Hypsiscopus murphyi sensu
Photo: Bryan Stuart
In one of those far-away places that the simple-minded authors of the story in Genesis about a small flat Earth with a dome over it being magicked up out of nothing in the Middle East, 10,000 years ago, could never have guessed existed, and some 2.5 million years before they though Earth existed, major environmental changes were driving the diversification of a species of snake into several descendant species, just as the Theory of Evolution predicts.
If those simple-minded Bronze Age pastoralists had known about it and understood its significance in terms of the history of life on Earth and the dynamic geology of the planet, just imagine how different their imaginative tale would have been! As it was, they had to do their best with what little knowledge and understanding they had.
The snake in question was the Rice Paddy snake, otherwise known as a mud snake, and the far-away place was Thailand where the rise of the Khorat Plateau caused environmental changes that resulted in the evolutionary diversification of the Hypsiscopus genus.
The team of researchers from various American and Southeast Asian Universities, who have shown this link between environmental change and evolutionary radiation in a genus was led by Dr. Justin Bernstein, of the University of Kansas Center for Genomics. Their findings are published open access in Scientific Reports and are explained in a Kansas University news release:
A University of Kansas study of rice paddy snakes in Southeast Asia gives key details to their diversification and natural history, adding molecular evidence that the rise of the Khorat Plateau and subsequent environmental shifts in Thailand may have altered the course of the snakes’ evolution some 2.5 million years ago. The findings were published today in the journal Scientific Reports.The team give more technical detail in their open access paper in Scientific Reports
Researchers say the implications could help tell the story of diversification more broadly in the region.
Bernstein, who currently serves at the University of Texas-Arlington, said the mud snakes, a family known as the Homalopsidae, are commonly found today in aquatic systems. Bernstein’s newest work on the homalopsids focuses on a subgroup called rice paddy snakes that are commonly found in agricultural fields and freshwaters streams in Southeast Asia.This paper concerns mud snakes typically found in aquatic systems across Southeast Asia, South Asia, East Asia, Australia and New Guinea. Deeper-level relationships regarding their evolution have recently begun to be studied, particularly through genome-scale data. However, finer-scaled evolutionary patterns remain to be fully revealed.
Dr. Justin M. Bernstein, Lead author
Center for Genomics
University of Kansas, Lawrence, KS, USA.
Although recent research has touched on the diversity of rice paddy snakes, their geographic distribution has touched off scientific speculation: One hypothesis suggests that around 2.5 million years ago, a plateau in Central Thailand, known as the Khorat Plateau, emerged from the ground, leading to the separation and subsequent diversification of snake populations over time. Indeed, molecular data provided insights into the timing of species diversification that aligned with the formation of the plateau.
However, a later genome-scale study challenged this hypothesis by pushing the divergence date backward, predating the plateau's formation.
Past that, the research team found varied differences in preferred habitats among different snake species using past and present niche models, hinting that other environmental factors might have influenced their routes toward diversification and geographic distribution.This discrepancy raises questions about the accuracy of different datasets in determining evolutionary timelines. To address this, our paper employs more limited molecular datasets but with more robust analyses and denser sampling to test the hypothesis. Our results suggest that the group indeed diversified after the Khorat Plateau rose, and environmental changes over time further contributed to their divergence.
Dr. Justin M. Bernstein
Bernstein’s collaborator included co-author Rafe Brown, KU professor of ecology & evolutionary biology and curator-in-charge of the Herpetology Division at KU’s Natural History Museum & Biodiversity Institute. Other co-authors included Harold Voris and Sara Ruane of the Field Museum in Chicago; Bryan Stuart of the North Carolina Museum of Natural Sciences; the late Daryl Karns of Hanover College; Jimmy McGuire of the University of California-Berkeley, Djoko Iskandar of the Institut Teknologi Bandung in Indonesia; Awal Riyanto of the National Research and Innovation Agency of Indonesia; Camilo Calderón‐Acevedo of the State University of New York: College of Environmental Science and Forestry; Marcelo Gehara of Rutgers University-Newark; and J. Angel Soto‐Centeno of Rutgers University-Newark and the American Museum of Natural History.
Bernstein and his collaborators relied on molecular data along with ecological niche modeling to shed new light on the rice paddy snakes, which depended on data about where specimens were located in the field. This approach could help conservation efforts going forward, or predictions of how species might fare in climate change scenarios.
He said the environmental data includes variables like temperature differences, seasonality and precipitation at different points in time, such as quarterly, monthly or annually.The whole point of ecological niche modeling, put simply, is if I take, say, 100 occurrence points for those snakes, and then I use 19 environmental data layers that correspond with each point, and compare it to a background — which would be the landscape with its environmental data regardless of snake occurrence points — do we see correlations and patterns? You're trying to determine the habitat suitability of your species of interest across a broad landscape, including areas where they have not been recorded from.
These 19 layers containing the environmental factors are ‘stacked’ in a way that each GPS coordinate — where a snake occurrence record is — has a set of 19 environmental variables associated with it.
Dr. Justin M. Bernstein
For instance, via this approach Bernstein said while these rice-paddy snakes don't exist in the Philippines, there are suitable habitats based off of where they live in Indochina.
The research builds on two of Bernstein’s earlier works. One study combines genetic analyses of older museum specimens' mitochondrial DNA with fresher genetic samples from recent field collections of mud snakes to learn more about diversity of homalopsids, including rice paddy snakes. The other study is a more focused study that described a new rice paddy snake species and posited the hypothesis of the Khorat Plateau based on current data but lacked the power to test it.Hypothetically they could live there. That doesn't mean they do. There is no evidence suggesting they are able to get across ocean waters and enter the Philippines, and it would be highly unlikely for that scenario to occur. But the analysis is just indicating there is suitable habitat elsewhere, in addition to where we find them now, and that can be really useful. If it's a continuous landscape and you haven't found any individuals of a species in a particular area, but you see high habitat suitability, maybe you can go find a population that is presently unknown to exist.
Dr. Justin M. Bernstein
While many species of the mud snakes are drab, Bernstein said others are highly charismatic.
Ultimately, the mud snake’s value may be in serving to show how species, and their morphological diversity, evolves over time, as well as how other organisms may react to changes in the ecosystems they live in.Some have tentacles as appendages on their face. You could find two of the same species in one hole, like a mud lobster hole, where one is white and black, and the other is bright red and black — very striking. Some have speckled yellow bellies, while others are black with bright orange flecks and stripes down their back. And other species have unique behaviors that are not seen in the 4,000-plus species of snakes. They are truly stunning snakes.
I saw a lot of opportunity in them as a model system for investigating biogeography. Honestly, using them more as a model system for understanding how species change or remain stable over time has been really valuable. We have several studies we want to pursue further, and many more in the works, and it all begins with understanding their evolutionary relationships.
Dr. Justin M. Bernstein
Abstract
Divergence dating analyses in systematics provide a framework to develop and test biogeographic hypotheses regarding speciation. However, as molecular datasets grow from multilocus to genomic, sample sizes decrease due to computational burdens, and the testing of fine-scale biogeographic hypotheses becomes difficult. In this study, we use coalescent demographic models to investigate the diversification of poorly known rice paddy snakes from Southeast Asia (Homalopsidae: Hypsiscopus), which have conflicting dates of origin based on previous studies. We use coalescent modeling to test the hypothesis that Hypsiscopus diversified 2.5 mya during the Khorat Plateau uplift in Thailand. Additionally, we use ecological niche analyses to identify potential differences in the niche space of the two most widely distributed species in the past and present. Our results suggest Hypsiscopus diversified ~ 2.4 mya, supporting that the Khorat Plateau may have initiated the diversification of rice paddy snakes. We also find significant niche differentiation and shifts between species of Hypsiscopus, indicating that environmental differences may have sustained differentiation of this genus after the Khorat Plateau uplift. Our study expands on the diversification history of snakes in Southeast Asia, and highlights how results from smaller multilocus datasets can be useful in developing and testing biogeographic hypotheses alongside genomic datasets.
Introduction
Widely distributed taxa can serve as excellent model systems to test biogeographic hypotheses, especially in regions with complex geologic histories and a mosaic of geological features. One group that includes several wide-ranging taxa, in one of the most complex regions are the mud snakes; Old World mud snakes of the family Homalopsidae consist of 57 species in 26 genera distributed throughout South and Southeast Asia, Australia, and New Guinea1. Homalopsids are found across aquatic environments with muddy substrates and varying salinities (e.g., rice paddies, tidal flats, mangroves, swamp forests, freshwater lakes and streams)2. These mud snakes exhibit a variety of feeding behaviors3, diets4 and morphological adaptations such as rostral mechanoreceptors5 and salt glands6. Recently, phylogenetic studies with multilocus datasets have expanded on the evolutionary relationships and divergence times of Homalopsidae7. A few genera of mud snakes are extremely abundant in aquatic systems of Southeast Asia and have some of the most widespread distributions of any terrestrial vertebrate1,2. This makes them ideal for investigating how Southeast Asia’s complex geologic history8,9 has generated patterns of diversity observed today.
Rice paddy snakes of the genus Hypsiscopus consist of four species. The newly described Hypsiscopus murphyi is distributed around and north of Thailand’s Khorat Plateau, and H. plumbeus is found around and south of the Khorat Plateau, and on the Indonesian islands as far east as Sulawesi7. Hypsiscopus matannensis and H. indonesiensis are endemic to Sulawesi, the eastern limit of the distribution of the genus (Fig. 1). Phylogenetic investigations of homalopsids using mitochondrially-driven multilocus data have placed the Hypsiscopus origin at ~ 2.5 million years ago (mya)7. Thus, it is hypothesized that the tectonic uplift event that led to the Khorat Plateau at ~ 2.5 mya9,10 may have been responsible for the diversification of rice paddy snakes7. However, date estimates of recent systematic works of Homalopsidae using genomic data pre-date the formation of the plateau with an estimated divergence of ~ 4 mya. These two studies7,11, each yielding conflicting divergence dates around the Khorat Plateau hypothesis, use different depths of DNA sequencing and different divergence date estimation techniques.Estimates of clade divergence timing on molecular phylogenies are standard in systematic studies12, especially parameter-heavy approaches that use model-based likelihood methods13,14 which have helped in formulating and testing biogeographic hypotheses. Modern phylogenetics now frequently use genomic datasets that include thousands of loci, but this comes at the cost of major increases in computational burden and analysis run times. Potentially alleviating some of these costs, summary coalescent methods aim to reconstruct phylogenies rapidly and estimate divergence dates (e.g., ASTRAL15; treePL16). Because of a higher number of informative sites and the potential to characterize evolutionary heterogeneity across independent genes, a greater number of loci is presumed to increase accuracy in divergence time estimates. Compared to single-gene or small multilocus datasets dated using computationally rigorous Bayesian methods like BEAST17, phylogenomic datasets are assumed to provide a better representation of species divergence and, as such, may allow for finer scale temporal discrimination of alternate hypotheses in biogeography18. However, the methods used to rapidly obtain divergence dates from genomic datasets may not be useful in a hypothesis-testing framework for particular geological events. This is due to genomic studies typically having lower sample sizes due to costs, thus possibly missing important population-level data, or because of the computation times associated with analysis of large datasets.Figure 1.
Sampling map of Hypsiscopus in this study. Map is colored by elevation (0–4509 m). The Red River and Khorat Plateau boundary are shown by the solid red line and dashed orange line, respectively.Photograph of H. murphyi by BLS.
Methods based on coalescent simulations of demographic models can be more intuitively customized to the study taxon to test specific evolutionary scenarios19. Coalescent models can incorporate multilocus or genomic datasets and can be fine-tuned to test phylogeographic hypotheses with large sample sizes. Obtaining accurate divergence dates is critical for downstream studies that aim to identify the causal factors of population splits and speciation, especially at potential biogeographic barriers20. Herein, we examine whether rice paddy snake diversification coincides with the rise of the Khorat Plateau and test for differences in each species’ environmental niche. The expansive range of the non-sister species H. murphyi and H. plumbeus (1.7 million km2 for H. murphyi and ~ 4 million km2 for H. plumbeus) means that they span a heterogeneous landscape of environmental, habitat, and topographic features. Phylogeographic structure and the maintenance of species limits driven by environmental heterogeneity has been documented in widely distributed taxa21,22,23, including areas that contain well-known biogeographic barriers24,25. Given the wide distribution of rice paddy snakes, we examine if quantifiable differences in the environmental niches reflect phylogeographic structure in these snakes26.
In this study, we used newly obtained sequence data for Hypsiscopus to investigate the diversification of rice paddy snakes through Southeast Asia. We obtained 303 new DNA sequences of 6 nuclear and 2 mitochondrial genes, and combined these with previously published data to generate a dataset consisting of 653 sequences across 8 genes for 151 individuals. Using coalescent demographic models with priors that encompass known Hypsiscopus evolutionary history, we tested the hypothesis that the crown group of Hypsiscopus diversified ~ 2.5 mya when the tectonic uplift of the Khorat Plateau took place9,10. Hypsiscopus is one of few taxa that have parapatric distributions around the plateau and are abundant enough to obtain a dense sampling scheme for evolutionary studies, making them an ideal system to test our diversification hypothesis. We aim to identify modes of speciation in Southeast Asia, which are often referred to in regards to the prevailing paradigm in this region: Pleistocene sea-level fluctuations. We performed quantitative morphological, molecular phylogenetic, and ecological analyses to investigate homalopsid phenotypic and genetic diversity, and predict that environmental data will yield quantifiable niche differences between the two widespread species: H. murphyi and H. plumbeus.
Molecular and morphological diversity in Hypsiscopus. Left) Phased concatenated phylogeny of Hypsiscopus (only one allele shown). Hypsiscopus murphyi is split into two subclades: East of the Red River (red) and west of the Red River (blue). Black circles at nodes represent strongly supported relationships (UFB ≥ 95 and SH-aLRT values ≥ 80). Scale bar in substitutions per site. Upper right) The six demographic scenarios tested in PipeMaster. Topology is based on the concatenated phylogeny (left), with both populations of H. murphyi collapsed into a single tip. The asterisk (*) shows the model with the highest support (Is). Bottom right) Linear discriminant analysis (LDA; 27 variables), showing three species of rice paddy snakes in morphospace. Points are shown with 68% Gaussian data ellipses. Density rugs (colored lines on axes) correspond to each point in morphospace. Density plots reflect the density of points in the plot for each species (colors correspond to the phylogeny).
Figure 3Ecological niche models of H. murphyi, H. plumbea, and H. matannensis. Colors represent habitat suitability, with warmer colors indicating higher habitat suitability based on environmental variables. Full-size images of each niche model can be found in Supplementary Figs. S5–S10.
Bernstein, J.M., Voris, H.K., Stuart, B.L. et al.
Integrative methods reveal multiple drivers of diversification in rice paddy snakes.
Sci Rep 14, 4727 (2024). https://doi.org/10.1038/s41598-024-54744-z
Copyright: © 2024 The authors.
Published by Springer Nature Ltd. Open access.
Reprinted under a Creative Commons Attribution 4.0 International license (CC BY 4.0)
Creationists will need to ignore how well the geological changes map onto the genetic changes as the genus diversified. Although correlation doesn't establish causality, it does add additional weight to the Theory of Evolution by Natural Selection that predicts environmental change will result in evolutionary change.
and of course, dedicated creationist delusionists will need to ignore the fact that these geological/environmental changes and the genetic changes as this genus of snake diversified all happened in that long period of Earth's history that happened before creationism’s god hit upon the idea of magicking a small, flat planet with a dome over it, out of nothing.
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