Multi-generation genetic and fitness effects of immigration in a natural meta-population of song sparrows (Melospiza melodia)

Abstract

Fragmentation leads to smaller habitat patches and population sizes, endangering population fitness and persistence, including through inbreeding depression and loss of genetic diversity. These effects can be mitigated through immigration when immigrants contribute to replenishing local genetic diversity, while also reducing local inbreeding and the resulting expression of inbreeding depression. The concept of genetic rescue relies on these effects in its theoretical predictions and management practice. However, there are also potential negative consequences of immigration, such as loss of local adaptation. In practice, the multi-generational genetic effects of natural immigration, stemming from the fitness of immigrants and their descendants, are not yet well known, precluding informed inferences on the net consequences. Hence, in this thesis, I quantified key multi-generational effects of immigration using long-term data from a system of song sparrows, Melospiza melodia, on Mandarte Island, BC, Canada, where the focal population occasionally receives natural immigrants. Specifically, I tested standard assumptions concerning the relatedness of immigrants to the recipient population (paper I), the fitness consequences of immigration across successive generations (paper II), consequential introgression of immigrant genes in the population (paper III) and potential modulation of such fitness and introgression consequences through non-random mating (paper IV). Specifically, in paper I, I tested the standard assumptions of population genetics, that immigrants are outbred and unrelated to the recipient population at the time of arrival. Using both microsatellites and pedigree inbreeding coefficient f, I showed that immigrants are effectively unrelated to each other and to the local population, and are also outbred relative to the local scale of pedigree inbreeding. These results show that recent immigrants have potential to import novel alleles, decrease local inbreeding, and induce substantial fitness consequences.

In paper II, I quantified the relative fitness of immigrants, natives and their descendants, utilizing line cross theory and planned comparisons to quantify key differences among defined filial groups for multiple major fitness components. I found strong effects, including high relative fitness in the first generation of immigrant-native descendants (F1), and loss of fitness in the second generation (F2), indicating strong heterosis followed by epistatic breakdown. These results indicate strong non-additive genetic effects on fitness, and imply that risks of outbreeding depression in crosses between weakly diverged natural populations should not be ignored.

In paper III, to quantify the expected persistence of immigrants’ genes in the focal population, collaborators and I used long-term pedigree data to estimate genetic contributions of immigrants and natives across up to fifteen years from arrival and recruitment. We showed that female immigrants contributed more than natives, while male immigrants’ lineages went typically rapidly extinct. Further, the high genetic contribution of female immigrants only emerged several years after the immigrants arrived, consistent with heterosisenhanced introgression.

Finally, in paper IV, I tested whether the fitness consequences of immigration were modulated through non-random pairing, and specifically whether F1 individuals paired with natives rather than other F1 individuals, thereby avoiding producing low-fitness F2 offspring. I found that low pairing success of male immigrants was a mechanism underpinning their fitness, with no evidence that F1s avoided each other.

In conclusion, immigrants had major fitness effects, both positive, and negative, and immigrants’ genes persisted over longer ecological time frames (here, 15 years), with strong sex-specific effects. These are surprisingly strong consequences of immigration, given that the focal song sparrow population is relatively well-connected and apparently unlikely to be strongly diverged from surrounding populations. These findings will be relevant to ambitions to understand and predict net genetic and fitness effects of immigration, and help to disentangle the trade-off between the benefits of outbreeding and the loss of local adaptation. Thereby, they can inform genetic rescue considerations and provide conceptual frameworks for estimating and understanding such complex effects in further systems in nature.