Human-Assisted Spread of a Maladaptive Behavior in a Critically Endangered Bird

<div><p>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 (<i>Petroica traversi</i>) 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.</p></div

Fitness consequences of rim laying behavior.

<p>Data from 2007–11 (during which rim eggs were not repositioned) shows that females that laid rim eggs had a significantly reduced clutch size (i.e. number of eggs laid inside nests that were incubated), and decreased hatching and breeding success compared to normal-laying females. We obtain p-values from likelihood ratio tests with generalized linear mixed models of data with sample size <i>n</i>.</p

Inferred trajectories of allele A under the simple dominant model (model No. 4 in Table 2) between 1980 and 1989.

<p>The mean trajectory is shown by black line and the 50% and 95% confidence sets of the trajectories are shown in decreasing shades of grey. Twice the population size (total number of alleles) is shown by the dashed and dotted line.</p

Pedigree of all black robins breeding between 1980 and 1989.

<p>All individuals are labelled and descend from one breeding pair (A1 and A2). Males are shown as squares. Females that lay rim eggs are shown as red ircles and females that do not lay rim eggs are shown as blue circles (pedigree was generated using Pedigraph <a href="http://www.plosone.org/article/info:doi/10.1371/journal.pone.0079066#pone.0079066-Garbe1" target="_blank">[31]</a>).</p

Model Selection.

<p>Log likelihood and posterior probability of the phenotypes conditional on the pedigree, founder genotypes and model of inheritance. Z is a sex chromosome. The prior probability of each model is uniformly distributed and all other models considered (see text) have zero likelihood.</p