Abstract

   Goldschmidt proposed macro/saltational evolution, which is infamously known as the “Hopeful Monster” theory. This proposal states that chromosomal rearrangement permits sudden speciation and macroevolution–large anatomical changes without intermediates—i.e., a new species with a new form emerges suddenly.

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   We consider this plausible. Chromosomal rearrangement could compromise meiosis due to the incompatibility in homologous chromosome alignments, causing subfertility in heterozygotes. Fertility could then be restored if homozygotes are produced by heterozygotes intercrossing. Thus, the creation of a reproductively isolated population is plausible within a few generations. Simultaneously, chromosomal rearrangement could modify the proximity of DNA sequences in the 3D chromosomal structure, potentially leading to changes in long-range enhancers of developmental genes. In rare occasions, one rearrangement event could impact multiple developmental processes, leading to independent anatomical traits - macroevolution. We propose that DNA synteny, the conserved proximity between genes in the genome, reflects functional blocks of long-range enhancers, and thus, conservation and disruption of DNA synteny can be tightly linked to unique body plans in phylum, class or family.

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   We found that the Wnt9b-Wnt3-Nsf locus in vertebrates is a good model to test this hypothesis, linking to the presence or absence of the female reproductive tract (FRT). This synteny is conserved in all vertebrates except in ray-finned fish, which has no FRT. In addition, Wnt9b and Wnt3 individually or coordinately affect the development of the jaw, limbs, and probably of the extragenital structure. These four anatomical traits are the unique emergent traits in the placoderm, the first-jawed vertebrates in fossils, and modified traits in ray-finned fish. We hypothesize that the rearrangements at the Wnt9b-Wnt3-Nsf locus played critical roles in the emergence of jawed vertebrates and ray-finned fish through modulating long-range enhancer interactions of Wnt9b/Wnt3 genes. In this proposal, we will experimentally identify their long-range enhancer sequences and functions. We will also establish computational strategies to identify other rare synteny breakpoints that may be related to different traits in different clades. This view allows the generation of a new species/class/phylum within a few generations, plausible without intermediates, and thus provides novel insights into evolution.

 

Overview

    The current common evolutionary view is based on the neo-Darwinian synthesis – slow, gradual changes in allelic frequency based on fitness selection. Reproductive isolation is recognized as the final step, or a product of, speciation. Instead, we ask reviewers to imagine reproductive isolation as the first step. What would happen if chromosomal rearrangements like inversion and translocation compromised meiosis due to incompatibility in two homologous chromosomes? Infertility or subfertility. Depending on the severity of subfertility, the generation of a reproductively isolated homozygous population is possible within a few generations. Then, consider the possibility of the breakpoints of a rearrangement also creating changes to long-range enhancers, leading to gene expression changes. Depending on the gene expression changes, phenotypic changes are possible. Finally, what would happen if the new genetically isolated population gained uniqueness, allowing it to take an unoccupied niche that no other species considers livable? The new population would be able to co-exist with the original species. The concept of allelic selection is not applicable when reproductive isolation occurs first. The concept of competition is also not applicable when a new population can immediately take a niche different from the previous species.

 

    Here, we propose an alternative perspective to the neo-Darwinian synthesis. The survival of a new minor population can depend on how different it is from the original population. For example, one eats something no one can eat, or lives in a place no one can live. Intrinsic accidental changes in genes or genomes can cause phenotypic and physiological changes in individuals. If individuals are reproductively isolated simultaneously, their phenotypic traits will be fixed instantaneously, while if not, the traits will be spread into a population. If it is a multigenic trait, the new trait will disappear without reproductive isolation. Only when the uniqueness of a new minor population is sufficient for their continuity can they survive as a new species. A new population survives in a new niche with its unique variation. Unlike competition-based selection, this process does not happen at the expense of the variation. In hindsight, this appears to be an environment selecting a fitter or a new population adapting to the new environment. This is retrospective reasoning but not a prospective logical explanation. Before the accidental intrinsic change occurred, the new environment was not recognized as livable. Evolution is the accidental creation of uniqueness that consequentially supports a population’s survival – survival in uncharted frontiers, not necessarily in competition.

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    The DNA sequence is intrinsically unstable, as proposed in the neutral theory by Motoo Kimura. Despite its instability, the anatomical properties of each species are generally stable. On the other hand, new species or new forms suddenly emerge in fossil records – known as the punctuated equilibria. Is this due to the incompleteness of fossil records? How are the differences in phyla or classes explained? As Goldschmidt proposed, macroevolution is a distinct event from microevolution. We propose that chromosomal rearrangement can cause saltational speciation due to meiosis block, and macroevolution because of alteration in long-range enhancers. Punctuated equilibria could be explained with macroevolution and the availability of uncharted niches. Because macroevolution is not a slow, gradual process, fundamental revision might be needed in the current evolutionary theory. As the first step, we will investigate the link between chromosomal rearrangement and its phenotypic consequence. Through our project, we will seek to identify additional widespread links between large genomic variation and the development of species/class/phylum-defining traits.

 

    We recognize the magnitude of our proposal's controversy and potential impacts on society because the concept of natural selection and gradualism is widely integrated into many disciplines, not limited to biology, but also philosophy, psychology, sociology, economy and so on. To succeed in establishing our hypothesis as a plausible theory, our project must apply the most rigorous approaches and current molecular genetic/genomic tools, combined with expertise in vertebrate development, evolution and computational genome analysis, to ensure any results that we produce that challenge entrenched concepts of natural selection and gradualism can be taken seriously by experts and laypeople alike. Our proposal does not aim to develop technologically new bench experiments. Instead, we want to build a new perspective. We have thoughtfully reevaluated the available observations and realized a possible reconstruction of the fundamental idea in biology and society.