Mar 7, 2017 - in Atlantic Canada. Canadian Journal of Zoology,. 70:106-114. SWOFFORD, D. L. ... the island fox, Urocyon tittoratis. Evolution, 45:1849-1868.
DISPERSAL ABILITIES AND GENETIC POPULATION STRUCTURE OF INSULAR AND MAINLAND ORYZOMYS PALUSTRIS AND PEROMYSCUS LEUCOPUS JANET
L.
LOXTERMAN, NANCY D. MONCRIEF, RAYMOND D. DUESER, CHARLES R. CARLSON, AND JOHN E PAGELS
Department of Biology, Virginia Commonwealth University, Richmond, VA 23284 (JLL and JFP) Virginia Museum of Natural History, Martinsville, VA 24112 (JU and NDM) Department of Fisheries and Wildlife, Utah State University, Logan, UT 84322 (RDD and eRe) Long-Tenn Ecological Research Program, University of Virginia, Charlottesville, VA 22903 (eRe)
A comparative hierarchical approach was used to examine allozymic variability within and among nine populations of Oryzomys palustris (marsh rice rat) and seven populations of Peromyscus leucopus (white-footed mouse) from the Virginia barrier islands and southern Delmarva Peninsula. O. palustris is an effective disperser over water and is present on 21 of 24 islands. In contrast, P. leucopus is a less effective disperser over water and occurs on only four of 24 islands. Of 31 loci, four were variable in O. palustris; six were variable in P. leucopus. The nine populations of O. palustris had an average heterozygosity of 2.4% with 6.7% polymorphic loci. For seven populations of P. leucopus, the average heterozygosity was 3.6% with 12.3% polymorphic loci. Both species had lower levels of variation among mainland populations than among island populations. Populations of P. leucopus exhibited considerable genetic differentiation (FST = 0.180) and lower levels of gene flow (Nm = 1.14) among populations, whereas O. paiustris had moderate levels of differentiation (FST = 0.135) and higher levels of gene flow (Nm = 1.60) among populations. Mantel tests indicated a significant relationship between genetic distance and geographic distance in Oryzomys but not in Peromyscus.
Key words: Oryzomys, Peromyscus, gene flow, dispersal, island biogeography, allozymes, isolating mechanisms Studies of island-dwelling organisms have long played an important role in testing evolutionary theory about patterns and processes related to genetic variation in natural populations (Ashley and Wills, 1987, 1989; Berry, 1986; Gill, 1976; Heaney, 1986; Kilpatrick, 1981; Schmitt et aI., 1995; Stewart and Baker, 1992; Wayne et aI., 1991). Populations on islands can provide an elegant model of genetic divergence in continental populations because of their smaller population sizes and geological histories that are often datable (Wayne et aI., 1991). Islands also often afford an opportunity to study population structures in which there is reduced exchange between subpopulations and for which there are sequential relationships between subpopulaJournal of Mamma logy, 79(1):66--77,1998
tions in space and time (Schmitt et a1., 1995). Furthermore, phenomena associated with island systems, including fragmentation of habitats and populations, local extinction, dispersal, and colonization, are important issues in conservation biology (A vise, 1992; Falk and Holsinger, 1991; Hanis, 1984; Hastings and Hanison, 1994; Shafer, 1990). Genetic variation, as measured by average heterozygosity and allelic diversity, is expected to be lower in island populations than in mainland populations of similar size (Berry, 1986; Browne, 1977; Kilpatrick, 1981; Wayne et aI., 1991). Both isolation by physical baniers to dispersal and isolation by distance among subpopulations may reduce gene flow thereby increasing in66
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LOXTERMAN ET AL.-GENE FLOW IN SYMPATRIC RODENTS
breeding and genetic drift (Ashley and Wills, 1987; Wayne et ai" 1991), Genetic diversity should be greater on larger and closer islands than on smaller and more isolated islands (Browne, 1977; Kilpatrick, 1981). Species with greater vagility also are expected to be less affected genetically by increased isolation than are less mobile species (Kilpatrick, 1981; Lomolino, 1986). Oryzomys palustris and Peromyscus leucopus were chosen to compare and contrast evolutionary forces influencing genetic structure of populations on the Virginia barrier islands. O. palustris, the marsh rice rat, typically is associated closely with water (Forys, 1990; Forys and Dueser, 1993; Wolfe, 1982) and inhabits grasslands and wetlands, both of which are present on all of the Virginia barrier islands. Rice rats occur on 21 of 24 barrier and marsh islands (Dueser, 1990, in litt.; Dueser et aI., 1979) and are ubiquitous on the mainland of the Delmarva Peninsula. This semi-aquatic species readily crosses large expanses of open water (Esher et al., 1978; Forys and Dueser, 1993). P. leucopus, the white-footed mouse, typically occurs in wooded upland habitats (King, 1968; Webster et aI., 1985). Wbitefooted mice inhabit only four islands: Assateague, Cedar, Fishermans, and Wallops (Dueser, 1990, in litt.; Fig. I), although this species is common in forests and fields on the mainland of the Delmarva Peninsula. Relative to O. palustris, water is a formidable physical barrier to dispersal for P. leucopus (Carter and Merritt, 1981; Savidge, 1973). This species does not readily enter water and does not possess adaptations for over-water dispersal (Carter and Merritt, 1981). We used a comparative hierarchical approach to characterize allozymic variation within and among populations of O. palustris and P. leucopus from the Virginia barrier islands and southern Delmarva Peninsula. Sampling proximal mainland areas and adjacent islands allowed direct assessment of effects of physical barriers to dispersal (and measurement of gene flow) be-
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tween comparable sites under comparable environmental regimes. The primary objectives were to assess relative levels of gene flow and genetic differentiation among subpopulations and to gain insight into evolutionary factors affecting genetic variation in these two species, which have demonstrably different dispersal abilities. Both species should exhibit increased genetic differentiation within and decreased gene flow among island populations relative to mainland populations. Gene flow should be reduced and genetic differentiation should be increased among populations of P. leucopus as a result of geographic barriers to dispersal (e.g., water). In contrast, O. palustris should have higher levels of gene flow and corresponding decreased genetic differentiation among populations (relative to P. leucopus) because water is not a substantial barrier to dispersal for marsh rice rats. MATERIALS AND METHODS
The study area was the southern Delmarva Peninsula and the Virginia barrier islands (Fig. 1), which extend 150 Ian along the seaward margin of the peninsula. These islands were formed in the late Holocene (Oertel and Kraft, 1994) and are isolated by deep inlets, tidal lagoons, and salt marshes (Dueser, 1990). The primary vegetative cover includes a variety of marsh and dune grasses (Spanina) and shrub thickets; only a few islands support maritime forests (McCaffrey and Dueser, 1990). This tide-dominated banier lagoon system is subject to frequent storms; islands often are overwashed, creating a dynamic ecological and evolutionary environment (Hayden et al., 1991; Oertel and Kraft, 1994). Oryzomys pallistris (n = 118) from nine sites (Fig. 1; sites 1-9) and Peromyscus leucoplls (n = 96) from seven sites (Fig. 1; sites 1-7) were analyzed (Table I); vouchers of all individuals were deposited in the Manunal Collection of the Virginia Museum of Natural History. Sampling sites were selected to represent northern, middle, and southern portions of the mainland and adjacent barrier islands to allow analysis of allelic frequency data by region. Representative pairs of island and mainland sites were used to assess
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' 1.0, and the middle region had an N m of 4.30 (Table 3). Gene flow calculated among the four mainland samples only was 4.40 migrants per generation.
3.-F-statistics analysis for each variable locus and estimated rate of gene flow (NnJ for
Oryzomys palustris from populations in three regions of the Virginia barrier islands and southern Delmarva Peninsula; significance of FST tested with the chi-square statistic. Location
Locus
Northern region (2 samples)
Mean Middle region (4 samples)
FIT
F"
6PGD
0.648
NP ADA
0.523 0.018 0.296
0.518 0.522 0.012 0.224
PGM3 6PGD
NP ADA Mean Southern region (3 samples)
PGM3 6PGD
NP ADA Mean **P < 0.01, *"''''P < 0.001.
1.000 -0.011
0.209 0.080 0.148 -0.007 -0.024 -0.068 0.026 0.002
1.000 -0.043 0.184 0.019
0.098 -0.020
-0.043 -0.145 -0.164 -0.146
Frr
0.271 0.002 0.006
chi-square
0.093
13.235*** 0.076 0.657 13.968**
0.064 0.032 0.031 0.062 0.055
5.960 2.948 3.198 12.300 24.406
0.013 0.019
0.930 1.389 5.460 22.394*** 30.173***
0.068 0.163 0.129
df
N.
2 4
2.44
3 3 3 6 15
4.30
2 2 2 4 10
1.69
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TABLE 4.-F~statistics analysis for each variable locus and estimated rate of gene flow (Nm) for Peromyscus leucopusfrom seven populations combined; significance ofFsT tested with the chi-square
statistic. Location
All regions (7 samples)
Locus
G6PD PGMI PEPA MPI NP CK2
Mean
*** p
