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Keywords:

  • calcium;
  • island rule;
  • nanism;
  • O matrix;
  • selective agent

Summary

  1. Body size is a defining phenotypic trait, but the ecological causes of its evolution are poorly understood. Most studies have considered only a single putative causal agent and have failed to recognise that different environmental agents are often correlated.
  2. Darwin suggested that although trait variation across populations is often associated with abiotic variation, evolution is more likely to be driven by biotic factors correlated with the abiotic variation. This hypothesis has received little explicit attention.
  3. We use structural equation modelling to quantify the relative importance of abiotic (pH, metal concentrations) and biotic (competition, predation) factors in the evolution of body size in three-spined sticklebacks Gasterosteus aculeatus on the island of North Uist, Scotland. We combine phenotypic data from multiple isolated populations, detailed characterisation of their environment and a common garden experiment that establishes the genetic basis of size differences.
  4. Three-spined sticklebacks on North Uist show almost unprecedented intraspecific evolution of body size that has taken place rapidly (<16 000 years). The smallest fish mature at only 7% of the mass of ancestral, anadromous fish. Dwarfism is associated with reduced abundance of a smaller competitor species, the nine-spined stickleback Pungitius pungitius, and with low pH indicative of poor resource conditions. Dwarfism also tends to occur where an important predator, the brown trout Salmo trutta, is also small. The abundance of P. pungitius and the size of S. trutta are themselves related to underlying abiotic environmental variation.
  5. Despite the close association between abiotic and biotic factors across populations, our results support Darwin's hypothesis that biotic factors, associated with variation in the abiotic environment, are more important in explaining evolution than is abiotic variation per se. This study demonstrates the importance of considering the relationships between environmental variables before conclusions can be drawn about the causes of (body size) evolution on islands.