Phylogenomics, taxonomy and lifestyle evolution of raft and brood-web spiders (Araneae: Felidae and Araneidae)
Abstract
Pisauridae Simon, 1890 or “nursing web spiders” is a global and heterogeneous assemblage of spider genera with diverse lifestyles, including web-making and non-web-making, terrestrial and semi-aquatic species, notably the “fishing spider” genus Dolomedes Latreille, 1804. Incomplete, unresolved or conflicting phylogenies have so far hindered tests of the monophyly and evolution of the genus Dolomedes and Pisauridae. Here, we broadly address these issues within a phylogenomic and comparative framework. Our goals are i) to reconstruct a robust phylogeny to test the monophyly of the genus Dolomedes and Pisauridae and to revise the classification of Dolomedes, ii) to estimate evolutionary changes and trends in lifestyle and trapping webs, and iii) to evaluate hypotheses regarding the association of morphological characters with the semi-aquatic lifestyle. For this purpose, we generated subgenomic data (ultraconserved elements or UCEs) for 53 Dolomedes species and 28 pisaurid genera. We analyzed these data using maximum likelihood, Bayesian, and multi-species coalescent approaches, as well as two different phylogenetic time calibration methods: RelTime and MCMCtree. Consistent across analytical approaches, our phylogeny rejects the monophyly of both Pisauridae and Dolomedes. The “Pisaurid” genus is divided into three clades: 1) Focal Clade I groups the majority, including Pisaura Simon, 1886, and thus represents true pisaurids; 2) Focal Clade II = Blandinia Tonini et al., 2016 is sister species to Trechaleidae Simon, 1890 and Lycosidae Sundevall, 1833. 3) Focal clade III includes the fishing and raft spider groups Dolomedes, Megadolomedes Davies and Raven, 1980, and Ornodolomedes Raven and Hebron, 2018, and is sister to focal clade II, Trechaleidae, and Lycosidae. Our classification, based on complementary taxa and morphological evidence, resurrects Dolomedidae Simon, 1876 and includes Dolomedes and the marine genera Bradystichus Simon, 1884, Megadolomedes, Caledomedes Raven and Hebron, 2018, Mangromedes Raven and Hebron, 2018, Ornodolomedes, and Tasmomedes Raven and Hebron, 2018. Both RelTime and MCMCtree analyses yielded comparable divergence estimates. The origin of the Pisauridae is estimated to be between 29 and 40 million years ago. Brandinia is dated to 21 to 34 million years ago, Dromedidae to 10 to 17 million years ago, and Dromedidae to 9 to 16 million years ago. Taxon sampling bias correction was performed in all evolutionary analyses to avoid misleading significant correlations and overanalysis of ancestral states. Evolutionary analyses reconstruct a semi-aquatic lifestyle as ancestral to a large clade that includes pisaurids, lycosids, omnivores, brandinia, and dromedids, which has reversed to a terrestrial lifestyle several times. Prey nets have evolved and reversed at least three times. Contrary to expectations, the evolution of lifestyle and prey nets is independent. Leg and tarsus lengths are not indicative of lifestyle, but semi-aquatic taxa are significantly larger than terrestrial ones. This pattern can be explained by a biomechanical threshold at which surface tension is broken when spiders forage in water. Our time-calibration analysis indicates that the evolution of pisaurids from a semi-aquatic ancestor to a terrestrial and web-building lifestyle coincided with a cooling and drying climate during the Middle Miocene. We therefore hypothesize that climatic changes acted as a strong selection pressure towards lifestyle diversification.
Phylogenomics, taxonomy, and lifestyle evolution of raft and brood-web spiders (Araneae: Stonechilidae and Theridiidae) Kuang-Ping Yu, Ren-Chung Cheng, Charles R. Haddad, Akio Tanikawa, Brogan L. Pett, Luis N. Piacentini, Peter Jaeger, Ho Yin Yip, Yuya Suzuki, Arnaud Henrard, Christina J. Painting, Cor J. Vink, Eileen A. Hebets, Mark S. Harvey, Matjaz Kuntner
