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Quantitative assessment of population genetic structure and historical phylogeography of the Alameda Whipsnake Masticophis lateralis euryxanthus

Released: 2011
Citation:
Richmond, J. Q., D. A. Wood, C. Hoang, and A. G. Vandergast. 2011. Quantitative assessment of population genetic structure and historical phylogeography of the Alameda Whipsnake Masticophis lateralis euryxanthus.  U. S. Geological Survey, Western Ecological Research Center. Data Summary prepared for USFWS Sacramento FWO. 81pp.

The Alameda whipsnake Masticophis lateralis euryxanthus has been the subject of conservation concern in California for over three decades. Management efforts to date have focused mainly on the snake’s ecology and preserving San Francisco Bay area populations that fit the description of the M. l. euryxanthus phenotype (Riemer 1954); however, these efforts have reached a point where continued management would benefit from knowledge on genetic variation within and among these populations. In this study, we use short tandem repeat loci (STR) and mitochondrial DNA (mtDNA) sequences to examine the population dynamics of M. l. euryxanthus, and frame this work within the historical, phylogeographic context of the parent species M. lateralis. We use both phylogenetic and population genetic analyses to examine patterns of variation at multiple geographic scales and over different evolutionary time frames.

 

Major findings

    • We found no evidence that populations with the M. l. euryxanthus phenotype form an exclusive mitochondrial clade; rather, M. l. euryxanthus haplotypes fall within a geographically restricted and well-supported clade that began to diversify in the late Pleistocene (~0.10 – 0.21 million years ago [Ma]), and separated from members of its sister clade during a time period that coincides with the formation of the San Francisco Bay (~0.51 Ma). This same clade, which we refer to as the ‘Central CA’ clade, also includes populations that do not have the M. l. euryxanthus phenotype.
    • A single haplotype predominates within the Central CA clade, and its constituent populations show evidence of a demographic and geographic range expansion that began approximately 0.25 Ma ago. The southern boundary of this clade extends substantially further south into the Diablo Range than the known distribution of M. l. euryxanthus.  
    • Levels of genetic divergence among the major mtDNA clades within M. lateralis in California exceed that of separate, currently recognized Masticophis species in the Cape Region of Baja California. Under a phylogenetic species concept, it would be possible to recognize these clades as separate species.
    • A strong signal of genetic isolation-by-distance was detected in both the STR and mtDNA data, and spatially explicit Bayesian assignment models based on the STR allele frequencies unambiguously detected four main clusters within East Bay area populations. These clusters largely assign to critical habitat units in Alameda and Contra Costa counties.
    • Divergence among clusters is moderate to high, and Bayesian inference of recent migration rates suggests that the sampled populations have a low proportion of immigrants.
    • Populations comprising several clusters in west Alameda and Contra Costa Counties show evidence of unidirectional gene exchange; genes from one cluster, formed by centrally located populations at the Stonebrae/Bailey Ranch site, are apparently moving to neighboring populations to the immediate north and south more frequently than they are moving in.
    • There is no strong evidence of recent reductions in effective population size at any of the sampling sites in the East Bay.
    • Greater phylogenetic and population genetic distinctiveness of individuals sampled near the Alameda-Santa Clara County line is concordant with a loss in the distinctiveness of the M. l. euryxanthus phenotype over the same general area, suggesting that this variation may reflect secondary contact between historically differentiated groups.

Conclusions

Our results indicate substantial, unrecognized phyletic diversity within M. lateralis, with three well-supported mtDNA clades occurring in California and two occurring in Baja California, Mexico. We found no evidence that M. l. euryxanthus populations form an exclusive mtDNA group; however, this is not an unexpected result given that neighboring populations belonging to separate subspecies do not form reproductively isolated units, and gene flow has the potential to obscure their phylogenetic history in areas of secondary contact. Spatial patterns of mtDNA haplotypes and STR alleles indicate that the current management units adequately reflect population genetic structuring for M. l. euryxanthus in the Bay area, but that individuals appear to be moving out of certain parts of western Alameda County more frequently than they are moving in. We discuss how the spatial dispersion of our sampling and the geography of critical habitat units may be influencing our results, and outline a set of criteria for identifying groups of populations that might be considered high-priority candidates for future management. Our criteria reconcile information from a variety of data, and emphasize a need to not only preserve the snake’s ecology, but also the microevolutionary processes that ultimately gave rise the existing genetic and phenotypic diversity within the species. We close with descriptions of future research projects that could add to a comprehensive model for the management of this species.



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This product is associated with the following project:
Conservation genetics of the endangered Alameda whipsnake

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