Speciation in the Peninsular Indian Flying Lizard (Draco dussumieri) Follows Climatic Transition and Not Physical Barriers

Abstract

Marked with high levels of endemism and in situ radiations, the Western Ghats mountains make for a compelling backdrop to examine processes that lead to the formation and maintenance of species. Regional geographic barriers and paleoclimatic fluctuations have been implicated as drivers of speciation, but their roles have not been explicitly tested in a phylogenomic framework. We integrated mitochondrial DNA, genome-wide SNPs and climatic data to examine the influence of geographic barriers and climatic transitions in shaping phylogeography and potential speciation in the Peninsular Indian Flying lizard (Draco dussumieri). We found strong evidence for two independently evolving, geographically distinct, northern and southern lineages within D. dussumieri that diverged during the early Pleistocene, and a gradient of admixed populations across a broad hybrid zone in the Central Western Ghats. Migrations after initial divergence were continuous, but gene flow remained consistently below thresholds required to homogenise lineages. We found more support for isolation by environment (especially rainfall regimes) than by distance. The range-break between lineages occurs at a transition zone in the Central Western Ghats that separates dissimilar rainfall regimes with no physical barriers. This limit is potentially an ecological barrier, which nevertheless was permeable during glacial maxima. We hypothesise that similar phylogeographic patterns will emerge in other widespread, wet-adapted species in the Western Ghats that presumably endured the same climatic processes.

Keywords: Western Ghats; contact zone; isolation by environment; paleoclimate; population demographics; squamate.

FIGURE 1

Elevation map of Peninsular India (a) with locations of Draco dussumieri sampled during this study. The contours of the Western Ghats are indicated by a solid line. Important regions and biogeographic barriers mentioned in the text are indicated. Hills in the southern Eastern Ghats marked with an ‘X’ refer to locations where D. dussumieri were found, but not collected (see Section 2). An adult male D. dussumieri (b) from the Agumbe plateau flashing his dewlap (Photo credit: Vinod Venugopal).

FIGURE 2

Mitochondrial phylogeny (a) of D. dussumieri (outgroup removed) with branch support values for the clades that inform our primary lineage hypothesis. Sampling locations for mitochondrial DNA data (b) colour coded according to clades. Distribution ranges of clades are either informed by our understanding of biogeographic barriers or follow sampling locations. Gaps between clades represent regions where D. dussumieri has not been collected or is presumed not to occur. The phylogenetic pattern in D. dussumieri follows a latitudinal gradient across Peninsular India.

FIGURE 3

Results of the STRUCTURE analysis (a) using the dataset with loci shared across at least 33 individuals (min33), mapped against sampling locations. The admixed individuals occur in the Wayanad, Coorg and Agumbe plateau regions (between 11.5° N–13.5° N) in the Western Ghats. The first two principal components (b) averaged from 25 replicate PCAs conducted on the min33 dataset, showing genetic segregation of the northern, southern,and admixed lineages. Triangle plot (c) using SNP data that maps hybrid index (S) against interclass heterozygosity (H). Individuals plotted on the curve follow theoretical expectations of Hardy–Weinberg equilibrium. Interclass heterozygosity of individuals plotted against latitude (d) in the Western Ghats shows that the more heterozygous individuals occur between 11.5° N–13.5° N. ADM, admixed individuals; NWG, Northern Western Ghats lineage; SWG, Southern Western Ghats lineage.

FIGURE 4

Pairwise F _ST as a function of geographic distances (a) between all individuals from within (grey) and between (black) lineages. Trend lines fitted using the R lm function show a discontinuous relationship among comparisons between and within lineages, a pattern suggestive of restricted gene‐flow supporting the presence of two species (see Prates et al. 2024). Genotype‐environment associations (b) that show SNPs that may be adaptively differentiated (significant correlations are colour coded) along axes of climatic predictors. Precipitation seasonality (bio15) was correlated with the most SNPs (34). The best‐fit population demographic model from GADMA (c) constructed using a mutation rate of 1.0 × 10⁻⁹ substitutions/site/year and two time‐intervals post initial divergence, showing population sizes (inset scale), times of key demographic events (divergence, population expansions, and migrations), and the strengths and directions of migration events (represented by black arrows). NWG, Northern Western Ghats lineage; SWG, Southern Western Ghats lineage.

FIGURE 5

Climatic niche models of the southern (a, c) and northern (b, d) lineages constructed using six weakly correlated climatic variables during the present (top panel) and the Last Glacial Maximum (LGM; bottom panel). Suitable ranges were greater for both lineages during the LGM when compared to the present.

FIGURE 6

Distributions of the northern and southern lineages of D. dussumieri (sensu lato) in context of precipitation seasonality (coefficient of variation) in the Western Ghats. Pie charts show ancestry proportions of admixed individuals in the Central Western Ghats. The range break between northern and southern lineages is indicated by a dotted line, which further separates regions with high versus moderate‐to‐low rainfall seasonality. The inset shows MaxEnt mean response curves (averaged from 30 replicates) to precipitation seasonality for both lineages. ADM, admixed populations; NWG, Northern Western Ghats lineage; SWG, Southern Western Ghats lineage.