Hybridization between multiple fence lizard lineages in an ecotone: locally discordant variation in mitochondrial DNA, chromosomes, and morphology

Abstract

We investigated a hybrid zone between two major lineages of fence lizards (Sceloporus cowlesi and Sceloporus tristichus) in the Sceloporus undulatus species complex in eastern Arizona. This zone occurs in an ecotone between Great Basin Grassland and Conifer Woodland habitats. We analysed spatial variation in mtDNA (N=401; 969 bp), chromosomes (N=217), and morphology (N=312; 11 characters) to characterize the hybrid zone and assess species limits. A fine-scale population level phylogenetic analysis refined the boundaries between these species and indicated that four nonsister mtDNA clades (three belonging to S. tristichus and one to S. cowlesi) are sympatric at the centre of the zone. Estimates of cytonuclear disequilibria in the population closest to the centre of the hybrid zone suggest that the S. tristichus clades are randomly mating, but that the S. cowlesi haplotype has a significant nonrandom association with nuclear alleles. Maximum-likelihood cline-fitting analyses suggest that the karyotype, morphology, and dorsal colour pattern clines are all coincident, but the mtDNA cline is skewed significantly to the south. A temporal comparison of cline centres utilizing karyotype data collected in the early 1970s and in 2002 suggests that the cline may have shifted by approximately 1.5 km to the north over a 30-year period. The recent northward expansion of juniper trees into the Little Colorado River Basin resulting from intense cattle overgrazing provides a plausible mechanism for a shifting hybrid zone and the introgression of the mtDNA haplotypes, which appear to be selectively neutral. It is clear that complex interactions are operating simultaneously in this contact zone, including the formation of hybrids between populations within S. tristichus having diagnostic mtDNA, morphology, karyotypes, and dorsal colour patterns, and secondary contact between these and a distantly related yet morphologically cryptic mtDNA lineage (S. cowlesi).

Empirical study of hybrid zone movement

“…At the frog Pseudophryne bibroni-Pseudophryne semiarmorata hybrid zone, a tail of asymmetric introgression of an Ldh isozyme marker diagnostic of P. semiarmorata populations into P. bibroni populations to the north of the hybrid zone also fits with the observed zone movement in favour of P. bibroni (McDonnell et al, 1978). A hybrid zone between lizards Sceloporus tristichus and Sceloporus cowlesi has moved over 1.5 km in around 30 years in favour of the former; correspondingly, S. cowlesi mitochondrial DNA is found introgressed over 8 km into the current range of S. tristichus (Leaché and Cole, 2007). Introgression between newts Triturus cristatus and Triturus marmoratus is found in the area of recent species replacement, but is absent in other areas (Arntzen and Wallis, 1991).…”

“…Human-induced climate change appears to have caused movement of the Pholidobolus montium-Pholidobolus affinis (lizards) hybrid zone, when fields which had been rocky with numerous agaves were cleared of rocks, irrigated and planted with crops (Hillis and Simmons, 1986), and hybridization between salamanders P. jordani and P. glutinosus may have increased due to intense timbering (Hairston et al, 1992). Ecological changes due to overgrazing may have caused movement in a hybrid zone between lizards S. cowlesi and S. tristichus (Leaché and Cole, 2007). Global warming was tentatively invoked to explain the movement of a hybrid zone between crickets A. fasciatus and A. socius (Britch et al, 2001).…”

“…When a currently moving zone shows a trail of introgression over a larger distance than the observed movement, researchers may infer that the movement can be to some extent extrapolated into the past (McDonnell et al, 1978;Leaché and Cole, 2007). In some cases, the limits of the neutral introgression may indicate the location where the initial hybrid zone was formed, but little certainty can be placed on this inference unless multiple neutral markers show a concurrent limit when examined at a range of spatial scales.…”

Patterns of differential introgression in a salamander hybrid zone: inferences from genetic data and ecological niche modelling

“…Many other cases documenting mtDNA introgression come from studies of naturally occurring hybrid zones showing shifts in clines of mtDNA relative to nuclear DNA and morphology (e.g. Arntzen & Wallis 1991;Sequeira et al 2005;Vörös et al 2006;Brito 2007;Hofman & Szymura 2007;Leaché & Cole 2007;Kawakami et al 2008).…”

Sex-specific clines support incipient speciation in a common European mammal

“…Likelihood profiles and two log-likelihood support limits (corresponding to 95% confidence intervals; Edwards, 1972) were explored using the 'cross-section' option. Cline coincidence (centres at the same position) and concordance (equal cline widths) were explored with a likelihood ratio test (LRT) following the procedure used by Phillips et al (2004) and adapted by Leache and Cole (2007).…”