Quantitative genetic analyses of Song Sparrows reveal the dark side of gene flow

Genetic variation from immigrant birds contributes to lower juvenile survival.

Gene flow is always good, right? The influx of individuals from neighboring regions leads to more genetic diversity, allowing the population to cope better with environmental changes. It sounds wonderful. The reality, however, is not that straightforward. Gene flow can also have negative effects, as nicely shown by a recent paper in the journal Evolution Letters. The researchers took a quantitative genetic approach to study juvenile survival in a population of Song Sparrows (Melospiza melodia). Before we delve into the findings of this paper, we need a crash course in the mathematics behind quantitative genetics. Take a deep breath and continue reading.

Quantitative Genetics

Most phenotypic traits show a range of variation. With regard to juvenile survival, for example, some individuals will die quickly while others make it into adulthood. This phenotypic variation (VP) is determined by genetic factors (VG), environmental factors (VE) and the interaction between genetics and environment (VEG). Or if we put into a formula:

VP = VG + VE + VEG

Next, let’s focus on the genetic component (VG). This part of the equation can be divided into three terms. The first term – additive genetic variance (VA) – captures the effect of an allele on a particular phenotype, causing it to deviate from the population mean. For example, imagine that a gene occurs in two variants: A and B. Individuals with variant A might show survival rates above the mean, while individuals with variant B survive lower than average. This variation can be captured in the term VA. The other two terms concern interactions between alternative alleles or different genes. The term VD focuses on dominance effects, such as variant X being dominant over variant Y. And the term VI captures interactions between different genes. These terms are less important for this blog post, but I mention them to provide the entire picture. Putting it all together gives this formula:

VG = VA + VD + VI

Splitting it up

Now that we have covered the basics of quantitative genetics, we can explore the findings of this study. The researchers focused on the additive genetic variance (VA) of juvenile survival. The value of VA can provide insights into the average fitness in a population. High values suggest plenty of genetic variation available for adaptation, while low values point to possible constraints. Scientists can calculate VA for particular phenotypes using mathematical “animal models”. I will not go into the details of these models, but you can check this paper for more information. Most models calculate VA for the entire population without taking into account potential population structure. Here, the new study comes into play. Jane Reid and her colleagues decided to split VA into two parts: the genetic variance in the local population (ai) and the genetic variance from immigrant birds (qi). To quantify the genetic difference between local birds and several immigrant populations, the researchers added a factor g to the mix. To put it into a formula (the last one, I promise):

VA = ai + g.qi

Migration-Selection Balance

With all the ingredients in place, we can finally look at the results from the analyses. When focusing on the local population, the breeding value for juvenile survival (ai) increased over time (between 1993 and 2018). In other words, juveniles with local parents had a higher chance of surviving into adulthood. The situation was drastically different from the immigrants. The contribution of immigrant genes lead to decreased breeding values (qi) over the years. This means that juveniles with an immigrant parent had a lower chance of reaching adulthood. The two effects – from the local population and from immigration – counteracted each other, resulting in a stable value for the total additive genetic variance (VA). This situation can be seen as a migration-selection balance where alleles from other populations are removed from the population through the low survival of juveniles.

The breeding values for the local population increase over time (figure A), while the values from immigrants decrease (figure C). Both effects balance each other out in the total additive genetic variance (figure E). Red dots indicate the arrival immigrant birds. From: Reid et al. (2021).

Overestimation

This study nicely shows the potential negative consequences of gene flow. Genetic variation from immigrant birds leads to lower juvenile survival. This effect would not have been apparent if the researchers had not discriminated between local birds and immigrants. Indeed, analyses without the immigrant effect resulted in an overestimation (by 47%) of the additive genetic variance for juvenile survival. The exact mechanisms behind the immigrant effect remain to be determined, but could be related to local adaptation or the dispersal of low-quality individuals. Regardless of the underlying mechanism, these findings highlight the importance of taking population structure into account when running animals models. More accurate fitness estimates will help us better understand the evolutionary changes in wild bird populations.

References

Reid, J. M., Arcese, P., Nietlisbach, P., Wolak, M. E., Muff, S., Dickel, L., & Keller, L. F. (2021). Immigration counter‐acts local micro‐evolution of a major fitness component: Migration‐selection balance in free‐living song sparrows. Evolution Letters, 5(1), 48-60.

Featured image: Song Sparrows (Melospiza melodia) © Frank Schulenburg | Wikimedia Commons

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