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Ecol Evol
2021 Dec 01;1123:17428-17446. doi: 10.1002/ece3.8376.
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Evolutionary innovations in Antarctic brittle stars linked to glacial refugia.
Lau SCY
,
Strugnell JM
,
Sands CJ
,
Silva CNS
,
Wilson NG
.
Abstract
The drivers behind evolutionary innovations such as contrasting life histories and morphological change are central questions of evolutionary biology. However, the environmental and ecological contexts linked to evolutionary innovations are generally unclear. During the Pleistocene glacial cycles, grounded ice sheets expanded across the Southern Ocean continental shelf. Limited ice-free areas remained, and fauna were isolated from other refugial populations. Survival in Southern Ocean refugia could present opportunities for ecological adaptation and evolutionary innovation. Here, we reconstructed the phylogeographic patterns of circum-Antarctic brittle stars Ophionotus victoriae and O. hexactis with contrasting life histories (broadcasting vs brooding) and morphology (5 vs 6 arms). We examined the evolutionary relationship between the two species using cytochrome c oxidase subunit I (COI) data. COI data suggested that O. victoriae is a single species (rather than a species complex) and is closely related to O. hexactis (a separate species). Since their recent divergence in the mid-Pleistocene, O. victoriae and O. hexactis likely persisted differently throughout glacial maxima, in deep-sea and Antarctic island refugia, respectively. Genetic connectivity, within and between the Antarctic continental shelf and islands, was also observed and could be linked to the Antarctic Circumpolar Current and local oceanographic regimes. Signatures of a probable seascape corridor linking connectivity between the Scotia Sea and Prydz Bay are also highlighted. We suggest that survival in Antarctic island refugia was associated with increase in arm number and a switch from broadcast spawning to brooding in O. hexactis, and propose that it could be linked to environmental changes (such as salinity) associated with intensified interglacial-glacial cycles.
FIGURE 1. Map of Southern Ocean with sampling locations of Ophionotus victoriae and O. hexactis defined for population genetic analyses. White lines = Antarctic Polar Front (APF) (solid) and southern boundary of the Antarctic Circumpolar Current (dashed). Top left map indicates the distribution of individual samples, blue = sequences generated in this study, gray = GenBank accessions, circles = O. victoriae, square = O. hexactis
FIGURE 2. Median joining haplotype network of Ophionotus victoriae and O. hexactis COI sequences (434 bp, n = 935), separated by (a) species, (b) Antarctic continental shelf and Antarctic islands within the Antarctic Polar Front, and (c) location. Size and colors of circle represent the number of samples and sample locations associated with each haplotype. Black circle = inferred haplotype missing in the dataset. Hatch lines = inferred mutation steps between haplotypes
FIGURE 3. Bayesian skyline plots (BSP; log10 scale) of past effective population size of the Southern Ocean brittle stars Ophionotus victoriae and O. hexactis based on COI sequences. Dashed line represents the time of the last glacial maximum (~20,000 years ago)
FIGURE 4. Visualization of spatial genetic patterns among Ophionotus victoriae samples based on the first three MEMGENE variables (“mgQuick”). Values alongside circles in the legend indicate MEMGENE score values. Circles of similar size and the same color represent individual sequence with similar scores on the MEMGENE axis (i.e., genetic similarities attributed to isolation‐by‐distance between samples). Overall, 46.0% of genetic variation can be explained by spatial scale (adjR
2 = 0.460). (a) MEMGENE1 shows a strong spatial pattern of two genetic clusters distinct to the continental shelf and Antarctic islands near the Antarctic Polar Front which contributes 57.2% of the adjR
2. (b) MEMGEN2 shows the second strongest spatial pattern of connectivity between Amundsen Sea, West Antarctic Peninsula, Scotia Sea and Bouvet Island which contributes 31.8% of the adjR
2. (c) MEMGENE3 shows the third strongest spatial pattern demonstrating structure connecting Scotia Sea, Heard Island and Prydz Bay, which contributes 4.78% of the adjR
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