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Population Genetics of the Endangered Giant Kangaroo Rat

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Population Genetics of the Endangered Giant Kangaroo Rat Population Genetics of the Endangered Giant Kangaroo Rat, Dipodomys ingens, in the Southern San Joaquin Valley Nicole C. Blackhawk, B.S. A Thesis Submitted to the Department of Biology California State University, Bakersfield In Partial Fulfillment for the Degree of Masters of Science Summer 2013 Copyright By Nicole Cherri Blackhawk 2013 Summer 2013 Population Genetics of the Endangered Giant Kangaroo Rat, Dipodomys ingens, in the Southern San Joaquin Valley Nicole C. Blackhawk This thesis has been accepted on behalf of the Department of Biology by their supervisory committee: 1 Population Genetics of the Endangered Giant Kangaroo Rat, Dipodomys ingens, in the Southern San Joaquin Valley Nicole C. Blackhawk Department of Biology, California State University, Bakersfield Abstract The Giant Kangaroo Rat (Dipodomys ingens) is a federally and state-listed endangered species, endemic to the San Joaquin Valley, Carrizo and Elkhorn Plains, and the Cuyama Valley. Populations of the endangered Giant Kangaroo Rat (Dipodomys ingens) have decreased over the past 100 years because of habitat fragmentation and isolation. Changes in the population structure that can occur due to habitat fragmentation can significantly affect the population size and the dispersal of these animals. Dr. David Germano and I collected small ear clippings from male and female Giant Kangaroo Rats from six sites along the southern San Joaquin Valley to determine the genetic population structure of this species in this part of their range. We predicted that geographic distance and isolation of populations would decrease genetic relatedness compared to populations closer together. Having a better understanding of the genetic structure in this species will help with conservation actions, such as translocating individuals within the range of the species. These data were compared to published estimates of genetic diversity of Giant Kangaroo Rats in the Carrizo Plain to the west and the Panoche area to the north, the other large population centers of this species. 2 Table of Contents Page List of Tables………………………………………………………………………….. 4 List of Figures………………………………………………………………...……….. 5 CHAPTER 1: Species Background and Purpose of the Study……………...…. … 7 Literature Cited………………………………………………………………………... 21 CHAPTER 2………………………………………………………………………….. 24 Population Genetics of the Endangered Giant Kangaroo Rat, Dipodomys ingens, in the Southern San Joaquin Valley Introduction……………………………………………………………………………. 25 Methods and Materials………………………...……………………………………… 27 Results…………………………………….…………………………………………… 30 Discussion……………………………….…………………………………………….. 33 Acknowledgements……………………………………………………………………. 39 Literature Cited………………………………………………………………………... 39 List of Figures…………………………………………………………………………. 48 CHAPTER 3: Conservation Actions and the Reassessment of Giant Kangaroo 54 Rat Habitat Occupancy…..………………………………………………………….. Genetic Rescue……………………….……………………………………………….. 57 Translocation as a Conservation Tool………………………………………………… 59 Effects of Habitat Fragmentation……………………………………………………… 63 Reassessment of Habitat Occupancy………………………………………………….. 65 Conclusions…………………………………………………..……………………….. 67 Acknowledgements………………………………………………………………….... 69 Literature Cited………………………………………………………………………... 70 3 List of Tables CHAPTER 2 TABLE 1………………………………………………………………………..……. 42 Observed allele frequencies by locus and population of Giant Kangaroo Rat (Dipodomys ingens) from the southern San Joaquin Valley, California TABLE 2…………………………………………………………………..…………. 44 Descriptive statistics for six populations across seven loci, including the mean sample size (n), proportion of polymorhphic loci (P), number of alleles (NA), number of effective alleles (Ne), information index (I), observed heterozygosity (Ho), expected heterozygosity (HE), the mean number of private alleles, and the fixation (F) indices of Giant Kangaroo Rat (Dipodomys ingens) from the southern San Joaquin Valley, California TABLE 3…………………………………………………………………..…………. 45 Population comparisons of six populations of Giant Kangaroo Rat (Dipodomys ingens) in the southern San Joaquin Valley using an analysis of molecular variance (AMOVA) TABLE 4…………………………………………………………………..…………. 46 Estimates of F-statistics across six populations of Giant Kangaroo Rat (Dipodomys ingens) in the southern San Joaquin Valley by locus FIS: standard genetic variation within populations; FST: standard genetic variation between populations; FIT: to partition genetic variation TABLE 5……………………………………………………………..………………. 47 Pairwise values of FST, ΦPT, and Nei’s genetic distance for six populations of Giant Kangaroo Rat (Dipodomys ingens) in the southern San Joaquin Valley, California 4 List of Figures CHAPTER 1 FIGURE 1……………………………………………………………………. 8 The Giant Kangaroo Rat (Dipodomys ingens). This individual was caught at a study site (North Lokern) west of Buttonwillow, Kern County, California, in the southern San Joaquin Valley. (Photographed by Nicole Blackhawk). FIGURE 2……………………………………………………………………. 13 The pictures show the differences in appearance of a normal seed cache (A) of the Giant Kangaroo Rat (Dipodomys ingens) compared to a population that has been experiencing food shortage (B). (Photographed by Nicole Blackhawk). FIGURE 3……………………………………………………………………. 15 Locations of Giant Kangaroo Rat (Dipodomys ingens) populations sampled for this project (orange triangles). The green triangles indicate the populations sampled previously by Good et al. (1997) and Loew et al. (2005). The grey shading indicates the species’ historic range (IUCN 2012). FIGURE 4……………………………………………………………………. 17 Three sites in the Lokern area of the southern San Joaquin Valley where I collected genetic samples of Giant Kangaroo Rats (Dipodomys ingens). A: North Lokern study site. B: Study site south of the North Lokern site. C: Study site south of Buttonwillow, California on the southeast portion of the Lokern. (A and C photographed by David J. Germano; B photographed by Nicole Blackhawk). FIGURE 5……………………………………………………………………. 19 Two sites in the southern San Joaquin Valley where I collected genetic samples of Giant Kangaroo Rats (Dipodomys ingens). A: Midway study site. B: Study site northwest of Midway site and southwest of the Lokern sites. (Photographed by David J. Germano). FIGURE 6……………………………………………………………………. 20 The northern most site (Northwest Belridge study site) where I collected genetic samples from Giant Kangaroo Rats (Dipodomys ingens) in the southern San Joaquin Valley. (Photographed by David J. Germano). 5 CHAPTER 2 FIGURE 1……………………………………………………………………. 49 Locations of Giant Kangaroo Rat (Dipodomys ingens) populations sampled for this project (orange triangles). The green triangles indicate the populations sampled previously by Loew et al. (2005). The grey shading indicates the species’ historic range (IUCN 2012) FIGURE 2……………………………………………………………………. 50 Locations of Giant Kangaroo Rat (Dipodomys ingens) populations sampled for this project (orange triangles). The grey shading indicates the species’ historic range (IUCN 2012) FIGURE 3……………………………………………………………………. 51 Visualization of Mantel test for geographic distance (GGD) vs. pairwise population ΦPT (PhiPTP) for six populations of Giant Kangaroo Rat (Dipodomys ingens) in the southern San Joaquin Valley, California FIGURE 4……………………………………………………………………. 52 Visualization of the percentage variation explained by the first three axes of the Principal Coordinate Analysis of six populations of Giant Kangaroo Rat (Dipodomys ingens) in the southern San Joaquin Valley, California FIGURE 5……………………………………………………………………. 53 UPGMA tree based on a pairwise population matrix of Nei’s genetic distances for six populations of Giant Kangaroo Rat (Dipodomys ingens) in the southern San Joaquin Valley, California CHAPTER 3 FIGURE 1…………………………………………………………………….. 66 The historic range of the Giant Kangaroo Rat (Dipodomys ingens). The red triangles represent the places that I traveled to that did not have Giant Kangaroo Rats present and the green graduated circles represent location and size of known populations that have been genetically sampled. The grey shading represents the species’ historic range (IUCN 2012). 6 CHAPTER 1 Species Background and Purpose of the Study Kangaroo rats (Dipodomys sp.) are rodents in the family Heteromyidae, which consists of six genera. The Heteromyidae is a group of small to medium sized rodents that occur primarily in deciduous thorn-scrub and arid-adapted habitats in North America (Alexander and Riddle 2005), and they exhibit an array of ecomorphological types (Hafner et al. 2007). The six genera are traditionally placed into three subfamilies: Heteromyinae, Perognathinae, and Dipodomyinae. Dipodomyinae is made up of two genera: Dipodomys, the kangaroo rats, and Microdipodops, the kangaroo mice. There are 21 recognized species of Dipodomys (Goldingay et al. 1997; Cooper and Randall 2007; Prugh and Brashares 2010) and California has the greatest diversity of kangaroo rats of any state (Grinnell 1922) with 13 species, of which there are 23 subspecies endemic to the state (Goldingay et al. 1997). This high diversity is likely due to the climatic history and geomorphic processes along the crustal plates extending the length of the state (Goldingay et al. 1997). Using genetic data, Hafner et al. (2007) affirmed the monophyly of Heteromyidae. Alexander and Riddle (2005) used maximum-likelihood, Bayesian, and maximum parsimony analyses of sequence data from two mitochondrial DNA genes, cytochrome oxidase subunit 3 gene, and cytochrome-b gene to determine phylogenetic relationships
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