Demographic effects may affect adaptation to islands
Evolution of immune genes in island birds: reduction in population sizes can explain island syndrome
Recommendation: posted 03 October 2022, validated 02 November 2022
The unique challenges associated with living on an island often result in organisms displaying a specific suite of traits commonly referred to as “island syndrome” (Adler and Levins, 1994; Burns, 2019; Baeckens and Van Damme, 2020). Large phenotypic shifts such as changes in size (e.g. shifts to gigantism or dwarfism, Lomolino, 2005) or coloration (Doutrelant et al., 2016) abound in the literature. However, less obvious phenotypes may also play a key role in adaptation to islands.
One such trait, reduced immune function, has important implications for the future of island populations in the face of anthropogenic-induced changes. Due to lower parasite pressure caused by a less diverse and less virulent parasite population, island hosts may show a decrease in immune defenses (Beadell et al., 2006; Pérez‐Rodríguez et al., 2013). However, this hypothesis has been challenged, as many studies have found ambiguous or conflicting results (Matson, 2006; Illera et al., 2015).
While most previous work has examined various immunological parameters (e.g., antibody concentrations), here, Barthe et al. (2022) take the novel approach of examining molecular signatures of immune genes. Using comparative genomic data from 34 different species of birds the authors examine the ratio of synonymous substitutions (i.e., not changing an amino acid) to non-synonymous substitutions (i.e., changing an amino acid) in innate and acquired immune genes (Pn/Ps ratio). Because population sizes on islands are lower which will affect molecular evolution, they compare these results to data from 97 control genes. Assuming relaxed selection on islands predicts that the difference between the Pn/Ps ratio of immune genes and of control genes (ΔPn/Ps) is greater in island species compared to mainland ones.
As with previous work the authors found that the results differ depending on the category of immune genes. Both forms of innate defense: beta-defensins and Toll-like receptors did not show higher ΔPn/Ps for island populations. As these genes still have a higher Pn/Ps than control genes, the authors argue these results are in line with these genes being under purifying selection but lacking an “island effect”. Instead, the authors argue that demographic effects (i.e., reductions in Ne) may lead to the decreased immunity documented in other studies. In contrast, there was a reduction in Pn/Ps in MHC II genes, known to be under balancing selection. This reduction was stronger in island species and thus the authors argue that this is the only class of genes where a role for relaxed selection can be invoked.
Together these results demonstrate that the changes in immunity experienced by island species are complex and that different categories of immune genes can experience different selective pressures. By including control genes in their study, they particularly highlight the importance of accounting for shifts in Ne when examining patterns of island species evolution. Hopefully, this kind of framework will be applied to other taxa to determine if these results are widespread or more specific to birds.
Adler GH, Levins R (1994) The Island Syndrome in Rodent Populations. The Quarterly Review of Biology, 69, 473–490. https://doi.org/10.1086/418744
Baeckens S, Van Damme R (2020) The island syndrome. Current Biology, 30, R338–R339. https://doi.org/10.1016/j.cub.2020.03.029
Barthe M, Doutrelant C, Covas R, Melo M, Illera JC, Tilak M-K, Colombier C, Leroy T, Loiseau C, Nabholz B (2022) Evolution of immune genes in island birds: reduction in population sizes can explain island syndrome. bioRxiv, 2021.11.21.469450, ver. 4 peer-reviewed and recommended by Peer Community in Evolutionary Biology. https://doi.org/10.1101/2021.11.21.469450
Beadell JS, Ishtiaq F, Covas R, Melo M, Warren BH, Atkinson CT, Bensch S, Graves GR, Jhala YV, Peirce MA, Rahmani AR, Fonseca DM, Fleischer RC (2006) Global phylogeographic limits of Hawaii’s avian malaria. Proceedings of the Royal Society B: Biological Sciences, 273, 2935–2944. https://doi.org/10.1098/rspb.2006.3671
Burns KC (2019) Evolution in Isolation: The Search for an Island Syndrome in Plants. Cambridge University Press, Cambridge. https://doi.org/10.1017/9781108379953
Doutrelant C, Paquet M, Renoult JP, Grégoire A, Crochet P-A, Covas R (2016) Worldwide patterns of bird colouration on islands. Ecology Letters, 19, 537–545. https://doi.org/10.1111/ele.12588
Illera JC, Fernández-Álvarez Á, Hernández-Flores CN, Foronda P (2015) Unforeseen biogeographical patterns in a multiple parasite system in Macaronesia. Journal of Biogeography, 42, 1858–1870. https://doi.org/10.1111/jbi.12548
Lomolino MV (2005) Body size evolution in insular vertebrates: generality of the island rule. Journal of Biogeography, 32, 1683–1699. https://doi.org/10.1111/j.1365-2699.2005.01314.x
Matson KD (2006) Are there differences in immune function between continental and insular birds? Proceedings of the Royal Society B: Biological Sciences, 273, 2267–2274. https://doi.org/10.1098/rspb.2006.3590
Pérez-Rodríguez A, Ramírez Á, Richardson DS, Pérez-Tris J (2013) Evolution of parasite island syndromes without long-term host population isolation: parasite dynamics in Macaronesian blackcaps Sylvia atricapilla. Global Ecology and Biogeography, 22, 1272–1281. https://doi.org/10.1111/geb.12084
Emma Berdan (2022) Demographic effects may affect adaptation to islands. Peer Community in Evolutionary Biology, 100153. https://doi.org/10.24072/pci.evolbiol.100153
The recommender in charge of the evaluation of the article and the reviewers declared that they have no conflict of interest (as defined in the code of conduct of PCI) with the authors or with the content of the article.
Evaluation round #2
DOI or URL of the preprint: https://doi.org/10.1101/2021.11.21.469450
Version of the preprint: 2
Author's Reply, 27 Sep 2022
Decision by Emma Berdan, posted 09 Sep 2022, validated 12 Sep 2022
I want to apologize again for the delay, I had to find a chunk of time to make extensive comments on the paper. Overall, I find that the authors did a great job of responding to the reviewer comments and improving the technical aspects of the paper. However, I still think that the readability needs to be improved and agree with the suggestions of reviewer 3. In addition, I attach an edited and noted copy that I have worked on with several questions as well as edits. In particular, the tense issue needs to be addressed as the manuscript switches between past and present tense. These are all superficial issue and can be easily addressed. I think having the manuscript read by a native speaker again before submission could be helpful as well. I am excited to see the next (and final) version of this manuscript!
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Reviewed by Steven Fiddaman, 22 Jul 2022
Reviewed by anonymous reviewer, 29 Aug 2022
Reviewed by anonymous reviewer, 16 Aug 2022
Evaluation round #1
DOI or URL of the preprint: https://doi.org/10.1101/2021.11.21.469450
Version of the preprint: 1
Author's Reply, 03 Jul 2022
Decision by Emma Berdan, posted 07 Mar 2022, validated 08 Mar 2022
I want to apologize for the delay with this decision; it was very difficult to find reviewers. The preprint has now been read by four reviewers and myself. All of us found merit in the study but there are several issues that should be addressed before publication.
By far the biggest issue raised is that the authors used different species for the island vs. mainland. This means that species itself is confounded with island vs. mainland and it seems that the phylogenetic distribution is skewed as well. This issue needs to be addressed up front.
Furthermore, several methodological questions need to be clarified such as sampling strategy and choice of “control genes”. Finally, the reviewers had a number of minor comments will improve readability that should be addressed as well. In addition, I had some comments that follow below. I look forward to reading a revised version of this manuscript.
Species names should always be in italics.
Lines 128-150 - This section is somewhat convoluted and it is hard to understand what your predictions are.
Figure 2 - The same color (purple) should not refer to different groupings in the two figures (A and B). This is confusing for the reader.
I found table 3 very difficult to read. Please re-do the formatting.