No abstract

Summary1. Deleterious recessive alleles that are masked in outbred populations are predicted to be expressed in small, inbred populations, reducing both individual fitness and population viability. However, there are few definitive examples of phenotypic expression of lethal recessive alleles under inbreeding conditions in wild populations. Studies that demonstrate the action of such alleles, and infer their distribution and dynamics, are required to understand their potential impact on population viability and inform management responses. 2. The Scottish population of red-billed choughs (Pyrrhocorax pyrrhocorax), which currently totals <60 breeding pairs and is of major conservation concern, has recently been affected by lethal blindness in nestlings. We used family data to show that the pattern of occurrence of blindness within and across affected families that produced blind nestlings was exactly 0Á25, matching that expected given a single-locus autosomal lethal recessive allele. Furthermore, the observed distribution of blind nestlings within affected families did not differ from that expected given Mendelian inheritance of such an allele. 3. Relatedness estimates showed that individuals from affected families were not more closely related to each other than they were to individuals from unaffected families that did not produce blind nestlings. Blind individuals tended to be less heterozygous than non-blind individuals, as expected if blindness was caused by the expression of a recessive allele under inbreeding. However, there was no difference in the variance in heterozygosity estimates, suggesting that some blind individuals were relatively outbred. These results suggest carriers of the blindness allele may be widely distributed across contemporary families rather than restricted to a single family lineage, implying that the allele has persisted across multiple generations. 4. Blindness occurred at low frequency (affecting 1Á6% of observed nestlings since 1981). However, affected families had larger initial brood sizes than unaffected families. Such high fecundity of carriers of a lethal recessive allele might reflect overdominance, potentially reducing purging and increasing allele persistence probability. 5. We thereby demonstrate the phenotypic expression of a lethal recessive allele in a wild population of conservation concern, and provide a general framework for inferring allele distribution and persistence and informing management responses.

A population's effective size (N ) is a key parameter that shapes rates of inbreeding and loss of genetic diversity, thereby influencing evolutionary processes and population viability. However, estimating N , and identifying key demographic mechanisms that underlie the N to census population size (N) ratio, remains challenging, especially for small populations with overlapping generations and substantial environmental and demographic stochasticity and hence dynamic age-structure. A sophisticated demographic method of estimating N /N, which uses Fisher's reproductive value to account for dynamic age-structure, has been formulated. However, this method requires detailed individual- and population-level data on sex- and age-specific reproduction and survival, and has rarely been implemented. Here, we use the reproductive value method and detailed demographic data to estimate N /N for a small and apparently isolated red-billed chough (Pyrrhocorax pyrrhocorax) population of high conservation concern. We additionally calculated two single-sample molecular genetic estimates of N to corroborate the demographic estimate and examine evidence for unobserved immigration and gene flow. The demographic estimate of N /N was 0.21, reflecting a high total demographic variance (σ2dg) of 0.71. Females and males made similar overall contributions to σ2dg. However, contributions varied among sex-age classes, with greater contributions from 3 year-old females than males, but greater contributions from ≥5 year-old males than females. The demographic estimate of N was ~30, suggesting that rates of increase of inbreeding and loss of genetic variation per generation will be relatively high. Molecular genetic estimates of N computed from linkage disequilibrium and approximate Bayesian computation were approximately 50 and 30, respectively, providing no evidence of substantial unobserved immigration which could bias demographic estimates of N . Our analyses identify key sex-age classes contributing to demographic variance and thus decreasing N /N in a small age-structured population inhabiting a variable environment. They thereby demonstrate how assessments of N can incorporate stochastic sex- and age-specific demography and elucidate key demographic processes affecting a population's evolutionary trajectory and viability. Furthermore, our analyses show that N for the focal chough population is critically small, implying that management to re-establish genetic connectivity may be required to ensure population viability.

Inbreeding can depress individuals’ fitness traits and reduce population viability. However, studies that directly translate inbreeding depression on fitness traits into consequences for population viability, and further, into consequences for management choices, are lacking. Here, we estimated impacts of inbreeding depression (B, lethal equivalents) across life-history stages for an extinct-in-the-wild species, the sihek (Guam kingfisher, Todiramphus cinnamominus). We then projected population growth under different management alternatives with our B estimates incorporated, as well as without inbreeding depression (B = 0) or with a conventional default B. We found that inbreeding depression severely impacted multiple life-history stages, and directly translated into an effect on population viability under management alternatives. Simulations including our B estimates indicated rapid population decline, whereas projections without inbreeding depression or with default B suggested very gradual population decline. Further, our results demonstrate that incorporation of B across life-history stages can influence management decisions, as projections with our B estimates suggested a need to switch to increased breeding management to avoid species extinction and support wild releases. Our results demonstrate that magnitude of B across life-history stages can translate into demographic consequences, such that incorporation of multiple life-stage B into population models can be important for informed conservation management decision-making.