Phylogenomic analyses reveal a Gondwanan origin and repeated out of India colonizations into Asia by tarantulas (Araneae: Theraphosidae)

Abstract

The study of biogeography seeks taxa that share a key set of characteristics, such as timescale of diversification, dispersal ability, and ecological lability. Tarantulas are ideal organisms for studying evolution over continental-scale biogeography given their time period of diversification, their mostly long-lived sedentary lives, low dispersal rate, and their nevertheless wide circumtropical distribution. In tandem with a time-calibrated transcriptome-based phylogeny generated by PhyloBayes, we estimate the ancestral ranges of ancient tarantulas using two methods, DEC+j and BBM, in the context of their evolution. We recover two ecologically distinct tarantula lineages that evolved on the Indian Plate before it collided with Asia, emphasizing the evolutionary significance of the region, and show that both lineages diversified across Asia at different times. The most ancestral tarantulas emerge on the Americas and Africa 120 Ma–105.5 Ma. We provide support for a dual colonization of Asia by two different tarantula lineages that occur at least 20 million years apart, as well as a Gondwanan origin for the group. We determine that their current distributions are attributable to a combination of Gondwanan vicariance, continental rafting, and geographic radiation. We also discuss emergent patterns in tarantula habitat preferences through time.

The tangled biogeographic history of tarantulas: An African centre of origin rules out the centrifugal model of speciation

“…Opatova et al (2020) used the fossil Rosamygale grauvogeli and Cretamygale chasei to calibrate the Avicularioidea–Atypoidea and Theraphosoidina–Nemesioidina splits respectively. Foley et al (2021) additionally used the fossil Ambiortiphagus ponomarenkoi to calibrate the Antrodiaetidae–Atypidae split. However, Magalhaes et al (2020) criticised the use of C. chasei and A. ponomarenkoi in calibrations because of a lack of synapomorphies that could be used to place these fossils in a phylogeny unambiguously.…”

“…Figures prepared with GPlates plate tectonics visualisation software (Müller et al, 2018) using the paleomap dataset by Scotese (2002). The different scenarios are – M1: Out of America 1 – American origin and dispersal from America to Africa directly as well as via India as suggested by Foley et al (2021), M2: Out of Africa – African origin and dispersal to other landmasses as shown in Opatova et al (2020), M3: Out of America 2 – American origin and dispersal to India via Africa as proposed by Miller et al (2011) and M4: Out of East Gondwana – Origin in one of the East Gondwanan landmasses and subsequent dispersal to America and Africa as suggested by Turk et al (2020). Check materials and methods section for the details of the models.…”

“…The ancient origins of tarantulas (family Theraphosidae), their circumtropical distribution and high levels of local endemism make for an intriguing model to understand this phenomenon at a continental scale (Bond et al, 2001; Bond & Stockman, 2008; Foley et al, 2021; Pocock, 1903; World Spider Catalog, 2022). Two previous studies on the historical biogeography of tarantulas propose conflicting hypotheses for their centre of origin.…”

“…Here, we aim to reconstruct the historical biogeography of tarantulas to understand where they originated and the direction and timing of dispersal events in this group. While we use the same genome‐scale dataset as Foley et al (2021), our biogeographic analyses incorporate a time‐stratified approach that accounts for varying distances between landmasses at different geological periods. Further, we use an improved interpretation of the fossil record following Magalhaes et al (2020) to inform our phylogenetic calibration.…”

“…We specifically aimed to address these limitations, improve on the two previous studies (Foley et al, 2021; Opatova et al, 2020) and incorporate a biogeographic model testing framework to explicitly test four different hypotheses: (a) an American origin scenario followed by dispersal to Africa via India, (b) American origin followed by dispersal to India via Africa, (c) an African origin and subsequent dispersal to other landmasses and (d) an east Gondwanan origin. Foley et al (2021) found support for the first scenario, and their study had better coverage of taxa compared to the study of Opatova et al (2020) who found support for the African origin scenario. In addition, given that South America harbours most of the extant diversity of tarantulas, we expect one of the American origin scenarios (hypotheses a and b) to be the most likely one.…”