One-way ticket to the blue: A large-scale, dated phylogeny revealed asymmetric land-to-water transitions in acariform mites (Acari: Acariformes)

Highlights

• The densest taxonomic coverage to date is employed to infer the phylogeny of mega-diverse Acariformes mites, including 150 families (367 terminals).

• Worm-like mites Nematalycidae and Eriophyoidea are unambiguously recovered as a clade. Tenneriffidae was grouped with Eleuthrengona.

• Inter-realm land–water transitions were directed, with most transitions occurred from terrestrial to aquatic habitats, but not back. A single possible exception was the freshwater ancestor of the Halacaroidea-Parasitengona clade, leading to a water-to-land transitions in terrestrial Parasitengona.

• In many lineages, colonization of the sea occurred via a freshwater ancestor.

• Most transitions were not related to mass extiction events, but some were linked to changes in configurations / drying out of ancient seas.

Abstract

Acariform mites are an ancient and megadiverse lineage that may have experienced a complex pattern of invasions into terrestrial and aquatic habitats. These among-realm transitions may relate to periods of turmoil in Earth’s history or be simply results of uneven biodiversity patterns across habitats. Here, we inferred a dated, representative acariform phylogeny (five genes, 9,200 bp aligned, 367 terminals belonging to 150 ingroup plus 15 outgroup families, 23 fossil calibration points) which was used to infer transitions between marine/freshwater/terrestrial habitats. We detected four unambiguous transitions from terrestrial to freshwater habitats (Hydrozetes, Naiadacarus, Fusohericia, Afronothrus, Homocaligus); one from freshwater to marine (Pontarachnidae), and four from marine to brackish or freshwater transitions (all among Halacaridae: Acarothrix; Halacarellus petiti; Copidognathus sp.; clade Limnohalacarus + Soldanellonyx + Porohalacarus + Porolohmannella). One transition to the sea was inferred ambiguously with respect to the ancestor being either terrestrial or freshwater (Hyadesiidae), and another must be most carefully examined by adding potential related taxa (Selenoribatidae + Fortuyniidae). Finally, we inferred a single, remarkable transition from aquatic to terrestrial habitats involving early evolution of the large and ecologically diverse lineage: the ancestor of the Halacaridae + Parasitengona clade was probably freshwater given our dataset, thus making terrestrial Parasitengona secondarily terrestrial. Overall, our results suggested a strong asymmetry in environmental transitions: the majority occurred from terrestrial to aquatic habitats. This asymmetry is probably linked to mites’ biological properties and uneven biodiversity patterns across habitats rather than Earth’s geological history. Since the land holds more acariform diversity than water habitats, a shift from the former is more likely than from the latter. We inferred the following relationships: alicid endeostigmatid + eriophyoid (Alycidae, (Nanorchestidae, (Nematalycidae, Eriophyoidea))) being sister group to the remaining Acariformes: (proteonematalycid Endeostigmata, alicorhagiid Endeostigmata, Trombidiformes, Oribatida (including Astigmata)). Trombidiform relationships had several novel rearrangements: (i) traditional Eupodina lacked support for the inclusion of Bdelloidea; (ii) Teneriffidae, traditionally placed among Anystina, was consistently recovered in a clade including Heterostigmata in Eleutherengona; (iii) several lineages, such as Adamystidae, Paratydeidae, Caeculidae and Erythracaridae, were recovered in a large clade along other Anystina and Eleutherengona, suggesting single origins of several fundamental character states, such as the reduction of the cheliceral fixed digit and development of the palpal thumb-claw complex.