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Principal coordinates analysis (PCoA) among Asian species of Artemia based on SSR markers. using nine (A) and five (B) loci. URM, A. urmiana; SIN, A. sinica; TIB, A. tibetiana; AMA; A. amati n. sp.; SOR, A. sorgeloosi n. sp..
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Species of Artemia are regionally endemic branchiopod crustaceans composed of sexual species and parthenogenetic lineages, and represent an excellent model for studying adaptation and speciation to extreme and heterogeneous hypersaline environments. We tested hypotheses of whether populations from the Tibetan Plateau belong to A. tibetiana Abatzopo...
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... Native Artemia species occur on all continents except Australia and Antarctica (Ruebhart et al. 2008;Muñoz and Pacios 2010); however, Parartemia is endemic to Australia. Although much more widespread, Artemia with nine sexually reproducing species plus a range of parthenogens (Rogers 2013;Asem et al. 2023aAsem et al. , 2023b appears to have far fewer species than Parartemia, which has eighteen described morphospecies (Timms 2014). ...
... Australocypris with 10 species is the most species-rich genus in Mytilocypridinae giant ostracods (Rahman 2024). Parartemia is much more species-rich than Artemia, which only has nine recognised species even though Artemia is essentially globally distributed (Rogers 2013;Asem et al. 2023b). Compared to Artemia, speciation in Parartemia is likely facilitated by their heavy, sinking resting eggs, which tend to retard dispersal (McMaster et al. 2007;). ...
Australian salt lakes contain a diverse range of endemic invertebrates. The brine shrimp Parartemia is among the most speciose and salt-tolerant of these invertebrates. The morpho-taxonomy of Parartemia is well established but there has only been limited molecular assessment of the phylogenetic relationships and boundaries of the morphospecies. We used multiple genetic markers (nuclear 28S and mitochondrial 16S and COI) and tree-building methods (Bayesian inference and maximum likelihood) to investigate the phylogeny of Parartemia. We also used species delimitation methods to test the validity of morphological species designations. The data set included all but 2 of the 18 described Parartemia morphospecies, collected from a total of 93 sites from across southern Australia plus some sequences from GenBank. The results identified large amounts of molecular divergence (e.g. COI P-values of up to 25.23%), some groups of closely related species (which also usually shared some morphological similarities) and some distinctive species, although the relationships among divergent lineages were generally not well resolved. The most conservative set of results from the species delimitation analyses suggests that the morphotaxonomy is largely accurate, although many morphospecies comprised divergent genetic lineages separated by COI P-values of up to 17.02%. Two putative new morphospecies, three cryptic species and one synonymy were identified. Our findings improve the knowledge of Parartemia taxonomy and will facilitate the development of future studies and conservation of this taxon.
... 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. ...
... 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). ...
... Thus, Artemia is among the few cases where sexual and asexual forms may coexist in time and sometimes in the same region (Kobayashi et al. 2013), though often sexual forms are adapted to specific environments (salt lakes and solar salt ponds). So, Artemia species (sexual forms) have regionally endemic dispersal patterns (Asem et al. 2023(Asem et al. , 2024, while parthenogenetic lineages (asexual forms) are widely distributed in the Old World (Amat 1980, Hontoria and Amat 1992a, Amat et al. 1995, Triantaphyllidis et al. 1997a, Sun et al. 1999, Maniatsi et al. 2011, Hontoria et al. 2012, Maccari et al. 2013a, b, Asem and Sun 2014a, b, Asem et al. 2016 and Australia (Timms 2012, 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 brine shrimp Artemia is an aquatic crustacean that is widely distributed worldwide, except in Antarctica [1][2][3][4]. Currently, nine species have been reported in the genus Artemia, including the newly reported species [5]. Three species of the genus, A. franciscana, A. monica, and A. persimilis, are native to the American Continent (New World), while Eurasia, Africa, and Australia (Old World) contain the other six sexual species alongside many obligate parthenogenetic lineages [2,[5][6][7][8][9][10]. ...
... Currently, nine species have been reported in the genus Artemia, including the newly reported species [5]. Three species of the genus, A. franciscana, A. monica, and A. persimilis, are native to the American Continent (New World), while Eurasia, Africa, and Australia (Old World) contain the other six sexual species alongside many obligate parthenogenetic lineages [2,[5][6][7][8][9][10]. Halophilic Artemia mainly inhabits coastal or inland salt lakes and is a keystone species in the food web of hypersaline ecosystems, where prokaryotes are relatively abundant and eukaryotes are rare [11,12]. ...
... Trinity v2.8. 5 Grabherr et al. [117] https://github.com/trinityrnaseq/trinityrnaseq Program to Assemble Spliced Alignments (PASA) v2.5.1 ...
... List of studied Artemia species and parthenogenetic lineages, their provenance and egg bank accession. a Artemia Reference Center, b referred to " Cai (1989a)" c Ocean University of China, d Institute of Aquaculture Torre de la Sal, e Geographic data only refer to Kazakhstan (see Asem et al., 2023), f Hainan Tropical Ocean University, g geographic coordinates only refer to Buenos Aires, this sample has been registered under ARC1321 from an unknown locality in Buenos Aires (Mahieu, personal communication, 2023). Eggs were cultured following Hontoria & Amat (1992a). ...
... Eggs were cultured following Hontoria & Amat (1992a). Only females were sequenced after reproduction mode confirmation by individual culture (Asem et al., 2021b(Asem et al., , 2023, as in most Old-World populations, Artemia species and parthenogenetic lineages may coexist and diploid parthenogens may produce rare males (see Saleem et al., 2019). Ploidy levels were determined by karyotyping using cloned nauplii . ...
... X69067; Perez et al., 1994) served as a reference sequence to assemble that of the A. salina and American species. Bowtie v2.2.9 software (Langmead & Salzberg, 2012) and Geneious R9.1 software (Kearse et al., 2012) were used for sequence mapping and reference-based assembly respectively, with parameter settings as in Asem et al. (2023). To confirm mitogenome sequence validity (circular sequences), each mitogenome was assembled twice and considered in two different positions with a 5,000 bp difference. ...
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. ...
... 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. ...
... 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. However, morphological variability in different ecological conditions (Asem et al. 2023), the lack of gene or genomic analysis underlying reproductive isolation (Wu and Ting 2004), and the heterogeneity of brines complicate taxon Artemia monica Verrill, 1869, endemic to Mono Lake (USA), and Artemia franciscana Kellogg, 1906, a widespread New World species. Artemia monica has been placed on the Red List of Threatened Species by the International Union for Conservation of Nature (IUCN) owing to population decline (IWCSG 1996). ...
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.
... Additional analyses of other Tibetan Plateau sites revealed the occurrence of sexual and parthenogenetic lineages (Zheng and Sun 2013). Recently, A. sorgeloosi from Haiyan Lake (Haiyan Xian, Haibei Tibetan Autonomous Prefecture) was identified and described (Asem et al. 2023). ...
... The Tibetan Plateau is a unique place to study gene level Artemia diversity and divergence. Asem et al. (2023) concluded that the regionally endemic Tibetan species (A. tibetiana and A. sorgeloosi) are monophyletic regarding their nuclear genomes but polyphyletic with respect to mitochondrial markers. ...
... The specific locality information is presented in Table 1. Two parthenogenetic Artemia individuals were reported from Haiyan Lake (Asem et al. 2023) and were also included in this study. Pair-wise geographical distances between lakes are presented in Table 2. ...
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 of hypersaline lakes. Analysis of ten Tibetan salt lakes demonstrated the occurrence of two regionally endemic species, A. tibetiana and A. sorgeloosi, with the latter being the dominant species with eight localities. Both species coexist in Jingyu and Jibu lakes, representing the first case of natural distribution overlap between sexual Artemia species. Artemia sorgeloosi exhibits higher genetic diversity and interpopulation differences, a result consistent with the heterogeneity of local salt lakes, local Artemia population demographics, and their adaptive potentials. Significant FST values demonstrate a gene flow barrier between A. sorgeloosi populations that is compatible with an “island biogeography” distribution pattern, making the Tibetan Plateau a sort of natural laboratory to study intraspecific population differences. Artemia sorgeloosi and the exotic A. franciscana were found coexisting in Yangnapen Lake, demonstrating the ability of this invasive species to colonize high-altitude inland habitats, and the need to monitor its presence and eventual expansion.
... There are six recognized bisexual species in the genus Artemia: Artemia salina (Linnaeus, 1758); Artemia urmiana Günther, 1899; Artemia franciscana Kellogg, 1906; Artemia persimilis Piccinelli and Prosdocimi, 1968; Artemia sinica Cai, 1989; and Artemia tibetiana Abatzopoulos et al., 1998. A. franciscana and A. persimilis are native to the New World, while the other four species are native to the Old World. Recently, Asem [4] identified two new bisexual species from Kazakhstan and the Qinghai-Tibet Plateau, which were named as A. amati and A. sorgeloosi, respectively. However, little is known about these two species. ...
... The other samples from the JYH, XH and YSH populations clustered with A. amati and an asexual lineage, forming a sister group with A. urmiana. A. sorgeloosi and A. amati are two new bisexual species, identified by Asem [4]. The specimens of A. sorgeloosi and A. amati came from Haiyan Lake in Qinghai, China, and an unknow locality in Kazakhstan. ...
... Accuracy of assignment at the species level for each population. References [4,[6][7][8][9][10]13,24,25,[41][42][43][61][62][63][64][65][66] Data Availability Statement: The CO1 sequences obtained from this study were deposited into the NCBI GenBank (PP093070-PP093156). ...
Artemia is a genus of halophilic zooplanktons comprising bisexual and parthenogenetic forms, which is an important model for investigating adaption to hypersaline ecosystems. The genus Artemia in China comprises four species: A. sinica, A. tibetiana, A. franciscana and A. parthenogenetica. To investigate the evolutionary relationship of bisexual and parthenogenetic Artemia in China, we analyzed the morphometrics and phylogenetics among twenty-two geographical populations in China. We found significant morphological differentiation across different species and strains of Artemia in China, which exhibited a high level of intra-population variation. We also found overlaps in morphological characteristics between populations, which may raise challenges for the classification of Artemia species using traditional morphological methods. A. franciscana, which originated from various regions in America, was generally distributed along the Chinese coastlines through multiple human introductions. Additionally, native Asian clades split into Western and Eastern Lineages during the late Miocene due to the Himalayan orogeny. Within the Western Lineage, A. tibetiana can be grouped into three taxon units: A. tibeitiana, A. sorgeloosi and A. urmiana. We also found that the distribution and genetic structure of A. sinica were influenced by climate oscillations during the Pleistocene, which might play a pivotal role in driving the formation of parthenogenetic strains in the Eastern Lineage. Overall, our study provides new insight into invertebrate evolution under geographical and climatic impacts in hypersaline environments.
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.
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.
The current systematics of the large branchiopod crustaceans are reviewed in relation to other crustacean groups and from class to genus level. Calmanostraca and Diplostraca are raised to superorder, and †Kazacharthra and Notostraca are both treated as orders. Problems and needs regarding the systematics of large branchiopods are presented and discussed, with suggestions for moving forward, stressing the need for modern methods and defensible taxonomic definitions. Subdividing taxonomic categories may or may not be warranted, but should never be based on only one gene, or on limited taxon sampling. Furthermore, splitting species out as new genera, when the original genus is poorly defined can only lead to future problems.
