Of Brobdingnag and Lilliput, or how the area of an island may determine the size of the bodies and genomes that inhabit it, along with their mutation rates

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Abstract

There are some disputed hypotheses for the recurrent observations of insular gigantism and dwarfism, like the island rule: small organisms would become larger on islands, while large organisms would become smaller. But, why is the latter? In addition, not all the observations fit this rule. Here I propose a causal model. Following the Island Biogeography Theory (IBT), insular aspects influence the census N . Observations suggest that variation in N is associated with variation in effective population size ( N e ). The body size of insular colonisers might change, following Damuth’s law, as N e can decrease at a differential rate from the island area A , resulting in a distinctive effective density . Interestingly, a prediction of the drift-barrier hypothesis is that N e is affecting mutation rates. Consequently, body mass, genome size and µ may be predicted to some extent by island area, as they are influenced by D e and N e . Falsification of the latter hypothesis is feasible by determining changes in genomic features of insular species. We now have the opportunity to interrogate the extensive data available. Here I ask: (i) How is decreasing island area predicting average body sizes? (ii) To which levels does this prediction apply (species, cells, genomes)? (iii) How well does the model fare on predicting µ over paradigmatic case studies? The resolution of these questions may provide a more reliable diagnosis of the evolutionary causes for somatic size variation.

Significance statement

Naturalists have long reported that insular species tend to become unusually large or small compared to their mainland relatives. Despite the familiarity of this “island rule”, there is still no broad mechanistic explanation for why these changes occur so consistently across different groups of organisms. This work proposes that an important neutral factor can be the change in effective density of isolated populations. By combining the expectations of Damuth’s law, the IBT model, and the nearly-neutral theory it offers unified predictions on how sudden constraints in island area can influence not only the evolution of body size, but also the direction of changes in genome size and evolutionary rates.

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