Speciation and adaptation in Antarctic sea spiders: Assessing the relative importance of genetic drift and natural selection using comparative population genomic and morphological approaches
Final Report Abstract
This project aimed at testing competing hypotheses underlying frequent speciation processes in Southern Ocean benthic invertebrates. The cold waters around Antarctica host a rich and highly endemic benthic fauna. Recent studies have found that many of these species consist of groups of discrete genetic clades interpreted as previously unrecognized species that radiated in the Pleistocene. These “cryptic” species can be distinguished with molecular methods (e.g. DNA barcoding) and in some cases with meticulous morphological analyses. Typically, the speciation events are interpreted as being driven by recent glaciations. The assumption is that speciation occurred “by chance” when formerly large populations were isolated into small allopatric refugia during glacial maxima, where they were then subjected to the strong effects of random genetic drift. Alternative models of speciation are rarely explored due to previous limitations in molecular techniques. Studies from other ecosystems suggest that ecological speciation, i.e., divergence due to strong differential selection, is one obvious alternative model. In the present project, high-resolution morphological and morphometric data are combined together with genome-wide information derived from target hybrid enrichment to study patterns of genetic drift and selection in a particularly successful group of Southern Ocean benthic species: the sea spiders (Pycnogonida). Building on our earlier studies, we analysed patterns of neutral and non-neutral variation in the two species flocks, Colossendeis megalonyx and Pallenopsis patagonica. These two sea spider species complexes are good models because in particular they consist of many genetically divergent “cryptic” species, and are broadly distributed. First, we provided large morphological information about phenotypic traits in the different genetic lineages as well as large genetic data sets (827 single-copy genes for Pallenopsis patagonica, 1607 for Colossendeis megalonyx). Based on this we could delineate further cryptic species and characterise them morphologically. While this was possible for several of the Pallenopsis species, delineation was difficult for several of the cryptic Colossendeis species due to overlapping, i.e. non-diagnostic traits. For Pallenopsis, we could successfully describe two new species: Pallenopsis aulaeturcarum sp. nov. Dömel and Melzer 2019 and Pallenopsis obstaculumsuperavit sp. nov. Dömel 2019. Only with genome-wide data it was possible to clarify the so-far controversial species status of Colossendeis megalonyx clades reported in earlier studies. The new data showed that within single clades delineated by the nuclear ITS-1 gene several species exist (e.g. clades E1 and D1 - distinct). Furthermore, within these species, gene flow among geographically distinct populations is basically absent. This adds important insights into mobility of Colossendeis individuals and shows that speciation may be facilitated due to the lack of gene pool homogenisation. Using different tests of selection on protein-coding genes we could find several genes under selection, yet none that would explain adaptive speciation in sibling species pairs. Divergence of co-occurring species was not significantly larger than for allopatrically occurring species, which would have been expected according to ecological character displacement to minimize interspecific competition. Therefore, based on both the morphological and genomic variation that we screened in this project in extremely great detail, we could not find any conclusive proof for ecological speciation.
Publications
- (2015) Regional differentiation and extensive hybridisation between mitochondrial clades of the Southern Ocean giant sea spider Colossendeis megalonyx. Royal Society open science 2: 140424
Dietz L, Arango C, Dömel JS, Halanych KM, Harder AM, Held C, Mahon AR, Mayer C, Melzer RR, Rouse G, Weis A, Wilson N, Leese F
(See online at https://doi.org/10.1098/rsos.140424) - (2017) Comparative study of bisected proboscides of Pycnogonida, Organisms, Diversity and Evolution 17: 121-135
Wagner P, Dömel JS, Hofmann M, Hübner J, Leese F, Melzer RR
(See online at https://doi.org/10.1007/s13127-016-0310-6) - (2017) Nuclear and mitochondrial gene data support recent radiation within the sea spider species complex Pallenopsis patagonica (Hoek, 1881). Frontiers Ecology and Evolution 4: 139
Dömel JS, Melzer RR, Harder A, Mahon A, Leese F
(See online at https://doi.org/10.3389/fevo.2016.00139) - (2018) Feeding ecology in sea spiders (Arthropoda: Pycnogonida): What do we know? Frontiers in Zoology 15: 7
Dietz L, Dömel JS, Leese F, Lehmann T, Melzer RR
(See online at https://doi.org/10.1186/s12983-018-0250-4) - (2019) Combining morphological and genomic evidence to resolve species diversity and study speciation processes of the Pallenopsis patagonica (Pycnogonida) species complex. Frontiers in Zoology,16:36
Dömel JS, Macher T-H, Dietz L, Duncan S, Mayer C, Rozenberg A, Wolcott KA, Leese F, Melzer RR
(See online at https://doi.org/10.1186/s12983-019-0316-y) - (2019) Phylogenomics of the longitarsal Colossendeidae: The evolutionary history T of an Antarctic sea spider radiation, Molecualr Phylogenetics and Evolution, 136, 206-214
Dietz L, Dömel, JS, Leese F, Mahon, AR, Mayer, C
(See online at https://doi.org/10.1016/j.ympev.2019.04.017) - (2020) Analyzing drivers of speciation in the Southern Ocean using the sea spider species complex Colossendeis megalonyx as a test case. Polar Biology, 43: 319-342
Dömel JS, Dietz L, Macher T-H, Rozenberg A, Mayer C, Spaak JM, et al.
(See online at https://doi.org/10.1007/s00300-020-02636-z)
