Mitogenomic phylogeny and divergence time estimation of Artemia leach, 1819 (Branchiopoda: Anostraca) with emphasis on parthenogenetic lineages

Abstract

Brine shrimp Artemia are extremophile invertebrates with unique adaptations to cope with hypersaline lakes. The genus comprises sexual species and parthenogenetic lineages with different ploidies, and populations exhibit an island biogeography dispersal model and accelerated molecular evolution due to the mutagenic effect of ionic strength variance, which has posed difficulties in shaping species and establishing reliable phylogenetic tree topologies and divergence times. We provide updated Artemia phylogeny and divergence time estimates based on the complete mitochondrial genome, which has proved more precise than partial mitochondrial or nuclear markers. Our analyses clustered the nine sexual species into well-supported clades. The parthenogenetic lineages each originated in different geologic periods, and do not share a direct common ancestor with the sexual species. Therefore, parthenogenetic lineages are the correct term instead of A. parthenogenetica. Phylogenetic trees contain a Long Branch Attraction (LBA) with A. salina and further analyses confirm that the LBA should be considered a true phylogenetic branch. Molecular dating and geographical evidence suggest that the ancestral Artemia taxon most probably originated in the Mediterranean area in ca. 33.97 Mya during the Paleocene Period. Artemia urmiana is the early established species (ca. 0.44 Mya, late Pleistocene), and the oldest ancestral branch included in the lineage of A. persimilis (originating ca. 33.97 Mya) according to estimated divergence times. We found that the Asian clade ancestor was more recently diverged (ca. 14.27 Mya, e Middle Miocene), except for the Asian species A. amati and A. tibetiana, each with distinct ancestors in different geologic periods. Regarding geologic divergence periods and ancestral evolutionary relationships, we conclude that Asian species cannot be considered as species complex.