Shifting evolutionary sands: transcriptome characterization of the Aptostichus atomarius species complex

Abstract

Background: Mygalomorph spiders represent a diverse, yet understudied lineage for which genomic level data has only recently become accessible through high-throughput genomic and transcriptomic sequencing methods. The Aptostichus atomarius species complex (family Euctenizidae) includes two coastal dune endemic members, each with inland sister speciesaffording exploration of dune adaptation associated patterns at the transcriptomic level. We apply an RNAseq approach to examine gene family conservation across the species complex and test for patterns of positive selection along branches leading to dune endemic species. Results: An average of~44,000 contigs were assembled for eight spiders representing dune (n = 2), inland (n = 4), and atomarius species complex outgroup taxa (n = 2). Transcriptomes were estimated to be 64% complete on average with 77 spider reference orthologs missing from all taxa. Over 18,000 orthologous gene clusters were identified within the atomarius complex members, > 5000 were detected in all species, and~4700 were shared between species complex members and outgroup Aptostichus species. Gene family analysis with the FUSTr pipeline identified 47 gene families appearing to be under selection in the atomarius ingroup; four of the five top clusters include sequences strongly resembling other arthropod venom peptides. The COATS pipeline identified six gene clusters under positive selection on branches leading to dune species, three of which reflected the preferred species tree. Genes under selection were identified as Cytochrome P450 2c15 (also recovered in the FUSTr analysis), Niemann 2 Pick C1-like, and Kainate 2 isoform X1. Conclusions: We have generated eight draft transcriptomes for a closely related and ecologically diverse group of trapdoor spiders, identifying venom gene families potentially under selection across the Aptostichus atomarius complex and chemosensory-associated gene families under selection in dune endemic lineages.

Phylogeography and cohesion species delimitation of California endemic trapdoor spiders within the Aptostichus icenoglei sibling species complex (Araneae: Mygalomorphae: Euctenizidae)

“…atomarius species complex based on mitochondrial data plus evidence of adaptive divergence (i.e., coastal dune habitats and lighter abdominal coloration). In a follow‐up study, Garrison et al ( 2020 ) found evidence of chemosensory‐associated gene families under selection in dune endemics compared with their inland sister lineages, further elucidating patterns of ecological differentiation between coastal and inland sister species. Another example within mygalomorphs includes Newton et al ( 2020 ) who initially identified five genetically distinct lineages within the Antrodiaetus unicolor species complex; however, genetic and ecological exchangeability assessments led to the delimitation of three species, not five, based on molecular, behavioral, and morphological data.…”

Microgeographic population structuring in a genus of California trapdoor spiders and discovery of an enigmatic new species (Euctenizidae: Promyrmekiaphila korematsui sp. nov.)

“…Establishing the structure and divergence levels within P . clathrata will facilitate a comparative approach to testing possible ecological and behavioral reproductive barriers (Bond & Stockman, 2008; Chambers et al., 2023; Garrison et al., 2020; Masta & Maddison, 2002; Newton et al., 2020; Starrett et al., 2018).…”

“…No obvious differences in genitalic and somatic morphology occur for males from the two main populations of P. clathrata, but limited sample size prevents more formal analyses . Establishing the structure and divergence levels within P. clathrata will facilitate a comparative approach to testing possible ecological and behavioral reproductive barriers Chambers et al, 2023;Garrison et al, 2020;Masta & Maddison, 2002;Newton et al, 2020;Starrett et al, 2018).…”