A new approach to identifying drivers of local adaptation
Using Connectivity To Identify Climatic Drivers Of Local Adaptation
Recommendation: posted 05 October 2017, validated 05 October 2017
Local adaptation, the higher fitness a population achieves in its local “home” environment relative to other environments is a crucial phase in the divergence of populations, and as such both generates and maintains diversity. Local adaptation is enhanced by selection and genetic variation in the relevant traits, and decreased by gene flow and genetic drift.
Demonstrating local adaptation is laborious, and is typically done with a reciprocal transplant design , documenting repeated geographic clines [e.g. 2, 3] also provides strong evidence of local adaptation. Even when well documented, it is often unknown which aspects of the environment impose selection. Indeed, differences in environment between different sites that are measured during studies of local adaptation explain little of the variance in the degree of local adaptation . This poses a problem to population management. Given climate change and habitat destruction, understanding the environmental drivers of local adaptation can be crucially important to conducting successful assisted migration or targeted gene flow.
In this manuscript, Macdonald et al.  propose a means of identifying which aspects of the environment select for local adaptation without conducting a reciprocal transplant experiment. The idea is that the strength of relationships between traits and environmental variables that are due to plastic responses to the environment will not be influenced by gene flow, but the strength of trait-environment relationships that are due to local adaptation should decrease with gene flow. This then can be used to reduce the somewhat arbitrary list of environmental variables on which data are available down to a targeted list more likely to drive local adaptation in specific traits. To perform such an analysis requires three things: 1) measurements of traits of interest in a species across locations, 2) an estimate of gene flow between locations, which can be replaced with a biologically meaningful estimate of how well connected those locations are from the point of view of the study species, and 3) data on climate and other environmental variables from across a species’ range, many of which are available on line.
Macdonald et al.  demonstrate their approach using a skink (Lampropholis coggeri). They collected morphological and physiological data on individuals from multiple populations. They estimated connectivity among those locations using information on habitat suitability and dispersal potential , and gleaned climatic data from available databases and the literature. They find that two physiological traits, the critical minimum and maximum temperatures, show the strongest signs of local adaptation, specifically local adaptation to annual mean precipitation, precipitation of the driest quarter, and minimum annual temperature. These are then aspects of skink phenotype and skink habitats that could be explored further, or could be used to provide background information if migration efforts, for example for genetic rescue  were initiated. The approach laid out has the potential to spark a novel genre of research on local adaptation. It its simplest form, knowing that local adaptation is eroded by gene flow, it is intuitive to consider that if connectivity reduces the strength of the relationship between an environmental variable and a trait, that the trait might be involved in local adaptation. The approach is less intuitive than that, however – it relies not connectivity per-se, but the interaction between connectivity and different environmental variables and how that interaction alters trait-environment relationships. The authors lay out a number of useful caveats and potential areas that could use further development. It will be interesting to see how the community of evolutionary biologists responds.
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 Huey RB, Gilchrist GW, Carlson ML, Berrigan D and Serra L. 2000. Rapid evolution of a geographic cline in size in an introduced fly. Science, 287: 308-309. doi: 10.1126/science.287.5451.308
 Milesi P, Lenormand T, Lagneau C, Weill M and Labbé P. 2016. Relating fitness to long-term environmental variations in natura. Molecular Ecology, 25: 5483-5499. doi: 10.1111/mec.13855
 Hereford, J. 2009. A quantitative survey of local adaptation and fitness trade-offs. The American Naturalist 173: 579-588. doi: 10.1086/597611
 Macdonald SL, Llewelyn J and Phillips BL. 2017. Using connectivity to identify climatic drivers of local adaptation. bioRxiv, ver. 4 of October 4, 2017. doi: 10.1101/145169
 Macdonald SL, Llewelyn J, Moritz C and Phillips BL. 2017. Peripheral isolates as sources of adaptive diversity under climate change. Frontiers in Ecology and Evolution, 5:88. doi: 10.3389/fevo.2017.00088
 Whiteley AR, Fitzpatrick SW, Funk WC and Tallmon DA. 2015. Genetic rescue to the rescue. Trends in Ecology & Evolution, 30: 42-49. doi: 10.1016/j.tree.2014.10.009
Ruth Arabelle Hufbauer (2017) A new approach to identifying drivers of local adaptation. Peer Community in Evolutionary Biology, 100034. 10.24072/pci.evolbiol.100034
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 #1
DOI or URL of the preprint: 10.1101/145169
Version of the preprint: 1
Author's Reply, 24 Aug 2017
Decision by Ruth Arabelle Hufbauer, posted 28 Jun 2017
Dear Dr. Macdonald and colleagues,
I really like your basic idea for refining hypotheses regarding local adaptation without doing reciprocal transplants – it is clever and makes a potentially important conceptual advance, which has excellent potential for application. If you are able to address the points made in the reviews, some of which are fairly substantial issues, I would consider recommending it on PCI Evol Biol (i.e. this is a decision akin to “major revision”). The Thomas Lenormand pointed out that clines can arise from historical/biogeographic events, and not reflect local adaptation, phenotypic plasticity or behavioral tracking. In addition to the four other concerns presented, make sure not to loose track of that. I hope you find the PCI process valuable. Thank you for submitting your work for review.
Best, Ruth Hufbauer