrated state but a dynamic kinetic stability state.) A multicellular organism is a network nested above the networks of cells through biochemical communications. The network with detours is fundamentally robust and plastic. The detours work as buffers against environmental changes.
Proteins are the major players in the network of biochemical reactions in cells and organisms. They are encoded in the DNA sequence of the genome as genes. This means although the network is genuinely robust, it is constrained by the genome. The DNA sequence limits the variation of proteins in the network. Thus, there is a limit of robustness, securing the original equilibrated state. When internal or external perturbation exceeds its robustness, out-of-equilibrium shifts into other equilibrated states in its reaction networks. This means that the phenotypic states are not infinite but constrained into multiple equilibrated states. When the perturbation further exceeds, the network cannot find the equilibrated states and will collapse. This happens at the cellular and organismal levels—a death.
Most phenotypes in a cell and an organism are in the robust equilibrated state of the network. On the other hand, some are regulated by only one to a few players, like the colours of an organism. If the consequence of multiple interactions in the complex network creates one phenotype, its phenotypic changes might be seen as the jumping of distinct multiple equilibrated states. On the other hand, if only a few players are involved, the phenotypic changes would be relatively gradual in one dimension.
The network stability and its equilibrated state are primarily controlled by the amount of each protein and its reaction's efficiency (i.e. protein functions). Since each protein is encoded in DNA as a gene, there are three distinct molecular mechanisms for regulating them: epigenetic, genetic and genomic. All three can cause similar phenotypic consequences but have specific heredity characteristics in generation and population.
The phenotypic change caused by epigenetic changes is reversible. This type of change occurs in an individual as well as a population. The amount of gene expression is often controlled by transcriptional regulation like DNA and histone methylation. In addition, the amount of protein is controlled by translational regulation. Generally, not only a single gene but many genes are simultaneously affected. They can be induced by environments such as food availability and temperature within a single species. Seasonal polymorphisms of insects are a good example.
Genetic and genomic changes also cause the phenotypic differences. In contrast to epigenetic changes, the changes are irreversible and always happen in a single cell or organism. Through replication, the phenotypic changes are inherited by its offspring. Genetic changes can affect the amount of gene expression by altering gene regulatory sequences. They can also compromise the functions of a protein by altering protein-coding sequences in the gene.
Genomic changes are irreversible changes at the chromosomal level. One form of genomic change is numerical changes in chromosomes, called karyotypic changes, including aneuploidy and polyploidy. The other form of genomic change is chromosomal rearrangement, including chromosomal translocation, inversion, deletion, duplication, etc. The gene and protein amounts can be altered because of the change in the number of alleles. Moreover, the function of specific genes might be disrupted at the breaking points of the chromosomal rearrangement.
Genetic and genomic changes can gain similar phenotypes in cells and organisms in a clonal population. However, there is a fundamental difference when this happens at an organism level. Successful meiosis is critical for the reproduction of multicellular organisms. During meiosis, two homologous chromosomes are paired to exchange their genetic materials DNA sequences. The two do not need to be identical but similar enough to recognize each other. Chromosomal rearrangement has a risk of preventing this essential chromosomal pairing event. Without successful meiosis, there is no gamete formation. Thus, there is no reproduction, and there is no offspring.
Natural selection considers that the phenotypes of each organism are the criteria of survival selection by an environment but not the molecular mechanisms causing the phenotypes. In this sense, the three distinct molecular mechanisms can theoretically create identical phenotypes that could be selected. However, there are apparent differences in the subsequent generation. If the epigenetic mechanism causes the phenotypes, the mechanism is encoded within the genome. Individuals in the same species can create the same phenotypic variations. Phenotypic selection can happen, but the available variations and their frequency in offspring are unchanged.
How about if the genetic mechanism causes the phenotype? There are several considerations. First, does a single gene or multiple genes control the phenotype? Second, is the allele(s) contributing to the phenotype dominant or recessive? Third, if multiple genes contribute, are there genetic interactions among them? The phenotype generated by the genetic mechanism can be inherited and reappear in the subsequent generation, but only sometimes. If the phenotype is caused by a dominant allele of a single gene, 50% of its offspring would reproduce it. Suppose a recessive allele of a single gene causes the phenotype. In that case, none of its offspring show the original phenotype because all offspring will be heterozygous with a wild-type allele. If multiple genes contribute in a complex manner, reproducing the same genetic combination is impossible within several generations, not only in the subsequent generation.
In animals, diploid organisms, beneficial alleles are not easily enriched in a population except for dominant alleles. Because of mating, genetic combinations are shaffled in each round of reproduction. Even if the advantageous combination is created, it is not fixed and easily diluted in a population. The advantageous phenotype often does not appear in the subsequent generation.
Then, does any genomic change have been linked with phenotypic changes at the organismal level? No. So far, not yet. However, genomic changes may prevent the homologous chromosomal pairing during meiosis. The heterozygous of a rearranged chromosome could be fertile, sub-fertile or sterile. If the fertility is not changed, the rearranged chromosome will be inherited in a population as a variant. If sterile, no offspring. The case of sub-fertility is fascinating. The fertility should fully recover if the rearranged chromosome becomes homozygous within a couple of next generations by sibling intercrossing. Homozygous of the rearranged chromosome should not have any issue in fertility. Theoretically, this can be a reproductive barrier. Reproductive isolation is achieved without geographical separation.
This subfertility sets a reproductive barrier between a tiny sibling population homozygous of the rearranged chromosome and the original population. If any phenotype is associated with this separation, the phenotype will be fixed in the new population. This new population can be a new species. Does the new species have a chance of survival in the condition outnumbered by the original population? If the new one must compete with the original, the opportunity will be very slim. On the other hand, if the newly fixed trait in the new species permits it to survive in an environment that cannot be used for the original one, there is a good chance. The two species do not need to compete but coexist.
Before the discovery of DNA, when genes were considered encoded on chromosomes as ‘ beads on a string,’ Goldschmidt saw chromosomes could carry information. The order within chromosomes is meaningful. A gene is not a separate entity like ‘beads on a string’ but is interconnected with its neighbours. Based on his chromosomal cytogenetic analysis and his knowledge of genetics and developmental processes, he speculated that chromosomal rearrangement can impact development, including body plan, by regulating the timing of gene functions. In modern terminology, this means gene regulation with long-range enhancers and 3D chromosomal conformations.
Although speciation based on chromosomal rearrangement is not appreciated in the current evolutionary biology, the whole genome sequence analysis of various organisms shows karyotypic differences and macroscopic chromosomal differences in addition to microscopic DNA sequence differences.
The theory of natural selection in Neo-Darwinism suggests that natural selection works on phenotypic variation. The cause of phenotypic variation has never been a part of consideration. If I follow this theory, whatever causes the advantageous phenotypic variation, they will have a higher chance of survival in a population. If the changes are epigenetic, the individuals presenting the phenotype can still be selected, but no specific genotype will be associated and enriched. If the changes are genetic or genomic, the survivors should increase the frequency of the advantageous allele. But there is no guarantee that the same phenotype will reappear in the next generation. Is it possible to have an adaptation without a continuous presentation of the advantages? I would say no. Sexual reproduction prevents adaptation. Accidental selection by genetic drifts or founder effects would be more effective in fixing any phenotype.
What does natural selection do? Just removing lethal deficiency, but not selecting better in fitness. ‘Death or alive’ in real nature is usually sporadic and unpredictable. No fitness can predict ‘death or alive’ after removing lethal deficiency. Survival up to reproductive ages is the only requirement for the continuity of species. A bit of luck and the lack of lethal deficiency are the requirements. You do not need to be better. In this way, phenotypic diversity encoded in the genome is constantly increasing. In the history of life, advantages are less significant. But robustness is critical. The robustness for continuation. Diploids can tolerate detrimental spontaneous mutations better than haploids, while haploids are more efficient in enriching advantageous mutations. Neither is better. Therefore, both are alive now. In the end, organisms are opportunistic. Whatever phenotypic changes that do not cause lethal deficiency and are not preventing reproduction will remain. This is why we can observe the enormous diversity of organisms on the earth.