Range and niche shifts in response to past climate change in the desert horned lizard (Phrynosoma platyrhinos)

Abstract

During climate change, species are often assumed to shift their geographic distributions (geographic ranges) in order to track environmental conditions - niches - to which they are adapted. Recent work, however, suggests that the niches do not always remain conserved during climate change but shift instead, allowing populations to persist in place or expand into new areas. We assessed the extent of range and niche shifts in response to the warming climate after the Last Glacial Maximum (LGM) in the desert horned lizard (Phrynosoma platyrhinos), a species occupying the western deserts of North America. We used a phylogeographic approach with mitochondrial DNA sequences to approximate the species range during the LGM by identifying populations that exhibit a genetic signal of population stability versus those that exhibit a signal of a recent (likely post-LGM) geographic expansion. We then compared the climatic niche that the species occupies today with the niche it occupied during the LGM using two models of simulated LGM climate. The genetic analyses indicated that P. platyrhinos persisted within the southern Mojave and Sonoran deserts throughout the latest glacial period and expanded from these deserts northwards, into the western and eastern Great Basin, after the LGM. The climatic niche comparisons revealed that P. platyrhinos expanded its climatic niche after the LGM towards novel, warmer and drier climates that allowed it to persist within the southern deserts. Simultaneously, the species shifted its climatic niche towards greater temperature and precipitation fluctuations after the LGM. We concluded that climatic changes at the end of the LGM promoted both range and niche shifts in this lizard. The mechanism that allowed the species to shift its niche remains unknown, but phenotypic plasticity likely contributes to the species ability to adjust to climate change.

Keywords: Great Basin; Last Glacial Maximum; niche assessment; niche shift; non-analog climate; range expansion.

Fig. 1

General sample sites of Phrynosoma platyrhinos species complex (P. goodei are represented in localities 7, 13–17, and 102 and P. platyrhinos from Yuma Proving Grounds in locality 2). Grey shadings represent the three main ecoregions of interest: Mojave Desert, Sonoran Desert, and the Great Basin (Olson et al. 2001). Pink and red circles represent localities above and below 5,000 feet, respectively, that were assigned to the populations that persisted throughout the LGM. Blue circles represent localities assigned to populations that expanded after the LGM. Grey circles were not included in either group due to unclear genetic signal.

Fig. 2

(a) Median-joining network of mtDNA sequences of the Phrynosoma platyrhinos species complex nested into 16 clades. Clade 1 represents the Yuma Proving Ground haplotypes, Clade 2 represents P. goodei, and Clades 3-16 represent P. platyrhinos. Circle size and shading reflect the number of individuals exhibiting a given haplotype ranging from 1 to 4, with several abundant haplotypes indicated by large circles labeled internally. The length of connection lines between haplotypes is proportional to the number of mutational changes, with the shortest line representing a single mutational change. (b) Distribution of nested clades identified from the median-joining network. Pie graph sizes reflect the sample size at each location progressing from smallest (n = 1) to largest (n = 6). The clade numbers and color correspond to those on the median-joining network. The polygons represent extent of the expanding haplotypes in the western (Hw1, Hw2 and their satellites indicated in green) and eastern Great Basin (He1, He2 and their satellites indicated in pink).

Fig. 3

Bayesian skyline plot derived from mtDNA sequences of the Phrynosoma platyrhinos species complex. The x-axis shows time and the y-axis shows effective population size of females. The black line is the median and the grey area represents the 95% upper and lower highest posterior density limits. The plot is presented truncated on the right as the missing region showed no evidence of change in effective population size.

Fig. 4

Pairwise genetic distances among populations derived from mtDNA sequences and interpolated across landscape for the Phrynosoma platyrhinos species complex. The interpolation is restricted to the current distribution of the species complex approximated by a climatic niche model (Appendix S3, Supporting Information). The shading gradation progresses from green (lowest differentiation among populations) to white (highest differentiation among populations).

Fig. 5

(a) Pairwise comparisons of the first three principal components representing the climatic niche of the Phrynosoma platyrhinos species complex. The red circles and red confidence ellipse represent the current niche, while the blue and green crosses and ellipses represent the LGM niche using CCSM and MIROC simulations, respectively. The black dashed circles in the first plot indicate confidence ellipses around localities belonging to the southern deserts, western Great Basin, and eastern Great Basin, respectively. The larger endpoints of the main loading variables of each principal component are listed along the axis of each principal component. (b) Current and LGM climatic niches of the P. platyrhinos complex with respect to the background points drawn from the respective climates. The niches are represented by ellipses while the background points are represented by symbols.

Fig. 6

Values for (a) the mean temperature of the warmest quarter (Bio10) and (b) the precipitation of the wettest quarter (Bio16) for the current climate and two models of the LGM climate (CCSM and MIROC, respectively). The insets on the right represent a response curve for each variable reconstructed from the current occurrence records of P. platyrhinos using the methodology of ecological niche modeling (see Appendix S3, Supporting Information).