Genetic rescue in a severely inbred wolf population

Abstract

Natural populations are becoming increasingly fragmented which is expected to affect their viability due to inbreeding depression, reduced genetic diversity and increased sensitivity to demographic and environmental stochasticity. In small and highly inbred populations, the introduction of only a few immigrants may increase vital rates significantly. However, very few studies have quantified the long-term success of immigrants and inbred individuals in natural populations. Following an episode of natural immigration to the isolated, severely inbred Scandinavian wolf (Canis lupus) population, we demonstrate significantly higher pairing and breeding success for offspring to immigrants compared to offspring from native, inbred pairs. We argue that inbreeding depression is the underlying mechanism for the profound difference in breeding success. Highly inbred wolves may have lower survival during natal dispersal as well as competitive disadvantage to find a partner. Our study is one of the first to quantify and compare the reproductive success of first-generation offspring from migrants vs. native, inbred individuals in a natural population. Indeed, our data demonstrate the profound impact single immigrants can have in small, inbred populations, and represent one of very few documented cases of genetic rescue in a population of large carnivores.

Keywords: Canis lupus; genetic rescue; heterozygosity; immigration; inbreeding; inbreeding depression.

Figure 1

Pedigree of breeding Scandinavian wolves from 1983 to 2012. Ellipses are females, rectangles are males, and diamonds represent litters where no offspring has yet entered the breeding population. The colours represent the inbreeding coefficient f of the individuals and litters (dark blue: 0 ≤ f < 0.1, light blue: 0.1 ≤ f < 0.2, yellow: 0.2 ≤ f < 0.3, orange: 0.3 ≤ f < 0.4, red: 0.4 ≤ f < 0.5, grey: unknown f). Founders, assumed to be nonrelated and thus their offspring f = 0, are nonfilled symbols with a blue frame. The pedigree also contains the identity (numbers) of the 28 wolves (Table S3, Supporting information) included in the 14 target pairs.

Figure 2

Geographic distribution of the original wolf pairs and their descendants. The location of wolf territories in Scandinavia 2008–2012, illustrating wolf pairs that can be traced back to the 14 original pairs (circles) that started to reproduce in 2008. Squares and triangles represent pairs with first‐ (F1) and second‐generation (F2) descendants, respectively, whereas diamonds symbolize pairs with both one F1 and one F2 descendant. Edge‐lined symbols represent breeding pairs. Dark blue represents the original pairs with an immigrant and pairs composed of immigrant descendants with partners descending from inbred pairs other than the 12 in the study. Light blue symbolizes pairs composed by an immigrant descendant and a descendant from one of the 12 inbred families included in the study (i.e. born 2008). Yellow, orange and red, respectively, represent the inbred native pairs with medium (f = 0.2–0.3), high (f = 0.3–0.4) and very high (f > 0.40) inbreeding levels and their descendants.

Figure 3

Pairing and breeding success of offspring to immigrant and inbred pairs. Observed pairing and breeding success of outbred offspring to immigrant wolves (i.e. all have f = 0) and inbred offspring (0.26 < f < 0.49) where both parents are native wolves (A, B; **⇒ P < 0.01), and their probability to establish with a partner and breed in relation to the inbreeding coefficient f (C, D) and standardized heterozygosity stMLH (E, F). In panels C–F, the histograms represent the frequency distribution of f values (C, D) and stMLH values (E, F) among individuals that were successful (upper histogram presented upside down) and unsuccessful (lower histogram) in pairing or breeding. Solid curves represent the success of individuals first identified within the natal territory, and dashed curves represent the success of individuals identified first time outside the birth site, that is postdispersal.

Figure 4

Annual population size and inbreeding levels of first‐time breeding pairs in the Scandinavian wolf population from 1997 to 2012. Population size is the mean census size using yearly direct count estimates from the combination of snow tracking and DNA analysis carried out within the framework of the Scandinavian wolf monitoring programme. Inbreeding levels refer to the inbreeding coefficients of the offspring in litters to first‐time breeding pairs. The angles of the arrows represent the average annual population growth rate (${\overline{\mathrm{\lambda }}}_{\mathrm{p}}$) before and after 2008, when the two immigrants started to breed. The population growth rate is corrected each year for the number of legally shot wolves (see Materials and methods).