Fuzzy boundaries: color and gene flow patterns among parapatric lineages of the western shovel-nosed snake and taxonomic implication

Abstract

Accurate delineation of lineage diversity is increasingly important, as species distributions are becoming more reduced and threatened. During the last century, the subspecies category was often used to denote phenotypic variation within a species range and to provide a framework for understanding lineage differentiation, often considered incipient speciation. While this category has largely fallen into disuse, previously recognized subspecies often serve as important units for conservation policy and management when other information is lacking. In this study, we evaluated phenotypic subspecies hypotheses within shovel-nosed snakes on the basis of genetic data and considered how evolutionary processes such as gene flow influenced possible incongruence between phenotypic and genetic patterns. We used both traditional phylogenetic and Bayesian clustering analyses to infer range-wide genetic structure and spatially explicit analyses to detect possible boundary locations of lineage contact. Multilocus analyses supported three historically isolated groups with low to moderate levels of contemporary gene exchange. Genetic data did not support phenotypic subspecies as exclusive groups, and we detected patterns of discordance in areas where three subspecies are presumed to be in contact. Based on genetic and phenotypic evidence, we suggested that species-level diversity is underestimated in this group and we proposed that two species be recognized, Chionactis occipitalis and C. annulata. In addition, we recommend retention of two subspecific designations within C. annulata (C. a. annulata and C. a. klauberi) that reflect regional shifts in both genetic and phenotypic variation within the species. Our results highlight the difficultly in validating taxonomic boundaries within lineages that are evolving under a time-dependent, continuous process.

Figure 1. Subspecies distribution and dorsal color patterns of the western shovel-nosed snake (Chionactis occipitalis) along with genetic sampling locations (black dots).

The presumed range of the morphological intergrade zone at the interface of C. o. annulata and C. o. klauberi is depicted by the dashed line.

Figure 2. Phylogeny for the western shovel-nosed snake (Chionactis occipitalis) based on partitioned Bayesian analysis of mitochondrial DNA sequence data (16S rRNA and ND1 genes) and the geographic distribution of the major lineages (Mojave lineage in blue, Sonoran lineage in red, and Colorado lineage in green).

The geographic distribution of clades within each lineage are outlined with a dashed line, clade E (yellow clade and dots) was routinely placed as sister to the Sonoran lineage, but posterior probabilities supporting this relationship were weak (Pp < 0.50). Black circles at nodes represent Bayesian posterior probabilities of ≥ 0.95. See Figures S1-3 for more detail within each mtDNA lineage.

Figure 3. Assignment probabilities based on the structure analysis (K  =  3).

a) Each individual is represented by a single column with membership assignment probabilities for each of the three clusters (K) noted as the relative proportion of each color (blue, green, and red represent the Mojave, Colorado, and Sonoran clusters, respectively). The vertical black bars represent the a priori subspecies assignment for each individual that was used in the analysis.

Figure 4. Range-wide geographic distribution of the three clusters inferred by structure (K  =  3) overlaid on the subspecies distributions.

Circles on the map are colored proportional to their posterior probability assignment to each of the three clusters.

Figure 5. Spatially-explicit estimate of population structure across Arizona based on the geneland analysis.

a) Map of Arizona and the geographic distribution of sampled individuals colored according to the probability of assignment within each cluster identified using geneland (green, orange, and red circles represent individuals assigned to Clusters A, B, and C, respectively). The shading indicates elevations below 300m (light grey), between 300 and 1000m (grey) and above 1000m (dark grey). b) Geneland probability contour maps for the three clusters across Arizona. The highest posterior probabilities are in white (p ≥ 0.9) and the lowest are in red (p ≤ 0.1) – contour lines within each map depict the spatial change in population assignment probability.