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Genetic Variability in Striped Skunks (Mephitis mephitis).

ANDREA BIXLER [1]

ABSTRACT--Understanding population genetics is important for increasing both our basic knowlege of wild species and our ability to conserve endangered species. In the Carnivora questions about genetic variability across the order also require population genetic information about more species. I present estimates of polymorphism and heterozygosity in the striped skunk, Mephitis mephitis, an abundant species throughout North America. In two populations in eastern Tennessee the average heterozygosity and polymorphism are, respectively: Cades Cove, 0.038 and 0.11; Knoxville, 0.040 and 0.11. These values are well within the ranges for mammals and are intermediate between values suggested by previous studies of skunks using small numbers of individuals. Possible explanations are discussed.

INTRODUCTION

There is great interest in understanding population genetics in wild animals, primarily in relation to conservation biology. Polymorphism and heterozygosity have been determined mainly for small geographically limited populations of endangered mammals (e.g., Bonnell and Selander, 1974; O'Brien et at., 1983; Dinerstein and McCracken, 1990). However, it is important also to obtain these measurements for other populations, including those that are abundant and widespread. This information would allow for enhanced understanding of population genetics in general, and conservation genetics in particular through comparisons of closely-related taxa in which one has a limited range or is endangered while the other is not.

A comprehensive review by Nevo (1978) showed that average polymorphism (P) and heterozygosity (H) in mammals are the lowest of any class of vertebrates and that vertebrates exhibit lower levels than both plants and invertebrates (mammals, 46 species: P = 0.147, H = 0.0359; vertebrates, 135 species: P = 0.173, H 0.0494; plants, 15 species: P = 0.259, H = 0.0706; invertebrates, 93 species: P = 0.397, H = 0.1123).

There has been substantial debate concerning levels of genetic variability in different groups of mammals (Wooten and Smith, 1985; Hard et al., 1988; Mitton and Raphael, 1990; Merola, 1994). Carnivora purportedly have low variability (e.g., Bonnell and Selander, 1974; O'Brien et at., 1983; for discussion and exceptions, see Fisher et at., 1976; Hartl et at., 1988; Mitton and Raphael, 1990; Merola, 1994). Hard et al. (1988) and Merola (1994) dispute the claim that carnivores generally have low variability, but acknowledge that some carnivore species show low levels of heterozygosity and polymorphism.

Within carnivores members of the family Mustelidae are thought to show low levels of polymorphism, with most species in the range of 0-10%, and heterozygosity, 0-3.3% (Table 1). However, all hut one of the zero values are from a single study (Simonsen, 1982) and higher values have been found for the same species by other researchers (Hard et al., 1988; Evans et al., 1989). Two species have levels well above the average for mammals (least weasel (Musteta nivalis), P = 0.225, H = 0.064, Hartl et at., 1988; American marten (Martes americana), P = 0.33, H = 0.17, Mitton and Raphael, 1990).

The striped skunk (Mephitis mephitis) is abundant throughout North America (Wade Smith and Verts, 1982). However, it has not been well studied. Most work on striped skunks has focused on the northern Great Plains states and adjacent areas of Canada where its home range, activity and dispersal patterns have been examined in an effort to better understand how it may spread rabies (e.g., Sargeant et al., 1982; Lariviere and Messier, 1997). No genetic surveys are available from that or any other area of its geographic range, so the population genetics of the striped skunk are not known. Only two studies have examined allozyme variability in skunks. O'Brien et al. (1989) used the kidney of a single striped skunk from Maryland in a molecular systematic study of black-footed ferrets (Mustela nigripes). They found one polymorphic locus out of 30 presumptive loci examined (P = 0.033, see Table 1). More recently, Dragoo et al. (1993) studied allozymes in heart, kidney and liver tissues of eight striped skunks from sev eral different populations (1 from Kansas, 2 each from two counties in New Mexico, 2 from Texas and 1 from New York). Their purpose was also to examine the systematics of the Mustelidae, and they report the number of polymorphic loci for all eight skunks as a group (not separated by population): 12 polymorphic out of 35 presumptive loci (P = 0.34). This ten-fold higher estimate of polymorphism could be due to the fact that Dragoo et al. (1993) used a much larger number of individuals than O'Brien et al. (1989) or because individuals sampled were from very disparate populations.

A genetic survey of a larger number of skunks from a single population could elucidate whether striped skunks fall into the same range of heterozygosity and polymorphism as other mustelids, carnivores and mammals. In this study I present further allozyme electrophoresis data on average polymorphism and heterozygosity in the striped skunk, Mephitis mephitis (Mephitidae, Dragoo and Honeycutt, 1997; formerly Mustelidae). These data are for two populations in Tennessee, a portion of the species' distribution not previously included in genetic studies.

METHODS

Collection.--Samples came from two populations in Tennessee: Cades Cove, Great Smoky Mountains National Park (n = 15, excluding an additional sample from the son of one animal for reasons of independence) and Knoxville (n = 7). These areas are referred to as populations because they are geographically and topographically separated (Cades Cove is a valley in the mountains southeast of the Tennessee River while Knoxville is northwest of the river and about 32 km away). However, gene flow may occur between the two since the distance separating them is well within the longest known dispersal distance of a striped skunk, 119 km (Sargeant et al., 1982) and skunks are known to be good swimmers (Wilber and Weidenbacher, 1961). Two other skunks trapped in Dubuque, Iowa were also sampled but are not included in the analysis due to the small sample size and non-independence of the samples (a mother-son pair). However, the results from this pair are mentioned anecdotally.

I trapped skunks in Cades Cove and Dubuque; those from Knoxville were trapped by VarmintBusters, an animal control agency. All skunks were anesthetized with a 4:1 mixture of ketamine hydrochloride and xylazine (Rosatte and Hobson, 1983; Servin and Huxley, 1992; R. Greenwood, pers. comm.). I obtained 0.5-2.0 ml blood from each animal by cutting into the quick of the claw and collecting the blood that dripped out in a vacutainer containing EDTA. Stiptik powder was applied to stop bleeding and the skunks were released after they had fully recovered from the anesthetic. Samples were kept on ice until plasma and red blood cells could be separated; both fractions were frozen at -80 C.

Allozyme analysis.--All enzyme systems were resolved using horizontal starch-gel electrophoresis, following methods and recipes in Selander et al. (1971) and McCracken et al. (1993). Blood fraction, buffer systems and proteins are as follows; the number of individuals from the Knoxville population is 7 and the number from Cades Cove is 15 unless noted otherwise: for red blood cells, morpholine citrate buffer, LDH I, II, III, IV, V (Cades Cove n = 11) and GPI (Cades Cove n = 11); tins versene borate buffer, general protein (Cades Cove n = 7). For plasma, Tris-HCI buffer, NP, TO and XDH; morpholine citrate buffer, MDH, PGDH, aGPD I, II, III and Hb (Cades Cove n = 14); tris versene borate buffer, SOD, AID, aNA I, II, III, IV and ADH; tris citrate pH 8.0 buffer, MEP and HBDH I, II; lithium hydroxide buffer, DIA; Poulik buffer, PEP (Cades Cove n = 13).

RESULTS

Polymorphism was identified at three of 28 presumptive loci examined: MDH, Hb and PEP (Table 2). There were no significant deviations from Hardy-Weinberg for the polymorphic loci. No alleles were present in one population and absent in the other, nor were there significant differences between the genotype frequencies in the populations (MDH: [[chi].sup.2] = 3.127, df = 1, P = 0.0770; Hb: [[chi].sup.2] = 0, df = 1, P [greater than] 0.9999; PEP: [[chi].sup.2] = 0.109, df = 1, P = 0.7409). There was an allele difference between the Tennessee populations and the pair of skunks from Iowa: both Iowa skunks possessed an allele at the GP locus that was different than the GP allele of all the skunks in the Tennessee populations.

There was one presumed mother-offspring pair in the Cades Cove population. Individual P174 was trapped with her son, 23; they differed in two out of three polymorphic loci for which they were examined (because the data for P174 and 23 are not independent, skunk 23 was excluded from all calculations). The pair of skunks trapped in Iowa were also presumed to be a mother-son pair; they were identical at all polymorphic loci. Average heterozygosity and polymorphism are, respectively: Gades Cove, 0.044 and 0.11 and Knoxville, 0.045 and 0.11.

DISCUSSION

This study suggests that striped skunks show levels of polymorphism and heterozygosity consistent with other studies of Mephitidae and Mustelidae [respectively, the family in which they are now placed (Dragoo and Honeycutt, 1997) and the family in which they were previously included; see Table 1] and other mammals (Nevo, 1978) and show slightly higher levels than the average for terrestrial carnivores (Merola, 1994). The present study includes few loci (28) and even fewer individuals (7 in one population and 7-15 in the other) but it is by far the largest study to date on population genetics of striped skunks.

My estimate of polymorphism is much higher than that of O'Brien et al. (1989), probably because they sampled only one individual, and much lower than that of Dragoo et al. (1993), probably because, although they sampled only eight individuals, these animals came from several different populations (I should note again that the intent of both these studies was not to estimate genetic variability but to develop phylogenies). However, it is possible that the populations of striped skunks I sampled are different than those studied previously. It is impossible to tell how diverse the habitats were of the skunk populations Dragoo et al. (1993) sampled in New Mexico, Kansas and Texas. However, Knoxville and Cades Cove contain various habitat types and animals living there might be expected to show genetic variation because of this. Knoxville is a suburban area in which the habitat may include farms and parks as well as apartments and shopping malls; not only is the structure of the habitat quite variable but food an d den availability and abundance of predators and competitors would vary greatly within the area. Cades Cove is also a heterogeneous environment including riparian and hillside forests, fields, campgrounds, picnic areas and parking lots. Temporal variability could also strongly affect skunks in Cades Cove because tourist season (primarily late spring through fall) leads to a large influx of people, cars and, potentially, food. I should also note that my assumption that Cades Cove and Knoxville represent two separate populations may be erroneous; as mentioned above, there may be gene flow between the two areas. This would mean that I sampled 14-22 individuals from one population in an extremely heterogeneous habitat and should expect greater genetic variability.

Striped skunks in the two sampled populations in Tennessee have relatively high levels of polymorphism and heterozygosity compared to many Mustelidae. These levels of genetic variability are comparable to those of other mammals (P = 0.147, H = 0.0359, Nevo, 1978) and are intermediate between results from the two previous studies of striped skunks (both of which used much smaller sample sizes). This study, therefore, provides further information about a little-known species and contributes data relevant to the larger issue of genetic variability within different taxonomic groups.

Acknowlegements.--J. L. Gittleman, G. Burghardt, A. C. Echternacht and C. F. McCracken provided advice throughout this study. J. New suggested the technique for obtaining blood. G. F. McCracken allowed me to use his allozyme laboratory and made comments on this manuscript. L. Comeaux, S. Z. Guffey and S. Maclain helped with allozyme analysis and interpretation; J. M. Harris and F. B. Schnee also provided support. Z. Tang-Martinez, R. H. and M. M. Bixler and two anonymous reviewers provided valuable comments on this manuscript. J. Kopp and family gave me access to the skunks on their property in Iowa, R. Wolfe of VarmintBusters provided me with Knoxville skunks and he and J. Wolfe generously allowed me to bleed animals at their home, even when they were expecting guests. Funding was provided by the Department of Ecology and Evolutionary Biology (formerly the Department of Zoology), University of Tennessee, Knoxville; a Theodore Roosevelt Memorial Fellowship from the American Museum of Natural History; and a C arlos Campbell Memorial Fellowship from the Great Smoky Mountains Conservation Association.

(1.) Present address: Department of Biology, University of Missouri-St. Louis, 8001 Natural Bridge Road, St. Louis 63121. Telephone: (314)516-6211; FAX (314)-516-6233; e-mail: abixler@jinx.umsl.edu

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Levels of genetic variability reported for mephitids and mustelids. N = number of individuals, Loci = number of loci examined, H = average heterozygosity, P = polymorphism. Values of H and P marked with an asterisk were calculated from raw data given in the reference; all other values are those reported by the author(s) of the paper cited
Species                N Loci   H        P
(Conepatus chinga)     2  35   --       0.26 [*]
(C. mesoleucus)        3  35   --       0.37 [*]
(Ictonyx striatus)     1  36  0.028 [*]  --
(Martes americana)    10  24  0.17      0.33
(M. foina)           121  15  0         0
(M. foina)             3  31  0.057     0.019
(M. martes)            2  15  0         0
(Meles meles)          5  15  0         0
(Meles meles)          2  31  0.014     0.029
(Meles meles)        170  23   --       0.087 [*]
(Mephitis macroura)    2  35   --       0.29 [*]
(M. mephitis)          1  30  0.033 [*]  --
(M. mephitis)          8  35   --       0.34 [*]
(M. mephitis)         15  28  0.044     0.11
(M. mephitis)          7  28  0.045     0.11
(Mustela erminea)     39  15  0         0
(Mustela erminea)      3  31  0.033     0.075
(M. nigripes)         12  46  0.008     0.02
(M. nigripes)         22   3  0         0
(M. nivalis)          13  15  0         0
(M. nivalis)          19  31  0.064     0.225
(M. putorius)         24  15  0         0
(M. putorius)         16  31  0.029     0.100
(Spilogate putorius)   2  35   --       0.20 [*]
Species              Reference
(Conepatus chinga)   Dragoo et al., 1993
(C. mesoleucus)      Dragoo et al, 1993
(Ictonyx striatus)   O'Brien et al, 1989
(Martes americana)   Mitton and Raphael, 1990
(M. foina)           Simonsen, 1982
(M. foina)           Hartl et al, 1988
(M. martes)          Simonsen, 1982
(Meles meles)        Simonsen, 1982
(Meles meles)        Hartl et al., 1988
(Meles meles)        Evans et al., 1989
(Mephitis macroura)  Dragoo et al, 1993
(M. mephitis)        O'Brien et al., 1989
(M. mephitis)        Dragno et al, 1993
(M. mephitis)        this study, Cades Cove pop'n
(M. mephitis)        this study, Knoxville pop'n
(Mustela erminca)    Simonsen, 1982
(Mustela erminea)    Hartl et al., 1988
(M. nigripes)        O'Brien et al., 1989
(M. nigripes)        Kilpatrick et al., 1986
(M. nivalis)         Simonsen, 1982
(M. nivalis)         Hartl et al., 1988
(M. putorius)        Simonsen, 1982
(M. putorius)        Hartl et al., 1988
(Spilogate putorius) Dragoo et al., 1993
                Allele frequencies and sample sizes for the
                 polymorphic loci found in two populations
                      of striped skunks in Tennessee
Locus Allele Cades Cove  n Knoxville n
MDH     a       0.67    16   0.36    7
        b       0.33         0.64
Hb      a       0.07    15   0.07    7
        b       0.93         0.93
PEP     a       0.46    14   0.36    7
        b       0.54         0.64
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Author:BIXLER, ANDREA
Publication:The American Midland Naturalist
Article Type:Statistical Data Included
Geographic Code:1U6TN
Date:Apr 1, 2000
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