Unraveling the genetic basis of adaptive traits in the endangered Hihi

Are these traits encoded by a few genes or many?

“Adapt, move or die.” That is a topic we discuss in the course Climate Change Ecology which I teach with several colleagues at Wageningen University. When the environment changes, some populations can quickly adapt to the new circumstances. The speed and success of adaptation is partly influenced by the genetic basis of the relevant traits. For example, theoretical work suggests that traits encoded by multiple genes can constrain rapid adaptation. With multiple genomic loci, chances are higher that some variation will be lost due to random processes, such as genetic drift. Moreover, some of these potentially adaptive loci might be linked with deleterious alleles, preventing these loci from increasing in frequency. It is thus important to understand the genetic basis of traits in order to predict their response to selection.

A recent study in the Proceedings of the Royal Society B took a closer look at the hihi (Notiomystis cincta), a small songbird endemic to New Zealand. The small population size of this endangered species makes it vulnerable to the effects of genetic drift. Previous work reported three traits are under selection: tarsus length, body mass and head–bill length. How quickly and efficiently these traits can adapt depends on their genetic basis. Are they encoded by a few genes or many?

Heritability

One way to determine the number of genes underlying is particular trait is to calculate how heritability is distributed across the genome. Heritability refers to the proportion of morphological variation that is explained by genetics. In other words, how much do offspring resemble their parents due to shared genetic variants. This is mostly tested using extensive pedigrees where you can directly compare the morphology of parents and their offspring. In this study, however, the researchers used a genomic relatedness matrix to calculate heritability (you can check out this paper for more details on this method).

Once you have calculated the heritability of a trait, you can check how much each chromosome contributes to this trait. If multiple chromosomes contribute to the genetic variation of a trait, it is likely influenced by multiple genes. In addition, if large chromosomes (which contain more genes) explain a more genetic variation than smaller chromosomes, the trait is probably polygenic.

In the hihi, analyses of the three traits revealed low heritability. It turned out that genetics explains only 13%, 6% and 12% of the morphological variation in tarsus length, body mass and head–bill length, respectively. Moreover, this variation was distributed across several chromosomes, indicating that multiple genes are involved. For two traits (tarsus length and body mass), there was a positive relationship between genetic variation and chromosome size, supporting the conclusion that these traits are influence by multiple genes.

The variation explained by genetic for the three traits is distributed across multiple chromosomes. For two traits (tarsus length and body mass), there is a positive – though not significant – relationship with chromosome size. From: Duntsch et al. (2020) Proceedings B.

Adaptive Potential

A second approach to determine the genetic basis of a trait is a genome-wide association scan (GWAS). This analysis checks which genomic loci are significantly associated with particular traits. If a trait with significant heritability has no significant GWAS peaks, the trait is probably polygenic. The researchers found no genetic variants that were significantly associated with any of the three traits, following the conclusions of the other analyses that these traits are influenced by multiple genes. For each trait, however, there were several genetic variants of interest (despite not being significant). For example, the genetic variant most strongly associated with tarsus length can be found in an intronic region of the HEY2 transcription factor which is involved in embryological development.

The information about the genetic basis of the three traits can help researchers to predict the rate of adaptation of this endangered species, and take appropriate conservation measures. The authors conclude:

We have demonstrated that many loci of small effect are likely to contribute the majority of variation to all three morphological traits. Given the small effective population size of all hihi populations, many adaptive variants are likely to be lost to drift at a rate that is faster than the input of new variation via mutation. This is likely to slow the speed of adaptation and lead to further constraint on the adaptive potential of the species.

References

Duntsch, L., Tomotani, B. M., de Villemereuil, P., Brekke, P., Lee, K. D., Ewen, J. G., & Santure, A. W. (2020). Polygenic basis for adaptive morphological variation in a threatened Aotearoa| New Zealand bird, the hihi (Notiomystis cincta). Proceedings of the Royal Society B287(1933), 20200948.

Featured image: Hihi (Notiomystis cincta) © Judi Lapsley Miller | Wikimedia Commons

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