Population-genomic analysis identifies a low rate of global adaptive fixation in the proteins of the cyclical parthenogen Daphnia magna

Type Article
Date 2022-03
Language English
Author(s) Fields Peter D1, McTaggart Seanna2, Reisser CelineORCID3, 4, Haag Christoph3, Palmer William H2, Little Tom J2, Ebert Dieter1, Obbard Darren J2, Lu Jian
Affiliation(s) 1 : University of Basel, Department of Environmental Sciences, Zoology, Vesalgasse 1, Basel, CH-4051, Switzerland
2 : Institute of Evolutionary Biology; School of Biological Sciences University of Edinburgh, Edinburgh, EH9 3JT, United Kingdom
3 : Centre d’Ecologie Fonctionnelle et Evolutive CEFE UMR 5175, Univ Montpellier, CNRS, EPHE, IRD, Univ Paul Valéry Montpellier 3, campus CNRS, 1919, route de Mende, 34293 Montpellier Cedex 5, France
4 : MARBEC, Univ Montpellier, CNRS, IFREMER, IRD, Montpellier, France
Source Molecular Biology And Evolution (0737-4038) (Oxford University Press (OUP)), 2022-03 , Vol. 39 , N. 3 , P. msac048 (18p.)
DOI 10.1093/molbev/msac048
WOS© Times Cited 5
Keyword(s) Daphnia magna, adaptive evolution, arms race, distribution of fitness effects, McDonald-Kreitman, immune genes, RNA interference

Daphnia are well-established ecological and evolutionary models, and the interaction between D. magna and its microparasites is widely considered a paragon of the host-parasite coevolutionary process. Like other well-studied arthropods such as Drosophila melanogaster and Anopheles gambiae, D. magna is a small, widespread, and abundant species that is therefore expected to display a large long-term population size and high rates of adaptive protein evolution. However, unlike these other species, D. magna is cyclically asexual and lives in a highly structured environment (ponds and lakes) with moderate levels of dispersal, both of which are predicted to impact upon long-term effective population size and adaptive protein evolution. To investigate patterns of adaptive protein fixation, we produced the complete coding genomes of 36 D. magna clones sampled from across the European range (Western Palaearctic), along with draft sequences for the close relatives D. similis and D. lumholtzi, used as outgroups. We analyzed genome-wide patterns of adaptive fixation, with a particular focus on genes that have an a priori expectation of high rates, such as those likely to mediate immune responses, RNA interference against viruses and transposable elements, and those with a strongly male-biased expression pattern. We find that, as expected, D. magna displays high levels of diversity and that this is highly structured among populations. However, compared to Drosophila, we find that D. magna proteins appear to have a high proportion of weakly deleterious variants and do not show evidence of pervasive adaptive fixation across its entire range. This is true of the genome as a whole, and also of putative ‘arms race’ genes that often show elevated levels of adaptive substitution in other species. In addition to the likely impact of extensive, and previously documented, local adaptation, we speculate that these findings may reflect reduced efficacy of selection associated with cyclical asexual reproduction.

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Fields Peter D, McTaggart Seanna, Reisser Celine, Haag Christoph, Palmer William H, Little Tom J, Ebert Dieter, Obbard Darren J, Lu Jian (2022). Population-genomic analysis identifies a low rate of global adaptive fixation in the proteins of the cyclical parthenogen Daphnia magna. Molecular Biology And Evolution, 39(3), msac048 (18p.). Publisher's official version : https://doi.org/10.1093/molbev/msac048 , Open Access version : https://archimer.ifremer.fr/doc/00754/86579/