Red-billed choughs are a species of conservation concern, as discussed a recent Journal of Animal Ecology publication investigating their effective population size.  Amanda Trask, lead author of the study, recently finished her PhD at the University of Aberdeen on conservation genetics and demographics of one of the last remaining red-billed chough populations in Scotland, and is currently working as a Research Ecologist with the British Trust for Ornithology.  Here, she tells us about some of her work on choughs and the genetic threats they face.

Effective population size (N_e) is a key parameter in conservation and evolutionary biology because it can provide a measure of how allele frequencies in an observed population may change over time. For conservation biologists, this means that N_e can be used to measure how much genetic variation is expected to be lost over future generations and therefore how viable a population is. For evolutionary biologists, N_e can also be used to estimate the effectiveness of selection relative to genetic drift in a population and therefore what the population’s evolutionary trajectory may be.  However, N_e is a notoriously tricky parameter to estimate for wild populations, in particular those with overlapping generations, and it is even trickier to understand the processes causing or contributing to that population’s N_e.

Our study system – the Scottish red-billed chough population

Red-billed choughs (Pyrrhocorax pyrrhocorax) are a species of conservation concern in Europe and in the UK. In Scotland in particular, there were estimated to be only ~53 breeding pairs left in 2014, with the majority of breeding pairs (46 in 2014) inhabiting the island of Islay in the Hebrides.  It was therefore the Islay chough population which was the focus of our study. From molecular genetic analyses, this population is likely to be isolated, with high genetic differentiation between the Scottish and other British Isles populations. This apparent isolation and small censused population size raises concern that the viability of this population may be at risk from genetic threats stemming from inbreeding and loss of genetic diversity. Indeed, inbreeding depression may already be manifesting in this population, for example through the expression of a large-effect recessive mutation causing blindness in chough nestlings (you can read more about this here).

Our study therefore had two aims: to assess the genetic threats facing one of Scotland’s last remaining chough populations by estimating its N_e and to provide a methodological example of the estimation of N_e in a wild population with not only over-lapping generations but also dynamic age structure.

Estimating N_e

N_e can be estimated using genetic or demographic approaches. Demographic approaches estimate N_e from the causal demographic parameters that generate the observed N_e. These approaches can therefore shed light on the processes causing the observed N_e, which can then be used to directly inform population management. In contrast, genetic estimators of N_e are generally calculated from the resultant effects of N_e on genetic variation, and therefore can’t tell you about the causal demographic processes. However, they can take into account all processes acting on N_e including immigration, low levels of which can otherwise be difficult to detect. To build a comprehensive picture of the N_e of the Islay chough population and understand processes underlying that N_e, we used both demographic and genetic estimators.

The Islay chough population has been monitored since 1981 by the Scottish Chough Study Group and therefore there was unusually detailed individual- and population-level demographic data that we could use in our N_e estimate. From sex-age-specific differences among individuals in their reproductive success and survival, we estimated the demographic variance of the population, and used this to estimate N_e following an approach by Engen et al. 2010.

N_e was estimated to be very low, only ≈30. This was mainly due to the high total demographic variance of the population, such that some breeding pairs of choughs have high reproductive success and the offspring they produce survive to become breeders themselves, while other pairs have low reproductive success and the few offspring they produce die before breeding. Some individuals therefore contribute much more to the ‘gene pool’ of the population than others, which acts to decrease N_e.

Interestingly, we also found that there were age-specific differences between the sexes in contributions to the total demographic variance of the population; younger aged females contributed more to the total demographic variance than younger aged males, while older aged males contributed more to total demographic variance than older aged females.

We also compared our demographic estimate of N_e to two different genetic estimators; linkage disequilibrium (LD), which measures associations between different alleles across sampled individuals, and Approximate Bayesian computation (ABC) using a variety of different genetic summary statistics to estimate N_e. Overall, these two genetic estimators supported our conclusion from the demographic estimator that current N_e is less than 50 and so provide no evidence of recent immigration and gene-flow into Islay’s chough population.

Implications of our study

Our study shows that key sex-age classes can contribute to a population’s total demographic variance and therefore act to decrease N_e in a wild population. Our study therefore demonstrates how assessments of N_e can identify key demographic processes that may affect a population’s evolutionary trajectory and viability, through their impact on N_e.

Our study also has direct relevance to the conservation management of the Islay chough population. From the small N_e estimate, the rate of increasing inbreeding and loss of genetic diversity is predicted to be high (~2% per generation) and this will continue if the population remains isolated. Future population management strategies should therefore consider re-establishing genetic connectivity between the Islay and other UK chough populations alongside continued habitat management, to increase genetic diversity and ensure long-term population viability.

More information:

Trask et al. (2017) Estimating demographic contributions to effective population size in an age-structured wild population experiencing environmental and demographic stochasticity. Journal of Animal Ecology.

Trask et al. (2016) Evidence of the phenotypic expression of a lethal recessive allele under inbreeding in a wild population of conservation concern. Journal of Animal Ecology, 85(4), 879-891.