Genetica 71: 167-173, (1986). 167 © Dr W. Junk Publishers, Dordrecht - Printed in the Netherlands.

Genic variation in the coyote, Canis latrans, in Tennessee, U.S.A.

M. J. Hamilton* & M. L. Kennedy Memphis State University, Department o f Biology, Memphis, TN 38152, USA. *Present address: Department o f Biological Sciences, and The Museum, Texas Tech University, Lubbock, TX 79409, USA.

Abstract

Protein variation, levels of heterozygosity, and interlocality gene variation were studied in the coyote, Canis latrans, using starch gel electrophoresis. Canis latrans were obtained from 27 counties in Tennessee. Eleven of 20 loci examined were found to be polymorphic with the remaining nine loci fixed for the same gene in all populations. Mean heterozygosity (I~) varied from 0.0%0 to 1.9% with a mean of 0.9%. These values are low for a mammal. Significant heterozygote deficiencies occurred in most groups. Results of F-statistics indi- cated a significant degree of population differentiation at four loci (Gdh, Idh-1, Mdh-2, 6-Pgd). Rogers' coefficients of genetic similarity ranged from 0.950 to 1.000 and showed C. latrans to be genetically homoge- nous in that portion of the range investigated.

Introduction

Although the coyote (Canis latrans) has been the subject of many biologic investigations relating primarily to systematic and ecologic questions (Be- koff, 1977), few studies have been directed toward inquiries concerning genetic variability. Previous genetic investigations have attempted to differenti- ate coyotes from domestic dogs or other similar carnivores (e.g., Fisher et al., 1976; Simonsen, 1976; Ferrell et al., 1980). However, little is known about the genetic structure of natural populations of C. latrans.

As the diversity of large mammals has decreased in recent times, few opportunities arise for the study of such species in new areas, especially large carnivores due to the amount of habitat necessary to support such species. However, the southeastern United States presently offers a unique situation for study of C. latrans. Gipson (1978) reported coy- otes to have been absent from states east of the Mississippi River for a period of about 60 years. During the early 1960's and 1970's, the species ex- panded its range into the southeastern United

States (Gipson, 1978). C. latrans has only recently been documented in Tennessee (Smith & Kennedy, 1983). Therefore, this state provides an interesting region in which to examine the genetic structure of an invading carnivore.

The purpose of the present study was to charac- terize the genetic structure of a large carnivore (C. latrans) in an area of recent colonization in relation to protein variation. This investigation should add to our understanding of genetic variability in the Carnivora as well as provide baseline data for fu- ture comparisons of coyotes in the southeastern United States.

Materials and methods

From the spring of 1979 through the winter of 1984, 239 coyotes were obtained from 27 counties in Tennessee. Specimens were provided primarily by trappers, hunters, and Tennessee Wildlife Resources Agency personnel. Animals were trans- ported to the Department of Biology at Memphis State University where liver and kidney samples

168

were removed and frozen for later electrophoretic analysis.

Proteins in both liver and kidney extracts were separated by the horizontal starch gel elec- trophoretic method. Tissue preparation and elec- trophoretic apparatus were similar to those of Selander et al. (1971) and Place & Powers (1978), while buffer systems followed those of Shaw & Prasad (1970), Selander et al. (1971), and Ayala et al. (1972). Staining procedures follow those of Selander et al. (1971) except where otherwise noted. Twenty presumed structural loci were examined: al- bumin (Alb), acid phosphatase (Ap; Harris & Hop- kinson, 1976), esterase-1, -2, and -3 (Es-1, -2, -3), glucophosphate isomerase (Gpt~, glutamate de- hydrogenase (Gdh; Shaw & Prasad, 1970), gluta- mate oxaloacetate transaminase-1, and -2 (Got-l, -2), isocitrate dehydrogenase-1 (Idh-1), lactate dehydrogenase-1, and -2 (Ldh-1, -2), malate dehydrogenase-1, and -2 (Mdh-1, -2), malic enzyme-1 (Me-l; Harris & Hopkinson, 1976), man- nose phosphate isomerase (Mpi; Nichols et al., 1973), peptidase-B (Pept-B, substrate used was leucyl-glycyl-glycine; Lewis & Harris, 1967 ), 6-phosphogluconate dehydrogenase (6-Pgd), phosphoglucomutase-1 (Pgm-1), and superoxide dismutase (Sod; Harris & Hopkinson, 1976). Loci designations primarily follow that of Selander et al.

(1971) with the exception of Es-1, -2, and -3 which follow Dew and Kennedy (1980), and Mpi and Pept-B which follow Harris and Hopkinson (1976). The fastest migrating allele at each locus was as- signed a letter of F and the slower allele was as- signed the letter S.

Specimens were grouped into sampling units (= localities or populations) according to counties. Counties with less than three specimens were pooled with specimens from adjacent counties in the same physiographic region to form a sampling unit for statistical analyses. The resulting 20 locali- ties and sample sizes are presented in Figure 1.

Allele frequencies and estimates of heterozygosi- ty were calculated from direct counts of genotypes. Chi-squared with Yates' correction factor (Sokal & Rohlf, 1981) was utilized to test for departures from Hardy-Weinberg equilibrium. Expected heterozy- gosity was calculated using Levene's (1949) formula for small samples. Genic relationships based on all loci were assessed by Wright's (1965) F-statistics, Rogers' (1972) coefficient of genetic similarity (S), Nei's (1972) genetic identity coefficient, and Hedrick's (1971) genotypic identity coefficient (I). These calculations were made using FORTRAN programs written by R. K. Chesser. Similarity and identity matrices were summarized in the form of dendrograms obtained by an unweighted pair-

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Fig. L Localities used in a study of genie variation in Canis latrans from Tennessee. Locality numbers and sample sizes are as follows: (1) Dyer Co., N = 1, Obion Co., N = 5; (2) Stewart Co., N -- 3; (3) Montgomery Co., N = 1, Robertson Co., N = 3; (4) Chea tham Co., N = 3; (5) Clay Co., N = 4; (6) Carroll Co., N = 6, Weakley Co., N = 1; (7) Benton Co., N = 26; (8) Humphreys Co., N = 2, Perry Co., N = 2; (9) Warren Co., N = 1, Wilson Co., N = 2; (10) Lauderdale Co., N = 4; (11) Tipton Co., N = 27; (12) Haywood Co., N = 16; (13) Madison Co., N = 11; (14) Decatur Co., N = 1, Henderson Co., N = 3; (15) Chester Co., N = 3; (16) Shelby Co., N = 44; (17) Fayette Co., N = 14; (18) Hardeman Co., N = 34; (19) Hardin Co., N = 2, McNairy Co., N = 5; (20) Franklin Co., N = 1, Williamson Co., N = 4. Total N = 239. See text for explanation of grouping method.

169

group method using arithmetic averages (UPGMA) of clustering from Rohlf et al. (1982).

Results

Of the 20 loci examined, nine were monomorphic with all samples fixed for the same allele. Allelic frequencies of the 11 polymorphic loci (frequency of the common allele in at least one population less than 0.99) are presented in Table 1.

For C. latrans, overall mean heterozygosity (171) varied from 0.0o70 to 1.9°70 with a mean of 0.9o70. Observed IZI values for each group are given in Ta- ble 1. Major contributors to heterozygosity were Es-3, Idh-1, and Mdh-2. Significant heterozygote deficiencies occurred in most groups (Table 1) with observed heterozygosity less than expected on the assumption of Hardy-Weinberg equilibrium.

Results of F-statistics indicated a significant de- gree (P < 0.05) of population differentiation (Ta- ble 2) at four loci (Gdh, Idh-1, Mdh-2, 6-PgtO. Of

the total genetic variation found in C latrans, 8.0°7o (Fsa-= 0.079) was due to intergroup gene differ- ences. High positive Fls values (ranging from -0.017 to 1.000) for most loci indicated that on the average there was significant deviation from Hardy- Weinberg equilibrium due to heterozygote deficien- cies within each group. Only the Mdh-1 locus showed a very slight excess of heterozygotes ( F I s = -0.017). High positive F~T values (ranging from 0.005 to 1.000) indicated a greater number of homozygous individuals than would be expected when data are pooled for all groups.

Results of cluster analysis produced from Rogers' coefficient of genetic similarity and Nei's genetic identity values were highly similar; there- fore, only those based on Rogers' coefficient are presented. Values of S ranged from 0.950 to 1.000, while I values ranged from 0.942 to 1.000. Genic relationships of C. latrans based on S and I are depicted in Figure 2. All groups of coyotes appear to be genetically very similar.

Table 1. Allelic frequencies and mean heterozygosities (IZI) for 11 polymorphic loci I of Canis latrans from Tennessee. 2

Locus Allele 1 2 3 4 5 6 7 8 9 10 N = 6 N = 3 N = 4 N = 3 N = 4 N = 7 N = 2 6 N = 4 N = 3 N = 4

Es-3 F 1.00 1.00 1.00 1.00 1.00 1.00 1.00 1.00 1.00 1.00 S

Gdh F 0.83 1.00 0.75 1.00 1.00 0.86 0.81 0.75 1.00 1.00 S 0.17 0.25 0.14 0.19 0.25

Idh-1 F 0.20 0.33 0.20 0.20 0.50 S 0.80 1.00 0.67 1.00 1.00 0.80 0.80 1.00 0.50 1.00

Mdh-1 F S 1,00 1.00 1.00 1.00 1.00 1.00 1.00 1.00 1.00 1.00

Mdh-2 F 1.00 1.00 1.00 1.00 1.00 1.00 1.00 1.00 1.00 1.00 S

6-Pgd F 0.25 0.04 S 1.00 1.00 0.75 1.00 1.00 1.00 0.96 1.00 1.00 1.00

Gpi F S 1.00 1.00 1.00 1.00 1.00 1.00 1.00 1.00 1.00 1.00

Alb F 1.00 1.00 1.00 1.00 1.00 1.00 1.00 1.00 1.00 1.00 S

Got-1 F 1.00 1.00 1.00 1.00 1.00 1.00 0.96 1.00 1.00 1.00 S 0.04

Ldh-I F S 1.00 1.00 1.00 1.00 1.00 1.00 1.00 1.00 1,00 1.00

Ldh-2 F 1.00 1.00 1.00 1.00 1.00 1.00 1.00 1.00 1.00 1.00 S

I7I(%) 3 Observed 0.0" 0.0 0.0" 0.0 0,0 0 .0 ' 0.7* 0 .0 ' 0 .0 ' 0.0 Expected 3.3 0,0 6.9 0.0 0.0 3. I 4.2 2. I 3.4 0.0

1 See text for explanation of loci abbreviations. 2 ~ee text for explanation of locality numbers. a Values marked with a single asterisk (*) indicate a significant difference (P_<0.05).

170

Table 1. Continued.

Locus Allele 11 12 13 14 15 16 17 18 19 20 N=27 N=16 N = l l N=4 N=3 N=44 N=24 N=34 N=7 N=5

Es-3 F 0.90 0.97 1.00 1.00 1.00 0.98 0.94 1.00 1.00 1.00 S 0.10 0.03 0.02 0.06

Gdh F 0.85 0.87 0.91 0.75 0.67 0.91 0.96 0.79 0.86 0.80 S 0.15 0.13 0.09 0.25 0.33 0.09 0.04 0.21 0.14 0.20

ldh-1 F 0.58 0.19 0.29 0.33 0.33 0.13 0.21 0.23 0.25 0.25 S 0.42 0.81 0.71 0.67 0.67 0.87 0.79 0.77 0.75 0.75

Mdh-1 F 0.02 0.13 0.04 0.02 0.04 S 0.98 1.00 1.00 0.87 1.00 0.96 0.98 0.96 1.00 1.00

Mdh-2 F 0.94 0.97 1.00 0.67 1.00 1.00 1.00 0.94 1.00 1.00 S 0.06 0.03 0.33 0.06

6-Pgd F 0.19 0.03 0,14 S 1.00 0.81 1.00 1.00 1.00 1.00 1.00 0.97 0.86 1.00

Gpi F 0.02 0.01 S 0.98 1.00 1.00 1.00 1.00 0.99 1.00 1.00 1.00 1.00

Alb F 1.00 1.00 1.00 1.00 1.00 1.00 1.00 0.97 1.00 1.00 S 0.03

Got-1 F 0.96 1.00 1.00 1.00 1.00 0.98 1.00 1.00 1.00 1.00 S 0.04 0.02

Ldh-1 F 0.03 S 1.00 1.00 1.00 1.00 1.00 1.00 1.00 0.97 1.00 1.00

Ldh-2 F 1.00 1.00 1.00 1.00 1.00 1.00 1.00 0.03 1.00 1.00 S 0.97

lq(%) 3 Observed 1.9" 0.9* 0.0' 1.3' 0.0" 1.0' 0.7* 1.3' 0.0' 0.0' Expected 6.1 4.9 3.0 8.7 5.3 3.1 2.9 5.7 4.7 3.9

Discussion

Little is known about the genetics of C. latrans throughout its distribution. Comparisons of animals from Tennessee (new population) with coy-

Table 2. Results of the analysis of Wright's F-statistics for each variable locus for Canis latrans from 20 locations. Sig- nificance of FST indicated by the Chi-squared value.

Locus a FST X 2 df

Es-3 0.0589 27.67 19 Gdh 0,0856 40.06* 19 Idh-1 0.t509 57,84* 19 Mdh-1 0.0627 27.84 19 Mdh-2 0.2285 103.76" 19 6-Pgd 0.1572 69.18" 19 Gpi 0.0144 6.78 19 Alb 0.0280 13.32 19 Got-1 0.0319 14.72 19 Ldh-1 0.0288 13.26 19 Ldh-2 0.0288 13.26 19 Mean 0.0796 387.50* 209

a See text for explanation of loci abbreviations. * Values marked with a single asterisk (*) indicate a significant

difference (P _< 0.05).

otes from other parts of the range (old population) are not available at this time. However, the degree of variability observed for coyotes in the present study follows the general pattern (low levels of vari- ation) noted for large mammals (Wooten & Smith, 1985). More specifically, our results agree with those of other investigations (e.g., McDermid et al., 1972; Simonsen, 1976; Manlove et al., 1980; O'Brien et al., 1983) which indicate that carnivores exhibit limited protein variation. Of the various hy- potheses offered as explanations for low levels of variability in large mammals (see Bonnell & Selander, 1974; Allendorf et al., 1979; Selander & Kaufman, 1973; Wooten & Smith, 1985), the prem- ise relating lower levels of genetic variability with large, mobile animals (Selander & Kaufman, 1973) appears to be the most applicable to the coyote. However, the relevance of a relationship between body size and genetic variability is uncertain (Wooten & Smith, 1985). The adaptive significance of low levels of polymorphism is poorly under- stood, and just how extensive this lack of protein variation is among the carnivores remains to be confirmed.

0.94 0.00 0.98 S

1.00

r :0 .825 20 7

.•12 19

15

2

8 16

9 11 14

0;94 0.90

r = 0 . 9 7 2

0.g8

I 1.00

12 "[19

2

5 I '° 8

c- 1; 14

18

Fig. 2. Dendrograms of genetic similarity (S) and genotypic identity (I) for Canis latrans from Tennessee.

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Wright's F-statistics measure the amount of genetic heterogeneity among and within popula- tions. Results of the present study indicate a moderate degree of population differentiation (Hartl, 1980). The average differentiation in popu- lations of C. latrans was about 8.00/o (FsT = 0.079) which is similar to values obtained for moose from different Scandinavian countries (9.0%o; Ryman et al., 1980), house mice from different farms (12.0°/0; Nei, 1975), prairie dogs from different wards and coteries (10.0%; Chesser, 1983), and marmots from different colonies (7.0%; Schwartz & Armitage, 1980). However, it is much lower than the values obtained among populations of pocket gophers (41.0°/0; Patton & Yang, 1977). Information con- cerning FsT values for carnivores is sparse at the present time, and it is difficult to evaluate the true nature of the FST value found for C. latrans.

Among populations of coyotes from Tennessee, significant differentiation was observed at four loci. Overall, however, populations were genetically very similar. This similarity could be due to gene exchange between populations, common selective pressures, or an interaction of the two. Crow and Kimura (1970) proposed that one animal dispersing between populations per generation is sufficient to maintain interpopulational homogeneity in allele frequencies. If mobility and dispersal potential of the coyote (Bowen, 1982; Woodruff & Keller, 1982) are considered, gene flow would play a substantial role in maintaining homogeneity among coyote populations in Tennessee.

The present study indicated a pattern of low het- erozygosity within C. latrans and high similarity among populations. However, the study area was within a region only recently invaded by the species (Smith & Kennedy, 1983). Low levels of heterozy- gosity and high similarity may result from coloni- zation and subsequent range expansion (Smith et al., 1977). In this model, a few individuals colonize a new area and form the nucleus for a population from which the next set of colonizers would be ob- tained. Repeated sampling of a series of sequential- ly related populations, each subjected to founder effects, would result in reduced genetic variability and high similarity between groups. At present, genetic information is not available to assess whether coyote populations are genetically equiva- lent thoughout their range or whether genetic variability has been lost in coyotes during the proc- ess of recent range expansion.

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Acknowledgement

We thank M. L. Beck, K. B. Davis, P. K. Kenne- dy, and G. A. Heidt for critically reviewing an earli- er draft of this manuscript. Appreciation is ex- pressed to the following for their assistance in collection of data: R. A. Van Den Bussche, P. K. Kennedy, E W. Weckerly, P. L. Leberg, and G. D. Baumgardner. Personnel from Tennessee Wildlife Resources Agency and Tennessee Valley Authority (Land Between The Lakes) aided in obtaining specimens. We thank M. H. Smith for the opportu- nity to use the facilities at the Savannah River Ecol- ogy Laboratory. This project was funded in part by Federal Aid to Wildlife Restoration, Tennessee Wildlife Resources Agency, W-46R Pittman- Robertson.

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Received 4.6.1985 Accepted in revised form 20.8.1986.