The complete mitochondrial genome of the intertidal spider (Desis jiaxiangi) provides novel insights into the adaptive evolution of the mitogenome and the evolution of spiders

Abstract

Background Although almost all extant spider species live in terrestrial environments, a few species live fully submerged in freshwater or seawater. The intertidal spiders (genus Desis) built silk nests within coral crevices can survive submerged in high tides. The diving bell spider, Argyroneta aquatica, resides in a similar dynamic environment but exclusively in freshwater. Given the pivotal role played by mitochondria in supplying most energy for physiological activity via oxidative phosphorylation and the environment, herein we sequenced the complete mitogenome of Desis jiaxiangi to investigate the adaptive evolution of the aquatic spider mitogenomes and the evolution of spiders. Results We assembled a complete mitogenome of the intertidal spider Desis jiaxiangi and performed comparative mitochondrial analyses of data set comprising of Desis jiaxiangi and other 45 previously published spider mitogenome sequences, including that of Argyroneta aquatica. We found a unique transposition of trnL2 and trnN genes in Desis jiaxiangi. Our robust phylogenetic topology clearly deciphered the evolutionary relationships between Desis jiaxiangi and Argyroneta aquatica as well as other spiders. We dated the divergence of Desis jiaxiangi and Argyroneta aquatica to the late Cretaceous at ~ 98 Ma. Our selection analyses detected a positive selection signal in the nd4 gene of the aquatic branch comprising both Desis jiaxiangi and Argyroneta aquatica. Surprisingly, Pirata subpiraticus, Hypochilus thorelli, and Argyroneta aquatica each had a higher Ka/Ks value in the 13 PCGs dataset among 46 taxa with complete mitogenomes, and these three species also showed positive selection signal in the nd6 gene. Conclusions Our finding of the unique transposition of trnL2 and trnN genes indicates that these genes may have experienced rearrangements in the history of intertidal spider evolution. The positive selection signals in the nd4 and nd6 genes might enable a better understanding of the spider metabolic adaptations in relation to different environments. Our construction of a novel mitogenome for the intertidal spider thus sheds light on the evolutionary history of spiders and their mitogenomes.

Comparative mitogenomic analyses provide evolutionary insights into the retrolateral tibial apophysis clade (Araneae: Entelegynae)

“…It is widely accepted that Ka/Ks > 1, Ka = Ks, and Ka/Ks < 1 generally represented positive selection, neutral mutation, and purifying selection, respectively (Meiklejohn et al, 2007). The Ka/Ks values for 12 PCGs of all the RTA mitogenomes were far lower than 1, which was seen to be the case in most of the arthropod mitogenomes, i.e., spiders (Li et al, 2021), spider mites (Sun et al, 2018) and insects (Wang et al, 2017;Cao et al, 2019;Chang et al, 2020), suggesting that these genes were evolving under purifying selection. These low Ka/Ks values indicated that purifying selection generally dominated mitogenome evolution of the RTA clade, which may be due to its importance in cellular respiration (Meiklejohn et al, 2007).…”

“…Since the sequencing of the first spider mitogenome ( Habronattus oregonensis ) ( Masta and Boore, 2004 ), 40 complete mitogenomes from 14 families of the RTA clade have been deposited in GenBank (as of March 2022). But relevant studies mainly focused on two characteristics exhibited by the sequenced mitogenomes of spiders, i.e., severely truncated tRNAs ( Masta and Boore, 2008 ; Pons et al, 2019 ) and frequent gene rearrangements ( Kumar et al, 2020 ; Tyagi et al, 2020 ; Li et al, 2021 ). However, other mitogenomic features of the RTA clade (e.g., nucleotide composition, codon usage, and evolutionary patterns) have not been comprehensively analyzed.…”

Adaptability and Evolution of Gobiidae: A Genetic Exploration

“…We used one-way ANOVA and multiple comparison analyses to compare the ω values (a value calculated from a concatenated sequence of 13 mtDNA PCGs and 13 values calculated from 13 mtDNA PCGs). The p -values were corrected using the false discovery rate (FDR) [ 23 ]. The ω values of 1, <1, or >1 in protein-coding sequences may be interpreted as neutral mutation, negative (purifying) selection, or positive (diversifying) selection, respectively.…”

“…We used one-way ANOVA and multiple comparison analyses to compare the ω values (a value calculated from a concatenated sequence of 13 mtDNA PCGs and 13 values calculated from 13 mtDNA PCGs). The p-values were corrected using the false discovery rate (FDR) [23].…”

“…One study found that the mitochondrial genes of killifish in the genus Fundulus, occupying different environments evolved at variable rates, but exhibited very low dN/dS ratios across all lineages of the genus [22]. Li et al (2021) constructed a novel mitogenome for the intertidal spider (Desis jiaxiangi) and found that positive selection signals in the mitogenome might adapt to different environments [23]. Dhar et al (2020) observed positive selection in mtDNA PCGs of intertidal chitons (Mollusca: Polyplacophora), indicating that mtDNA PCGs have a role in metabolic adaptations to different environments [12].…”