Evolutionary models demonstrate rapid and adaptive diversification of Australo-Papuan pythons.

Evolutionary biology royalsocietypublishing.org/journal/rsbl Research Evolutionary models demonstrate rapid and adaptive diversification of AustraloPapuan pythons Damien Esquerré1, Ian G. Brennan1, Stephen Donnellan2,3 and J. Scott Keogh1 1 Cite this article: Esquerré D, Brennan IG, Donnellan S, Keogh JS. 2022 Evolutionary models demonstrate rapid and adaptive diversification of Australo-Papuan pythons. Biol. Lett. 18: 20220360. https://doi.org/10.1098/rsbl.2022.0360 Received: 4 August 2022 Accepted: 25 November 2022 Subject Areas: evolution Keywords: adaptive radiation, Australia, snakes, Wallace’s line, morphometrics, Gondwana Author for correspondence: Damien Esquerré e-mail: Electronic supplementary material is available online at https://doi.org/10.6084/m9.figshare. c.6330215. Division of Ecology and Evolution, Research School of Biology, The Australian National University 0200, Canberra, ACT, Australia 2 School of Biological Sciences, The University of Adelaide, Adelaide, SA 5005, Australia 3 Evolutionary Biology Unit, South Australian Museum, North Terrace, Adelaide, SA 5000, Australia Lineages may diversify when they encounter available ecological niches. Adaptive divergence by ecological opportunity often appears to follow the invasion of a new environment with open ecological space. This evolutionary process is hypothesized to explain the explosive diversification of numerous Australian vertebrate groups following the collision of the Eurasian and Australian plates 25 Mya. One of these groups is the pythons, which demonstrate their greatest phenotypic and ecological diversity in Australo-Papua (Australia and New Guinea). Here, using an updated and near complete time-calibrated phylogenomic hypothesis of the group, we show that following invasion of this region, pythons experienced a sudden burst of speciation rates coupled with multiple instances of accelerated phenotypic evolution in head and body shape and body size. These results are consistent with adaptive radiation theory with an initial rapid niche-filling phase and later slow-down approaching niche saturation. We discuss these findings in the context of other Australo-Papuan adaptive radiations and the importance of incorporating adaptive diversification systems that are not extraordinarily species-rich but ecomorphologically diverse to understand how biodiversity is generated. 1. Introduction Lineages that encounter multiple available ecological niches may ultimately diversify to fill this ecological space, a process known as adaptive radiation [1,2]. This results in both an increase in speciation rates as the lineages diversify and the evolution of novel phenotypes as they adapt to the new ecological niches [3–5]. Colonization of an environmentally diverse region with less competition is a common precursor to adaptive radiation, and it has resulted in many spectacular radiations, both at small geographical scales [6,7] and when continents approach each other—facilitating biological exchanges [8–11]. Australo-Papua, the region comprising Australia, New Guinea and surrounding islands, broke apart completely from Antarctica in the early Eocene (around 45 Mya) and then began a long period of isolation from other major landmasses [12,13]. This time and isolation allowed for the diversification of many animal and plant groups including the iconic Australian marsupials and Eucalyptus trees, among many others [14–17]. However, many of the most diverse and emblematic groups in the region are descended from much more recent colonization events from Asia, coinciding with the collision of the Eurasian and Australian plates in the Oligocene around 25 Mya [18–20]. Squamate reptiles are extraordinarily diverse in the Australo-Papua region and the vast majority of this diversity is comparatively recent [19]. For example, agamid lizards, monitor lizards, blind snakes, elapid snakes and pythons are all groups that arrived to Australo-Papua probably sometime in the late Palaeogene and early Neogene © 2022 The Author(s) Published by the Royal Society. All rights reserved. We use a range of methods to detect diversification patterns consistent with adaptive radiation. To test our hypotheses on a wellsampled and updated phylogenetic tree with recent changes in python taxonomy [36,37], we built a species tree with Astral III v. 5.7.8 [38] using the gene trees for 33 species from 376 nuclear exons from Esquerré et al. [25], as well as a mitochondrial genome gene tree including 32 of those species and five species not sampled for the nuclear exons and not included in Esquerré et al. [25]. We time-calibrated this tree using MCMCTree from the PAML 4.9 package [39], using the dates inferred by Esquerré et al. as secondary calibrations. See electronic supplementary material for details. This time-calibrated tree contains 37 of the 40 (93%) currently recognized species: 27 for the Australo-Papuan clade, eight for the Afro-Asian clade and the two Malayopython species from Southeast Asia. During an adaptive radiation, we often expect early bursts of diversification as lineages diversify to fill available niches. To visualize the diversification patterns, we constructed lineage through time (LTT) plots [40] of the Pythonidae and the Australo-Papuan clade separately and of the 95% confidence 3. Results In the LTT plot (figure 1), the Pythonidae as a whole falls well within a pure-birth model of diversification, whereas the Australo-Papuan clade clearly fits an early burst pattern. For the Australo-Papuan clade, the maximum log-likelihood 2 Biol. Lett. 18: 20220360 2. Methods interval (CI) of 1000 simulated trees under a pure-birth model and an early burst model (with a γ-statistic of −1). This was done with the functions ltt95 and pbtree from the R package phytools [41]. As an additional more powerful tool to test the hypothesis that reaching Australo-Papua resulted in an increased rate of diversification with subsequent slow-down as a consequence of niche filling, we fitted constant rate (CR) and DD birth–death models to the Pythonidae and Australo-Papuan clade trees and performed a bootstrap-likelihood ratio test of DD against CR and computed the power of the test. This was done using the R package DDD [42,43]. In an attempt to identify diversification patterns associated with crossing biogeographic lines, we implemented a method based on graph theory that estimates the spectral density profile of a tree based on its Laplacian graph [44]. These spectral densities are used to identify different ‘modalities’ that can reflect distinct diversification patterns. In addition to fitting a model with the optimal number of modalities (i), we fitted models with 1 to (i) modalities to identify modalities in the tree that were consistent across all models. This was performed using the R package RPANDA [45]. Finally, we implemented the recently developed Bayesian method cladogenetic diversification rate shift (CLaDS) that ai (...truncated)