A well‐resolved transcriptomic phylogeny of the mite harvestman family Pettalidae (Arachnida, Opiliones, Cyphophthalmi) reveals signatures of Gondwanan vicariance

Abstract

Aim:We explored the extent to which Gondwanan vicariance contributed to the circum-Antarctic distribution of the mite harvestman family Pettalidae, a group of small, dispersal-limited arachnids whose phylogeny has been poorly resolved, precluding rigorous biogeographic hypothesis testing. Location: Continental landmasses of former temperate Gondwana (Chile, SouthAfrica, Sri Lanka, Australia and New Zealand).Taxon: Pettalidae, Opiliones. Methods:We generated transcriptomes for a phylogeny of 16 pettalids, spanning 9 genera. Data were analysed using maximum likelihood, Bayesian inference and coalescence methods. The phylogenetic position of the Sri Lankan genus Pettalus was further explored using quartet likelihood mapping and changes in gene likelihood scores. We also estimated divergence times and looked for signatures of extinction across Antarctica and central Australia using previously published phylogenies with near-complete species sampling constrained to match our transcriptomic results.Finally, we estimated ancestral ranges and inferred instances of vicariance. Results:We recovered a well-supported topology with a division between taxa from landmasses that made up East Gondwana, and a grade of taxa from West Gondwana.Pettalus was resolved either as the sister group of the Queensland-endemic Austropurcellia, or as the sister group to a larger clade from East Gondwana, though favouring Pettalus + Austropurcellia. Divergence times for multiple vicariance events coincided with Gondwana's breakup. Speciation-extinction analysis found one diversification process for the family: an initial burst of cladogenesis that slowed down through time.Main Conclusions: Given that the order of cladogenesis corresponds to the order in which Gondwana fragmented, and the concurrent timing of vicariance and rifting, Gondwanan breakup explains major biogeographic patterns in Pettalidae. Some divergences predate initial rifting, but there is no evidence of trans-oceanic dispersal.The Sri Lanka-eastern Australia relationship makes sense in the light of large-scale Gondwanan breakup, a remarkable feat for such an ancient event. , all of whom helped collect specimens for this project. All specimens were collected under valid permits (New Zealand multiple permits [38002-RES]; Australia [QLD #WITK13653913, #WITK08381010; WA Permits #OF000190, #CE000648, #SF004565]; Chile [Autorización #026/2014]; South Africa [Eastern Cape permits #CRO 108/11CR and CRO 109/11CR; KZN #OP 4085/2011] and Western Cape Permit # AAA007-00344-0035). We thank Rosa Fernández and Martin Schwentner for their help in teaching molecular and computational methods involved in RNA sequencing. Adam Baldinger and Breda Zimkus provided collections support at the MCZ. Computations for this project were done on the Odyssey cluster, supported by the FAS Division

Complex patterns of Gondwanan biogeography revealed in a dispersal‐limited arachnid

“…The patterns seen in Triaenonychidae suggest a much more complex history of connectivity between Tasmania and Australia not seen in other studies of co-distributed arthropods (e.g. Baker, Boyer, et al, 2020;Giribet & Edgecombe, 2006;Oliveira & Mayer, 2017). Some studies are suggestive of similarly complex patterns, but divergence F I G U R E 6 Hypothetical reconstruction of ancestral triaenonychid distribution in the late Jurassic.…”

“…We estimated divergence dates using the beast 2.6.1 package (Bouckaert et al, 2019). Fossil calibrations followed commonly used Opiliones fossils and calibrations (Baker, Boyer, et al, 2020;Fernández et al, 2017;, with the addition of one fossil in Travunioidea. Four fossil calibrations were used, all of which were in outgroup taxa: (1) Eophalangium sheari Dunlop, Anderson, Kerp & Hass, 2004, the most ancient Opiliones fossil known dating to 405 Ma (Dunlop et al, 2003) and currently hypothesized to be part of an extinct stem lineage that is sister group to Cyphophthalmi (Garwood et al, 2014), was used to calibrate the root of Opiliones;…”

“…short-range endemism). The DEC and DIVALIKE models were tested using two sets of dispersal multipliers, a 'strict' set where multipliers ranged from 0.01 to 1 and a 'lenient' set where multipliers ranged from 0.1 to 1 (as done in Baker, Boyer, et al, 2020).…”

“…It is clear that dispersal ability and niche specificity of a taxon are correlated with the extent of its geographic distribution, such that low-dispersal taxa have smaller ranges (Agnarsson et al, 2014;Böhning-Gaese et al, 2006;Laube et al, 2013), and low dispersers in discontinuous habitats tend to be short-range endemics (Arribas et al, 2021;Harvey, 2002 terranes, shows only vicariance among regional lineages with these vicariant events attributable to or predating continental fragmentation (Baker, Boyer, et al, 2020). The triaenonychids are also a low dispersal taxon with high microhabitat specificity, but based on years of our personal observations, these characteristics are not as extreme as those in Pettalidae as triaenonychids generally occupy a broader niche where the two families are sympatric.…”

“…"-McLoughlin (2001) Biogeographic studies of Gondwanan taxa have been the source of much debate regarding the relative importance of vicariance versus dispersal in explaining current distributions of taxa across these terranes (e.g. Baker, Boyer, et al, 2020;Chousou-Polydouri et al, 2019;Michalak et al, 2010;Upchurch, 2008). While the debating has largely settled, acknowledging the importance of both processes, studies of Gondwanan taxa still offer much to the field of biogeography.…”