Desert Tortoises in the Genomic Age: Population Genetics and the Landscape

Abstract

The California Department of Fish and Wildlife (CDFW) provided research funds to study the conservation genomics and landscape genomics of the Mojave desert tortoise, Gopherus agassizii, in response to the Desert Renewable Energy Conservation Plan (DRECP). To do this, we consolidated tissue samples of the desert tortoise from across the species range within California and southern Nevada, generated a DNA dataset consisting of full genomes of 270 tortoises, and analyzed the way in which the environment of the desert tortoise has determined modern patterns of relatedness and genetic diversity across the landscape. Here we present the implications of these results for the conservation and landscape genomics of the desert tortoise. Our work strongly indicates that several well-defined genetic groups exist within the species, including a primary north-south genetic discontinuity at the Ivanpah Valley and another separating western from eastern Mojave samples. We also use existing desert tortoise habitat modeling data with a novel extension of genetic \"resistance distance\" using geographic maps of continuous space to predict the relative impacts of five proposed development alternatives within the DRECP and rank them with respect to their likely impacts on desert tortoise gene flow and connectivity in the Mojave. Finally, we analyzed the impacts of each of the 214 distinct proposed development area \"chunks,\" derived from the proposed development polygons, and ranked each chunk in terms of its range-wide impacts on desert tortoise gene flow.\n\n\n\nO_FIG O_LINKSMALLFIG WIDTH=200 HEIGHT=150 SRC=\"FIGDIR/small/195743_ufig1.gif\" ALT=\"Figure 1\">\nView larger version (147K):\norg.highwire.dtl.DTLVardef@b60416org.highwire.dtl.DTLVardef@1c649f2org.highwire.dtl.DTLVardef@120e625org.highwire.dtl.DTLVardef@e59b34_HPS_FORMAT_FIGEXP M_FIG C_FIG PrefaceO_ST_ABSContextC_ST_ABSThe following document is a report that was submitted to the California Department of Fish and Wildlife, describing a series of analyses to help understand the impacts of several alternative spatial configurations of renewable energy development on gene flow of the federally threatened Mojave desert tortoise. These development alternatives were the centerpiece of the Desert Renewable Energy Conservation Plan (DRECP), a landscape-level land use planning initiative undertaken by the Bureau of Land Management (BLM), U.S. Fish and Wildlife Service (USFWS), California Energy Commission (CEC), and the California Department of Fish and Wildlife (CDFW). We were tasked by the California Department of Fish and Wildlife with providing a detailed analysis of these alternative plans on desert tortoise gene flow, and submitted the report for the public comment period for the initial implementation of the DRECP.\n\nFuture PlansO_ST_ABSCurrent state of landscape-level planning for the Mojave desert tortoiseC_ST_ABSThe five proposed land use configuration alternatives analyzed in the subsequent report include public and private lands spread across several counties in California. Shortly after the end of the DRECPs public comment period, the government agencies that developed the DRECP announced that they would be splitting its implementation into two phases: one that deals with land use decisions on BLM-controlled lands and one that deals with non-BLM areas (Sahagun 2015).\n\nPhase I of the DRECP was approved by the Bureau of Land Management on September 14, 2016 (U.S. Bureau of Land Management 2016). This phase includes land use planning decisions for BLM-administered lands. Specifically, 388,000 acres of public lands were designated as development focus areas (DFAs). In applications for leasing lands for renewable energy development, DFAs will not require the same degree of environmental evaluation prior to permitting, as theyve already been evaluated in the context of the DRECP. The application process for renewable energy development within DFAs will be streamlined to encourage development in these areas. Phase I also designated a total of 6,527,000 acres for natural resource conservation. This includes California Desert National Conservation Lands, Areas of Critical Environmental Concern, and Wildlife Allocations. A further 2,691,000 acres were designated for recreation under Phase I. Phase II of the DRECP is currently under development in conjunction with county-level governments to extend this landscape-level planning beyond BLM-administered lands.\n\nAuthor ContributionsThis was a collaborative report. Evan McCartney-Melstad performed the simulations of the low-coverage full genome approach (see Figure 2); conducted all of the laboratory work to generate the genome sequences; performed all of the bioinformatic analyses to bring the raw sequence data to the various stages required for different analyses; wrote the software to quickly estimate pairwise genetic relationships between individuals using read count data in low coverage sequence data (www.github.com/atcg/cPWP); performed some of the population genetic analyses; and wrote and edited several sections of the report.\n\nO_FIG O_LINKSMALLFIG WIDTH=200 HEIGHT=122 SRC=\"FIGDIR/small/195743_fig2.gif\" ALT=\"Figure 2\">\nView larger version (16K):\norg.highwire.dtl.DTLVardef@30a49forg.highwire.dtl.DTLVardef@187c3d8org.highwire.dtl.DTLVardef@4abe98org.highwire.dtl.DTLVardef@126febe_HPS_FORMAT_FIGEXP M_FIG O_FLOATNOFigure 2.C_FLOATNO Comparison of two different sequencing approaches in their ability to differentiate very slightly differentiated populations (Fst=0.001)\n\nC_FIG Peter Ralph (in collaboration with Gideon Bradburd and Erik Lundgren) invented and implemented the random walk-based gene flow model that we used to estimate reductions in gene flow due to development, and also developed the theory behind the read-based pairwise pi and genetic covariance estimation used here, in addition to writing and editing several sections of the report. Gideon Bradburd also performed some of the population genetic analyses and wrote and edited several sections of the report. Jannet Vu collected and curated the spatial environmental data and generated the maps that are included in the report (Figures 10, A10-A13), and also wrote Appendices I and IV. Bridgette Hagerty, Fran Sandmeier, Chava Weitzman, and C. Richard Tracy contributed approximately 1,000 desert tortoise blood samples that they collected (at great effort), in addition to knowledge of tortoise ecology and conservation, as well as the results of previous microsatellite-based genetic analyses and editing of the report. H. Bradley Shaffer wrote and edited several sections of the report, and is listed as the lead author for his role in conceiving of and obtaining funding support for the project.\n\nO_FIG O_LINKSMALLFIG WIDTH=154 HEIGHT=200 SRC=\"FIGDIR/small/195743_fig10.gif\" ALT=\"Figure 10\">\nView larger version (82K):\norg.highwire.dtl.DTLVardef@11e99acorg.highwire.dtl.DTLVardef@1faf2f5org.highwire.dtl.DTLVardef@64c440org.highwire.dtl.DTLVardef@1907837_HPS_FORMAT_FIGEXP M_FIG O_FLOATNOFigure 10.C_FLOATNO Spatial configuration of the proposed development chunks (see Appendix 4).\n\nC_FIG