Rapid morphological evolution in the Silvereye: random processes or selection?

A clever combination of morphological and genomic analyses provide the answer.

Evolution is often depicted as a slow and gradual process that we cannot observe during our lifetime. However, evolutionary changes can happen relatively fast. When a few individuals colonize a new area, they get exposed to novel selective pressures and the population might show rapid morphological changes. In addition, the random sampling effect during the founding event can also speed up evolution. The newly arrived members might be a biased sample from the source population. For example, bigger birds might be more likely to reach an isolated island. It is, however, often extremely difficult to determine whether natural selection or random processes are driving the rapid morphological changes.

One approach is to study a recent colonization event and calculate the Ne* statistic, which was introduced by Lande (1976). This statistic can be applied to a morphological trait and indicates the effective population size that is required to explain morphological shifts by random processes alone. Next, the resulting Ne* can be compared with the actual effective population size (Ne). If this actual population size is larger than the Ne*, then drift is insufficient to explain the morphological changes and selection needs to be invoked.

French Polynesia

Calculating a statistic is relatively straightforward, but where can we find a recent colonization event? In 1937, the aviculturist Eastham Guild introduced the silvereye (Zosterops lateralis) to the island of Tahiti in French Polynesia. The introduced population persisted in low numbers until the late 1950s after which they expanded into all habitat types on the island, and later even dispersed to ten other islands in the archipelago. A recent study in the journal Heredity took advantage of this situation and closely studied morphological evolution of these silvereye populations.

Ashley Sendell-Price and his colleagues measured several morphological traits for almost 200 silvereyes. For each trait, they calculated Lande’s statistic Ne* and compared it with the actual effective population size. These analyses showed that most rapid morphological shifts could be explained by random processes alone. There were, however, some exceptions, such as the morphology of the bill. These exceptions were supported by additional genomic analyses.

Colonisation history of the silvereye across islands of French Polynesia. From Sendell-Price et al. (2020) Heredity.

Candidate Genes

Apart from the morphological analyses, the researchers performed a genomic scan to detect genes under positive selection. This exercise led to a list of 12 candidate genes. Here are the most relevant ones that have been found in other bird species:

  • VPS50: associated with bill length in Berthelot’s pipit (Anthus berthelotii)
  • VPS13B: under directional selection between species of Darwin’s finches
  • NFIA: associated with bill length in the house sparrow (Passer domesticus)
  • PTDSSI: under directional selection in birds of paradise
  • OSR2: experimentally demonstrated to play a role in beak development in birds

The remaining candidate genes (E2F4, FREM2, PBX3, RALGPS1, TMC6 and ZMYND11) are all associated with craniofacial disorders in several non-avian species. Taken together, the morphological and genomic results indicate that the observed morphological shifts within the French Polynesian population of silvereyes are due to a combination of random and selective processes.

Overview of candidate genes under positive selection in different silvereye populations across French Polynesia. From Sendell-Price et al. (2020) Heredity.

References

Sendell-Price, A. T., Ruegg, K. C., & Clegg, S. M. (2020). Rapid morphological divergence following a human-mediated introduction: The role of drift and directional selection. Heredity124(4), 535-549.

Featured image: Silvereye (Zosterops lateralis) © Bernard Spragg | Wikimedia Commons

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