Human-assisted spread of a maladaptive behavior in a critically endangered bird

PLoS One. 2013 Dec 9;8(12):e79066. doi: 10.1371/journal.pone.0079066. eCollection 2013.

Abstract

Conservation management often focuses on counteracting the adverse effects of human activities on threatened populations. However, conservation measures may unintentionally relax selection by allowing the 'survival of the not-so-fit', increasing the risk of fixation of maladaptive traits. Here, we report such a case in the critically-endangered Chatham Island black robin (Petroica traversi) which, in 1980, was reduced to a single breeding pair. Following this bottleneck, some females were observed to lay eggs on the rims of their nests. Rim eggs left in place always failed to hatch. To expedite population recovery, rim eggs were repositioned inside nests, yielding viable hatchlings. Repositioning resulted in rapid growth of the black robin population, but by 1989 over 50% of all females were laying rim eggs. We used an exceptional, species-wide pedigree to consider both recessive and dominant models of inheritance over all plausible founder genotype combinations at a biallelic and possibly sex-linked locus. The pattern of rim laying is best fitted as an autosomal dominant Mendelian trait. Using a phenotype permutation test we could also reject the null hypothesis of non-heritability for this trait in favour of our best-fitting model of heritability. Data collected after intervention ceased shows that the frequency of rim laying has strongly declined, and that this trait is maladaptive. This episode yields an important lesson for conservation biology: fixation of maladaptive traits could render small threatened populations completely dependent on humans for reproduction, irreversibly compromising the long term viability of populations humanity seeks to conserve.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Birds / genetics
  • Birds / physiology*
  • Endangered Species
  • Female
  • Humans
  • Inbreeding
  • Male
  • Phenotype
  • Selection, Genetic / genetics
  • Songbirds / genetics
  • Songbirds / physiology

Grants and funding

Research in 2007–09 was funded by a New Zealand Foundation for Research, Science and Technology fellowship (UOCX0601) to MM. Research in 2010 was supported by the School of Biological Sciences, University of Canterbury and in 2011 by a grant from the Brian Mason Scientific and Technical Trust. AMP is supported by a Royal Society of New Zealand Rutherford Discovery Fellowship, and acknowledges past support of the Royal Swedish Academy of Sciences through a grant from the Knut and Alice Wallenberg Foundation. RS is supported by a Research Chair in Mathematical Models of Biodiversity held by Veolia Environment, the French National Museum of Natural History and Centre for Mathematics and its Applications, Ecole Polytechnique, Palaiseau, France. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.