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COI phylogeny of Asian Artemia based on Bayesian inference (BI) and Maximum-Likelihood (ML). The number behind major nodes denote posterior probabilities. The Bayesian support values (left) and Maximum-Likelihood bootstrap (right) are shown for each major node. Artemia salina was used as an outgroup. SAL: A. salina, FRA: A. franciscana, SIN: A. sinica, PENTA P.L.: pentaploid parthenogenetic lineage, TETRA P.L.: tetraploid parthenogenetic lineage, URM: A. urmiana, TIB: A. tibetiana, AMA: A. amati, TRI P.L.: triploid parthenogenetic lineage, DI P.L.: diploid parthenogenetic lineage, SOR: A. sorgeloosi (complete information and accession numbers of sequences are available in Table 3 and S1).
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Hypersaline lakes in arid and semi-arid areas are unique ecosystems that harbor unique extremophile organisms, such as Artemia, the paradigmatic example of adaptation to harsh living conditions. We assessed the mitogenomic biodiversity of Artemia species from the Tibetan Plateau, China, a remote and yet minimally disturbed ecosystem with a variety...
Citations
... Three native species inhabit the New World, including Artemia monica Verrill, 1869 (Mono Lake, USA), reproductively isolated by an ecological barrier, e.g. immigrants do not tolerate the water conditions of Mono Lake, and so its taxonomic status awaits more systematic studies (see: Asem et al. 2023Asem et al. , 2024, Artemia franciscana Kellogg, 1906 (North, Central, and South America), and Artemia persimilis Piccinelli and Prosdocimi, 1968 (Chile and Argentina). Six native species occur in the Old World consisting of A. salina (Linnaeus, 1758) (Europe and Africa), Artemia urmiana Günther, 1899 (Urmia Lake, Iran, and the Crimean Peninsula), Artemia sinica Cai, 1989 (Central and East China), Artemia tibetiana Abatzopoulos, Zhang and Sorgeloos, 1998 and Artemia sorgeloosi Asem, Eimanifar, Hontoria, Rogers and Gajardo, 2023 (both in the Tibetan Plateau, China), and Artemia amati Asem, Eimanifar, Hontoria, Rogers and Gajardo, 2023 (Kazakhstan) (Hontoria and Amat 1992a, b, Cohen et al. 1999, Gajardo et al. 2002, Crespo and De los Ríos-Escalante 2004, Gajardo et al. 2004, Asem et al. 2010a, Cohen 2012, 2023, De los Ríos-Escalante and Salgado 2012, Mechaly et al. 2013, Rogers 2013, Asem et al. 2024. ...
... immigrants do not tolerate the water conditions of Mono Lake, and so its taxonomic status awaits more systematic studies (see: Asem et al. 2023Asem et al. , 2024, Artemia franciscana Kellogg, 1906 (North, Central, and South America), and Artemia persimilis Piccinelli and Prosdocimi, 1968 (Chile and Argentina). Six native species occur in the Old World consisting of A. salina (Linnaeus, 1758) (Europe and Africa), Artemia urmiana Günther, 1899 (Urmia Lake, Iran, and the Crimean Peninsula), Artemia sinica Cai, 1989 (Central and East China), Artemia tibetiana Abatzopoulos, Zhang and Sorgeloos, 1998 and Artemia sorgeloosi Asem, Eimanifar, Hontoria, Rogers and Gajardo, 2023 (both in the Tibetan Plateau, China), and Artemia amati Asem, Eimanifar, Hontoria, Rogers and Gajardo, 2023 (Kazakhstan) (Hontoria and Amat 1992a, b, Cohen et al. 1999, Gajardo et al. 2002, Crespo and De los Ríos-Escalante 2004, Gajardo et al. 2004, Asem et al. 2010a, Cohen 2012, 2023, De los Ríos-Escalante and Salgado 2012, Mechaly et al. 2013, Rogers 2013, Asem et al. 2024. Thus, Artemia genetic diversity is distributed in locally adapted sexual populations, facilitated by the ecological heterogeneity of lakes and lagoons, and their island-like (allopatric, i.e. regionally endemic) distribution (Gajardo and Beardmore 2012, Asem et al. 2023, 2024see also: De Meester et al. 2002, Rogers 2015. ...
... Six native species occur in the Old World consisting of A. salina (Linnaeus, 1758) (Europe and Africa), Artemia urmiana Günther, 1899 (Urmia Lake, Iran, and the Crimean Peninsula), Artemia sinica Cai, 1989 (Central and East China), Artemia tibetiana Abatzopoulos, Zhang and Sorgeloos, 1998 and Artemia sorgeloosi Asem, Eimanifar, Hontoria, Rogers and Gajardo, 2023 (both in the Tibetan Plateau, China), and Artemia amati Asem, Eimanifar, Hontoria, Rogers and Gajardo, 2023 (Kazakhstan) (Hontoria and Amat 1992a, b, Cohen et al. 1999, Gajardo et al. 2002, Crespo and De los Ríos-Escalante 2004, Gajardo et al. 2004, Asem et al. 2010a, Cohen 2012, 2023, De los Ríos-Escalante and Salgado 2012, Mechaly et al. 2013, Rogers 2013, Asem et al. 2024. Thus, Artemia genetic diversity is distributed in locally adapted sexual populations, facilitated by the ecological heterogeneity of lakes and lagoons, and their island-like (allopatric, i.e. regionally endemic) distribution (Gajardo and Beardmore 2012, Asem et al. 2023, 2024see also: De Meester et al. 2002, Rogers 2015. In addition to sexual species, parthenogenetic groups exist in specific areas (Barigozzi 1974), such as the Old World and Australia (Sun et al. 1999, Hontoria et al. 2012, Timms 2012, Asem and Sun 2014a, b, 2016, Rogers and Timms 2014). ...
Parthenogenesis is an asexual reproduction mode characterized by the development of a female oocyte without fertilization. From an evolutionary perspective, parthenogenesis seems less successful than the predominant sexual mode, though there are groups in which both reproductive types exist, an example of which is the genus Artemia Leach, 1819. This salt-tolerant crustacean inhabiting hypersaline environments contains regionally endemic sexual species and obligate parthenogenetic groups with different ploidy levels, collectively referred to as Artemia parthenogenetica. Here, we discuss the difficulties of using a common species concept in Artemia Leach, 1819. While sexual species are widespread and fit the Biological Species Concept (BSC), which emphasizes reproductive isolation to maintain species genetic integrity or cohe-siveness, it does not apply to uniparental organisms originating from sexual species with major meiotic changes. We show that different ploidy levels of parthenogenetic Artemia groups with uniform nuclear gene pools are maternally independent genetic entities (or cohesive), collectively and wrongly referred to as Artemia parthenogenetica. Thus, we conclude that 'Artemia parthenogenetica' is an invalid nominal specific name. Additionally, parthenogenetic Artemia groups cannot be considered a form of Artemia species (A. urmiana and/or A. sinica). In conclusion, we recommend using the term 'parthenogenetic lineage(s)' instead of 'parthenogenetic population(s)' to describe asexual Artemia group(s), because in modern population genetics and systematics, the term 'population' refers to interbreeding individuals with sexual reproduction. Furthermore, it clarifies that parthenogenetic lineages of Artemia are native to Mediterranean biodiversity.
... The genus Artemia includes four parthenogenetic lineages distinguished by varying ploidy levels (di-, tri-, tetra-, and pentaploidy) (Asem et al., 2024 b). Barigozzi (1974) described the asexual parthenogenetic forms as "A. ...
... parthenogenetica". Despite the unresolved biological origins of parthenogenetic Artemia, its evolutionary origins have been extensively examined (Asem et al., 2024 b). When analyzing mitochondrial genomic markers, parthenogenetic Artemia is identified as a polyphyletic group (Maniatsi et al., 2011;Asem et al., b, 2024, in contrast to its classification as a monophyletic group based on nuclear genomic markers (Nougué et al., 2015;Rode et al., 2022;Asem et al., 2024 b). ...
... Despite the unresolved biological origins of parthenogenetic Artemia, its evolutionary origins have been extensively examined (Asem et al., 2024 b). When analyzing mitochondrial genomic markers, parthenogenetic Artemia is identified as a polyphyletic group (Maniatsi et al., 2011;Asem et al., b, 2024, in contrast to its classification as a monophyletic group based on nuclear genomic markers (Nougué et al., 2015;Rode et al., 2022;Asem et al., 2024 b). Consequently, asexual Artemia forms cannot be classified as members of a single taxon. ...
In light of the pivotal role of Artemia Leach, 1819 as food in larviculture and fisheries, it becomes imperative to continually reassess its resources and deepen our understanding of its species diversity. Such efforts are essential for the effective management of its commercial exploitation and the promotion of sustainable aquaculture activities. Here we present a comprehensive review of historical documents dating back to the 10th century and contemporary scholarly articles. The findings indicate the existence of 59 sites (natural resources and farming sites) across Iran where Artemia has been recorded. This is a significant increase from the 23 reported in the last checklist in 2016. The data indicate that regional A. urmiana Günther, 1899 occurrences warrant classification as “Critically Endangered” on the “Regional Red List” of Iran. Remarkably, apparently the Bazangan Lake has a natural population of Artemia, probably a consequence of climatic change. We highlight the threat posed to Artemia species diversity by the invasive American brine shrimp A. franciscana Kellogg, 1906, noting its presence in 12 locations compared to 7 in 2016. Preliminary studies suggest that the indigenous parthenogenetic Artemia lineages in Iran exhibit superior production potential when compared to both A. franciscana and the native A. urmiana. In light of these findings, the study recommends prioritizing the utilization of native parthenogenetic Artemia in aquaculture, to conserve Artemia biodiversity.
... Because Artemia species and lineages are regionally distributed and adapted to harsh and ecologically variable conditions, coupled with an island biogeography type distribution of intraspecific diversity (Gajardo et al., 2004;Rogers, 2015;Asem et al., 2023Asem et al., , 2024a, they represent unique conditions for studying evolutionary divergence. Such evolutionary change is likely to be accelerated or affected by climate change and anthropogenic impacts. ...
... Such evolutionary change is likely to be accelerated or affected by climate change and anthropogenic impacts. Consequently, the taxonomic status of some species, particularly of those in places difficult to access (Tibet, Kazakhstan, etc.) or less studied, is subject to debate (Asem et al., 2023(Asem et al., , 2024a. One problem is the uncoupling of evolutionary change at morphological and molecular levels, reflected by the occurrence of "sibling species", e.g., . ...
... The copyright holder for this preprint (which this version posted July 29, 2024. ; https://doi.org/10.1101/2024.07.26.600140 doi: bioRxiv preprint (Muñoz et al., 2010, Maniatsi et al., 2011Maccari et al., 2013a;Eimanifar et al., 2014, Asem et al., 2023, 2024a, and lack of common maternal ancestor, synonymisation of A. tibetiana or A. sorgeloosi with A. urmiana is not supported. Neither do they represent a "species complex". ...
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.
... The anostracan genus Artemia Leach, 1819 (brine shrimp) is widely distributed in insular hypersaline seasonally astatic aquatic habitats in arid and semi-arid regions (Rogers 2015, Asem et al. 2023 and comprises regionally endemic sexual species (Gajardo et al. 2002, Asem et al. 2023, 2024a and parthenogenetic lineages (Asem et al. 2024b). Given the isolation of hypersaline lakes and lagoons and their heterogeneous ecological and ionic composition (brines can be highly variable in chloride, carbonate, and sulphate), Artemia populations are useful models to assess allopatrically and ecologically driven differentiation. ...
Species are fundamental units of nature that need proper identification in order to assess and conserve biodiversity. Artemia is a model crustacean for population analysis and comparison in regionally endemic sexual species and parthenogenetic lineages distributed in hypersaline lakes, lagoons, and solar saltworks scattered in arid and semi-arid areas worldwide. The taxonomy of two American Artemia species has been controversial: Artemia monica Verrill 1869, adapted to the carbonate rich conditions of Mono Lake (California, USA), and Artemia franciscana Kellogg, 1906, a species broadly distributed in the Americas. The former species has been poorly studied despite being listed as threatened on the IUCN Red List. In contrast, the latter has been extensively studied, is broadly distributed in the Americas, and has become established as a non-native invasive species in Europe, Asia, Africa and Australia. Given the need to conserve A. monica, and the intraspecific diversity of invasive A. franciscana, and the local species in areas invaded by this species, we reconsider their biodiversity and taxonomic status currently threatened by synonymization. In conclusion, A. monica and A. franciscana should be treated as two separate species which are ecologically and reproductively isolated.
The brine shrimp Artemia , a crustacean adapted to the extreme conditions of hypersaline environments, comprises nine regionally distributed sexual species scattered (island-like) over heterogeneous environments and asexual (parthenogenetic) lineages with different ploidies. Such sexual and asexual interaction within the genus raises questions regarding the origin and time of divergence of both sexual species and asexual lineages, including the persistence of the latter over time, a problem not yet clarified by the use of single mitochondrial and nuclear markers. Based on the complete mitochondrial genome of all species and parthenogenetic lineages, this article first describes the mitogenomic characteristics (nucleotide compositions, genome mapping, codon usage, and tRNA secondary structure) of sexual species and asexual types and, secondly, it provides a comprehensive updated phylogenetic analysis. Molecular dating and geographical evidence suggest that the ancestral. Artemia taxon originated in the Mediterranean area or South America in ca . 33.97 Mya during the Paleogene Period. The mitogenomic comparisons suggest that the common ancestor of diploid and triploid parthenogenetic lineages ( ca . 0.07 Mya) originated from a historical ancestor ( ca. 0.61 Mya) in the Late Pleistocene. Additionally, the common ancestor of tetraploid and pentaploid parthenogenetic lineages ( ca. 0.05 Mya) diverged from a historical maternal ancestor with A. sinica ( ca . 0.96 Mya) in the early Pleistocene. The parthenogenetic lineages do not share a direct ancestor with any sexual species. The Asian clade ancestor diverged more recently ( ca. 14.27 Mya, Middle Miocene). The mitogenomic characteristics, maternal phylogenetic tree, and especially divergence time prove that A. monica and A. franciscana ( time of divergence ) are two biological species.
The Qinghai-Tibet Plateau is one of the areas the richest in salt lakes and Artemia sites. As a result of climate
warming and wetting, the areas of salt lakes on the plateau have been increasing, and the salinities have
decreased considerably since 1990s. However, the impact of salinity change on the genetic diversity of Artemia is
still unknown. Kyˆebxang Co is the highest (4620 m above sea level) salt lake currently with commercial harvesting of Artemia resting eggs in the world, and harbors the largest Artemia population on the plateau. Its salinity
had dropped from ~67 ppt in 1998 to ~39 ppt in 2019. Using 13 microsatellite markers and the mitochondrial
cytochrome oxidase submit I (COI) gene, we analyzed the temporal changes of genetic diversity, effective
population size and genetic structure of this Artemia population based on samples collected in 1998, 2007 and
2019. Our results revealed a steady decline of genetic diversity and significant genetic differentiation among the
sampling years, which may be a consequence of genetic drift and the selection of decreased salinity. A decline of
effective population size was also detected, which may be relative to the fluctuation in census population size,
skewed sex ratio, and selection of the declined salinity. In 2007 and 2019, the Artemia population showed an
excess of heterozygosity and significant deviation from Hardy-Weinberg Equilibrium (p < 0.001), which may be
associated with the heterozygote advantage under low salinity. To comprehensively understand the impact of
climate warming and wetting on Artemia populations on the plateau, further investigation with broad and
intensive sampling are needed.
