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Evolutionary Genetics of Birds. V. Genetic Distances Within Mimidae (Mimic Thrushes) and Vireonidae (Vireos)

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Evolutionary Genetics of Birds. V. Genetic Distances Within Mimidae (Mimic Thrushes) and Vireonidae (Vireos) Biochemical Genetics, Vol. 20, Nos. 1/2, 1982 Evolutionary Genetics of Birds. V. Genetic Distances Within Mimidae (Mimic Thrushes) and Vireonidae (Vireos) John C. Avise, 1 Charles F. Aquadro, 1 and John C. Patton I Received 22 Apr. 1981--Final 17 June 1981 Genetic distances (D's) between five species within each of the families Mimidae and Vireonidae were estimated from frequencies of protein electro- morphs at 23 loci. For three mimid species in the genus Toxostoma, D equals 0.084 (range, 0.069-0.104); and among three mimid genera, D equals 0.223 (0.167-0.278). These distances typify values previously reported in other birds at comparable levels of taxonomic recognition. In sharp contrast, the mean genetic distance among five congeneric species of Vireonidae is far higher, D = 0.360 (0.027-0.578). One possible explanation for these results is that Vireo species are considerably older, on the average, than are species of Toxostoma or than are members of severai other avian genera assayed to date. Conventional thought about the origin and relative age of the Vireoni- dae appears compatible with this explanation. Although genetic distances in the Vireonidae are large by "avian standards," they remain modest or even small in comparison with distances between many nonavian vertebrate congeners. Results for the Mimidae and the Vireonidae are directly contrasted with genetic distances in well-known genera of Amphibia and Reptilia. KEY WORDS: genetic divergence; protein electrophoresis; phylogeny; Ayes. This research was supported by NSF Grant DEB 7814195 and by a grant from the American Philosophical Society. ' Department of Molecular and Population Genetics, University of Georgia, Athens, Georgia, 30602. 95 0006-2928/82/0200-0095503.00/© 1982 Plenum Publishing Corporation 96 Avise, Aquadro, and Patton INTRODUCTION An emerging generalization from electrophoretic comparisons of structural gene products is that genetic distances within genera and families of birds are usually smaller than genetic distances within most genera and families of nonavian vertebrates. This "conservative" pattern of avian protein divergence has been reported in the Icteridae (Smith and Zimmerman, 1976), Muscica- pidae (Avise et al., 1980a), Emberizidae (Avise et al., 1980b), Parulidae (Barrowclough and Corbin, 1978; Avise et al., 1980c), and Anatidae (Patton and Avise, 1982). The conservative pattern of protein evolution in birds might conceivably be a reflection of the recent origin of many avian species surveyed thus far. In this study we examine genetic distances at 23 loci in five species of vireos (Vireonidae). Vireos represent a relatively ancient group of Passeriformes that one might expect to exhibit large protein differences. Therefore, we hypothesize that the Vireonidae are an excellent group to test the generaliza- tion of conservative protein evolution in birds. Because specimens of "mockingbirds and thrashers" (Mimidae) were available, an opportunity was also provided to examine genetic distances between several species and genera in that family. Genetic distances in birds have been explicitly contrasted with those in selected fish and mamma!s (Avise et al., 1980b,c). Here we will compare the genetic distances of Vireonidae and Mimidae against previously reported distances in representa- tives of two other classes of vertebrates--the reptiles and amphibians. MATERIALS AND METHODS The Mimidae and Vireonidae are compact New World Passeriforme families, comprised of about 31 species (13 genera) and 43 species (4 genera), respectively. [For general taxonomic discussion, we will arbitrarily follow the recent classification of Morony et al. (1975).] The sample of species studied (Table I) was governed solely by the availability of fresh specimens, most of which were TV "tower-kill migrants" kindly donated by staff of the Tall Timbers Research Station, Leon County, Florida. Specimens of Mimus polyglottos, Toxostoma curvirostre, and T. dorsale were collected in Brews- ter County, Texas, and two other specimens of Mimus polyglottos were taken in Athens, Georgia. Standard techniques of one-dimensional starch-gel electrophoresis were used to assay variation in proteins encoded by 23 genetic loci. With slight modifications, the techniques employed, the loci assayed, and their designa- tions are similar to those described in detail by Avise et al. (1980a). Electromorphs were assigned numerical values determined by their mobilities relative to the mobilities of the common electromorph at each locus in Dumetella carolinensis (Mimidae) or Vireo olivaceus (Vireonidae). Only Genetic Distances in Birds 97 Table I. Estimatesof Mean Heterozygosity(H) per Sample, Based on 23 Assayed Loci Species English name Sample size H _+ SE Mimidae (1) Dumetella carolinensis Gray catbird 24 0.018 _+ 0.007 (2) Mimus polyglottos Northern mockingbird 8 0.010 +_ 0.007 (3) Toxostoma rufum Brown thrasher 7 0.048 _+ 0.024 (4) Toxostoma curvirostre Curve-billedthrasher 4 0.000 (5) Toxostoma dorsale Crissal thrasher 1 0.000 Totals 44 0.015 Vireonidae (1) Vireo griseus White-eyedvireo 5 0.036 _+ 0.028 (2) Vireo philadelphicus Philadelphiavireo 1 0.000 (3) Vireoflavifrons Yellow-throatedvireo 4 0.043 _+ 0.026 (4) Vireo solitarius Solitary vireo 16 0.054 _+ 0.021 (5) Vireo olivaceus Red-eyed vireo 58 0.048 _+ 0.015 Totals 84 0.036 intrafamily comparisons were attempted, so shared electromorph designa- tions do not imply electrophoretic identity between the two families. Heterozygosities (H's) were determined by averaging the proportions of heterozygous individuals observed per locus. Genetic similarities (I's) and distances (D's) between species were calculated using Nei's (1972) formulas, and matrices of D were used to generate phenetic dendrograms by UPGMA [unweighted pair-group method of analysis with arithmetic means (Sneath and Sokal, 1973)]. The "fits" of distances implied by the dendrograms to distances in the matrices from which the dendrograms were derived were evaluated by the F statistic of Prager and Wilson (1978). Smaller values of F indicate greater congruence, but any F < 0.10 implies good fit. Several of the species assayed were represented by few individuals (Table I). The use of small sample sizes (when larger samples were unavaila- ble) for the purpose of calculating mean genetic distance between species can be justified on both empirical (Gorman and Renzi, 1979) and theoretical (Nei and Roychoudhury, 1974) grounds. Although larger samples would undoubtedly result in slightly different estimates of D, the magnitude of this sampling bias is trivial when compared against the magnitude of differences in D's among birds, amphibians, and reptiles reported here. RESULTS Genetic Variation For the Mimidae, the per-species counted H was 0.015, and for the Vireoni- dae, H was 0.036 (Table I). Three species (Toxostorna curvirostre, T. 98 Avise, Aquadro, and Patton ss sssss s ss ss ~OOOOO~OOOO OOOOOO I O ~ O o % O r~ I I I O OOO~ ..= I © ? OO c- I I ol Oo O I I c~ OO I I I o o m I I I I I Genetic Distances in Birds 99 dorsale, and V. philadelphicus) lacked detectable variation at the loci assayed, but these species were represented by few individuals (<4). When mean heterozygosities per species are weighted by sample size, values become H = 0.019 and H = 0.048 in the Mimidae and Vireonidae, respectively. The estimates of H for Vireonidae are very close to mean values previously reported in other Passeriformes (Avise et al., 1980c), while estimates of H for the Mimidae average about one-third to one-half as large. Frequencies of alleles in the two families (Table II) form the empirical base for D calculation and for the following brief discussion of genetic relationships. Relationships Within Mimidae The three assayed species of Toxostoma comprise a singl__e branch of the dendrogram and cluster at a low level of genetic distance (D = 0.09; Fig. 1). The samples of Mimus polyglottos from Texas and Georgia shared common MIMIDAE (mimic thrushes) Toxostoma dorsale Toxostoma curvirostre Toxostoma rufum Mimus polyglottos Dumetella carolinensis _•1• Hylocichla mustelina J 1.14 i 1.12 i 1,0i i 0 !8 10!6 I 01.4 I 01.2 I 0 Plethodon (woodland salamanders) ~ fourchensis ouachitae caddoensis ~ glutinosus yonahlossee 1,14 i 1.12 i 1.10 i 01.8 i 01,8 i 01,4 i 012 i 0i Anolis (anole lizards)~ poncensis cristatellus evermanni --~"- - 4 cuvieri I. cybotes 1. |4 I t,12 I 1,10 I 018 I 01,6 I 014 I 01,2 I 0I GENETIC DISTANCE Fig. I. Protein dendrograms of the Mimidae, and of representative salamanders (Plethodon) and lizards (Anolis), plotted on a common scale of Nei's (1972) genetic distance. Data for the subset of closely related species within Plethodon are from Duncan and Highton (1979), and Anolis data are from Wyles and Gorman (1980). Fit to the distance matrix for Mimidae is F = 0.054. I00 Arise, Aquadro, and Patton electromorphs at all loci and hence were lumped for further analyses. In the dendrogram Mimus polyglottos joins Toxostoma at D = 0.19, and Dume- tella carolinensis follows at D = 0.25 to complete the UPGMA array. Many authors have considered the Mimidae to be closely allied to the thrushes, Turdidae [Muscicapidae in the classification of Morony et al. (1975)]. Beecher (1953), for example, classified mimic thrushes (Mimidae) as a subfamily of Turdidae, and several other recent classifications agree (Sibley, 1970). For this reason, we compared all of our samples of the Mimidae to the wood thrush (Hylocichla mustelina) (N = 7). At 23 loci, the mean genetic distance of Hylocichla to the assayed mimids (D = 0.68; Fig. 1) is nearly 2.5 times as large as the greatest assayed distance between any two mimids (D = 0.28 between Dumetella carolinensis and Toxostoma rufum). Earlier, we compared Dumetella carolinensis against seven species of the Turdidae at 25 to 27 loci (Avise et al., 1980a).
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