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Comparative phylogeography in North American birds.

The study of geographic variation provides a glimpse of evolution at its most basic spatial level (Gould and Johnston 1972). Modern studies of geographic variation emphasize molecular techniques, as investigators search for spatial patterns of genetic variation that can be interpreted in the context of evolutionary models. This endeavor, using phylogenetic analyses of intraspecific mitochondrial DNA (mtDNA) variation, was aptly termed "phylogeography" by Avise et al. (1987; see also Avise 1989). One can examine phylogeographic patterns of mtDNA variation, and evaluate the relative roles of gene flow, bottlenecks, and historical or ecological barriers in effecting spatial patterns. Another refinement in the study of geographic variation is the comparison of broadly codistributed (sympatric) species (Cracraft 1989), or comparative phylogeography. This endeavor has parallels with historical biogeography (Wiley 1988). For example, Arise (1992) documented a congruent phylogeographic pattern in the mtDNA genomes of several vertebrate and invertebrate species that inhabit southeastern North America. Avise concluded that a common historical event separated the Atlantic and Gulf coast gene pools of an ancestral community of North American species. Study of any one species by itself would not reveal whether such a pattern was general. In this paper, I provide a general overview of comparative phylogeography and illustrate the approach with empirical examples from the North American avifauna.

COMPARATIVE PHYLOGEOGRAPHY: OVERVIEW

The null hypothesis of comparative phylogeography is unresolved. Drawing an analogy from historical biogeography (e.g., Wiley 1988), one could test whether currently codistributed species exhibit congruent geographic patterns of genetic variation, which might be predicted because a given area has but a single history (see Cracraft 1988). That is, one could examine each species' haplotype phylogeny for congruent geographic patterns. A first-order explanation (e.g., parsimony) of congruence would be that historically codistributed species responded in similar ways to isolating barriers (Wiley 1988). The question of whether to expect congruence for phylogeographic (within-species) comparisons is not clear, owing to the potentially shorter time scale than that considered by historical biogeographers. The views of some palcoecologists on the stability of communities suggest a hypothesis of incongruence, because "Communities have broken up and reformed in different configurations repeatedly and regularly on time scales of a few thousand years" (Bennett 1990). Davis (1983) documents major North American habitat shifts less than 20,000 ybp. Given these observations, one might not expect congruent patterns among species because community membership has not been stable for sufficiently long periods of time to allow development of phylogeographic structuring. Fluctuating community membership might especially be true for groups of organisms such as north temperate birds, which likely recently recolonized glaciated areas. However, given that ecogeographic trends such as Bergmann's rule (e.g., James 1991) are apparent in the phenotypes of many vertebrates including temperate-breeding bird species, parallel patterns of (genetic) phylogeography might be expected to exist.

The choice of species compared is important in comparative phylogeography and biogeography. If one compared only species in a genus or single habitat type, the results of the study might have limited generality. The more taxonomically, geographically, and ecologically diverse the species compared, the more general the results will be. For example, the phylogeographic congruence documented by Avise (1992) was apparent in a diverse array of organisms, including a terrestrial bird, marine invertebrates, freshwater fishes, and marine fishes. In fact, if one were to suggest comparison of such diverse taxa a priori, concern might be raised over whether the species were truly comparable. Conversely, when such a diverse group of species shows a common phylogeographic pattern, it becomes a strength of the study. In the Avise study, the taxonomic diversity of species showing the pattern suggests a pervasive vicariant event. I suggest that a priori, the only prerequisite for comparing species is that they are currently codistributed (i.e., sympatric) over a reasonably large area that includes different habitats, and potential environmental or geological barriers (i.e., regions with ostensibly different histories, analogous to areas of endemism in biogeography). Although one might argue that only species with congruent phylogeographic patterns are "truly comparable," this is a result, not a prediction, of comparative phylogeographic analysis. Eliminating species from comparison a priori, because they were not "comparable" for some reason (e.g., habitat), reduces the chance of finding general patterns.

An underappreciated aspect of both phylogeography and biogeography is the comparison of all codistributed species, whether or not they exhibit congruent patterns. Incongruent, or idiosyncratic (Lamb et al. 1992), patterns of differentiation are strong evidence of different histories. Incongruent patterns could result from species' differences in: response to barriers or selective gradients, levels of gene flow, rates of molecular evolution, effective population size or generation time. That is, species might have been historically codistributed, but variable responses to historical events produced conflicting phylogeographic patterns. Species recently colonizing an area might not exhibit phylogeographic patterns simply because of insufficient time in situ for differentiation, and because vicariant events evident in some species simply preceded their arrival in the community. For example, Wenink et al. (1994) found that the dunlin (Calidris alpina) exhibited extensive geographic differentiation in mtDNA sequences whereas the similarly distributed turnstone (Arenaria interpres) was essentially unstructured. Wenink et al. postulated that the turnstone recently expanded from a refuge in which its population was bottlenecked, which would explain its lack of phylogeographic structure. If study of additional species revealed extensive incongruence, it would support the paleoecological view of shifting community membership.

Molecular methods provide a means of discerning alternative reasons for incongruence. For example, if a species has only recently colonized the region being studied, there are often genetic signatures (Rogers and Harpending 1992). Species without phylogeographic structure might be found to have higher rates of dispersal. The turnstone had low levels of genetic variability, suggestive of a recent bottleneck (Wenink et al. 1994); perhaps its dispersal rate would prevent future differentiation. Thus, the reasons for incongruence can sometimes be discerned because in addition to geographic patterns, phylogeographic studies yield information on levels of genetic variation, gene flow, population structure, all factors important in the evolution of geographic variation.

Comparison of individual phylogeographies offers insight into the recent histories of communities. If many species in a community exhibited evidence of common responses to historical events (Avise 1992), one could infer a long history of co-association of the component species. One might then ask questions about co-evolution (Brooks and McLennan 1991). Some studies (Bowen and Avise 1990; Lamb et al. 1992) have not found congruent patterns. Therefore, additional empirical studies are required to determine whether communities typically exhibit (1) a congruent pattern in a diverse group of species indicative of common history (Avise 1992), (2) relatively small groups of species each of which responded to different events at different times, producing "tiers" or layers of historical diversification, or (3) more-or-less random assemblages of species with different histories, and recently arrived, nondifferentiated forms. Each of these outcomes can reflect different degrees of species' stability in communities.

COMPARATIVE PHYLOGEOGRAPHIES OF NORTH AMERICAN BIRDS

To illustrate the comparative phylogeographic approach, I compared the geography of mtDNA variation in five bird species: the Canada goose (Branta canadensis, Anserinae; Van Wagner and Baker 1990), chipping sparrow (Spizella passerina, Emberizinae; Zink and Dittmann 1993a), song sparrow (Melospiza melodia, Emberizinae; Zink and Dirtmann 1993b), fox sparrow (Passerella iliaca, Emberizinae; Zink 1994), and red-winged blackbird (Agelaius phoeniceus, Icterinae; Ball et al. 1988). These species provide a limited test of general patterns, because only birds were compared, including four passerine and one nonpasserine (Canada goose) species (although three subfamilies are represented). Several factors suggest that these species are "comparable." These species are widespread and codistributed across substantial regions of North America [ILLUSTRATION FOR FIGURE 1 OMITTED], and they occur on opposite sides of major barriers. Each species occupies somewhat different habitats, but if vicariance events fragmented ancestral biotas, then codistributed taxa would have been similarly affected irrespective of their habitat affinities or taxonomic affiliation (Avise 1994, Wiley 1988). The species are each currently considered single biological species (AOU 1983). Species were selected at random in the sense that they were not surveyed initially to test a general phylogeographic hypothesis. These species were subjected to more comprehensive molecular analyses over a wider continental area than any other species studied to date. Although each species currently occupies large expanses of recently unglaciated lands (Pielou 1991), the degree of geographic variation in phenotypes, measured as the number of subspecies (AOU 1957), ranges from little (chipping sparrow) to extensive (song sparrow) (Table 1), suggesting that historical genetic patterns might exist. The song and fox sparrows are relatively closely related (Zink 1982), and have similar habitat requirements throughout large portions of their ranges, suggestive of a history of co-distribution. Both species exhibit extensive geographic variation in size and plumage coloration; notably, both species become darker in the Pacific Northwest.

The aspects noted above suggest why one might test for congruent phylogeographies among the five codistributed species. The first goal is therefore to test whether these species exhibit congruent mtDNA phylogeographic patterns. A second goal is to summarize less extensive mtDNA surveys of other codistributed birds to search for congruent patterns of phylogeography. The main purpose of the study is to ask whether common historical patterns are evident in currently [TABULAR DATA FOR TABLE 1 OMITTED] codistributed species, and if so, to discern relevant vicariant barriers. If mtDNA phylogeographies are incongruent, the goal is to consider what factors contribute to incongruence. Both goals address factors involved in the evolution of geographic variation itself.

MATERIALS AND METHODS

In each of the original studies (Table 1), samples were collected from breeding populations and surveyed using restriction endonuclease analysis of purified mtDNA (Lansman et al. 1981; Dowling et al. 1990). For most studies, the numbers of restriction endonucleases used were similar. Restriction site or fragment variation was analyzed, and for each species composite haplotypes were constructed. The mtDNA genetic distance (p, percent haplotype divergence) between composite haplotypes was computed following equations in Nei and Li (1979). Haplotypes were then clustered using a phenetic algorithm (UPGMA; Sneath and Sokal 1973) to estimate the depth of the haplotype trees and geographic patterns of mtDNA similarity. Phylogenetic relationships among haplotypes were also determined for each species using a maximum parsimony algorithm (consult original papers). Degree of geographic variation was considered in relation to an estimate of species' age. Assuming a monotonic relationship between mtDNA distance (p) and time since divergence from a common ancestor, distance to extant sister species can betaken as an estimate of relative age (caveats for this approach are discussed below). Dispersal distance was estimated by a computer program provided by J. E. Neigel, following the method presented in Neigel et al. (1991). The method of Neigel et al. (1991) was used specifically because it applies to nonequilibrium populations, which is likely true of most north temperate birds including those studied here (Neigel and Avise 1993); nonequilibrium means that computation of statistics such as Fst likely is inappropriate.

TABLE 2. Some factors that lead to geographically invariant species.

Ecological factors

Insufficient range size Range ecologically homogeneous Habitat generalist

Genetic factors

Insufficient genetic variation Bottlenecks Genetic constraints on phenotypic plasticity High dispersal (gene flow) Interspecific differences in stage of equilibrium

Historical factors

Species too "young" Species not historically widespread

RESULTS

MtDNA comparisons of the five bird species reveal two salient points. Despite the existence of morphologically based subspecies in all five codistributed species, only the fox sparrow and Canada goose exhibit structured phylogeographic patterns, which themselves differ (the phylogeographic split in Canada goose is north of the range of the fox sparrow). There is some tendency for red-winged blackbirds from the southwestern part of their range to exhibit similar haplotypes, but it is not a clear-cut division (Ball et al. 1988). Within the major mtDNA lineages of Canada goose and fox sparrow little mtDNA differentiation exists (Van Wagner and Baker 1990; Zink 1994). Secondly, the depths of the haplotype trees differ by a factor of four ([ILLUSTRATION FOR FIGURE 1 OMITTED], Table 1), with the Canada goose showing the deepest splits, and the chipping sparrow the shallowest. I assume roughly equal rates of mtDNA evolution as a working hypothesis.

DISCUSSION

Factors Affecting Phylogeographic Structures

The results presented in Figure 1 reveal no evidence of common phylogeographic histories among the five species, which leads to the question: why do codistributed species of birds have different patterns and degrees of mtDNA differentiation? Several ecological, genetic, and historical factors could be involved (Table 2).

Ecological Factors. - Different phylogeographic structures [ILLUSTRATION FOR FIGURE 1 OMITTED] could reflect differences in species' ecologies (Table 2). Each species occupies a broad geographic range, which was well sampled, arguing against insufficient range size, or accidents of sampling as reasons for different phylogeographic patterns. The species' ranges span several major environmental barriers. Because a wide continental area is occupied by each species, use of microhabitats might lead to differing degrees of genetic differentiation. The song sparrow occupies several microhabitats (Aldrich 1984), whereas the chipping sparrow and red-winged blackbird occur in the same basic habitat throughout their ranges (AOU 1983). However, these three species lack phylogeographic structure despite differential microhabitat use. The four groups of the fox sparrow each occupy a somewhat different habitat (Swarth 1920). Possibly, fox sparrows became adapted to these habitats during periods of isolation, preventing coalescence as habitats reconnected (the four groups of the fox sparrow are parapatric, and considered phylogenetic species by Zink 1994). However, there is little mtDNA differentiation within groups (Zink 1994), despite the existence of named subspecies and habitat variation. Differential use of habitats or existence in different ecoregions (Aldrich 1984) seem not to explain observed phylogeographic patterns, except perhaps in the fox sparrow.

Genetic Factors. - Phylogeographic structures might vary because of differences in levels of genetic variation or gene flow (Wenink et al. 1994). Each species has approximately equivalent amounts of genetic variation in its mtDNA genome (Table 1), but differences exist in the degree to which this variation is partitioned geographically. Bottlenecks could have culled genetic variation, and possibly truncated the depth of haplotype trees, but the similar average numbers of mtDNA haplotypes per individual (Table 1) argue against population constrictions.

The magnitude of gene flow could influence degree of mtDNA geographic differentiation. MTDNA data suggest little or no gene exchange between groups of the fox sparrow and Canada goose; the phylogeographic breaks appear sharply defined, without major clines on either side. Dispersal estimates (Table 1) are of similar magnitude for geographically homogeneous groups in the fox sparrow, and for the other three species (excluding Canada goose). Dispersal distances exceed those calculated for some other vertebrates (Neigel and Avise 1993), which supports the generalization that avian dispersal is high (Barrowclough 1980; Moore and Dolbeer 1989). Hence, gene flow probably inhibits geographic differentiation within groups of the fox sparrow, and in chipping sparrow, song sparrow and red-winged blackbird, even though these species currently span environmental barriers.

Another factor that might explain differences in degree of mtDNA differentiation is whether species differ in relative stages of equilibrium. For example, if two widespread species were fragmented by a vicariant event, one would eventually expect that haplotypes in each species would be monophyletic on each side of the isolating barrier. However, it takes up to 4N generations for monophyly of haplotypes to occur (Neigel and Avise 1986), and the rate of approach to monophyly might depend on mutation rate and long term effective population size (Slatkin and Maddison 1989). It is possible that the red-winged blackbird and song and chipping sparrows will eventually attain an mtDNA pattern like that observed in the fox sparrow. However, at this stage in their history, such is not the case. Furthermore, gene flow appears adequate to prevent differentiation.
TABLE 3. MTDNA distance (p) from nearest congener for several avian
taxa.


                                        MtDNA
                                      distance
Species                              to nearest
(number of subspecies)                congener          References


Geographic structure apparent


Sharp-tailed sparrow (5)                0.023               1, 2
Seaside sparrow (9)                     0.023               1, 3
Fox sparrow (18)                        0.060               4, 5
Canada goose (10)                       0.060               6
Savannah sparrow (21)                   0.059               1, 7
Black-capped chickadee (7)              0.037               8
Carolina chickadee (5)                  0.035               8
Boreal chickadee (4)                    0.036               8
Plain titmouse (10)                     0.038               9
Brant (4)                               0.078               6
LeConte's thrasher (3)                  0.077               5
Curve-billed thrasher (7)               0.082               5


                               Mean     0.050


Species without significant geographic structure


Red-winged blackbird (18)               0.030               10, 11
Chipping sparrow (7)                    0.036               12
Song sparrow (34)                       0.026               13, 5
Tufted titmouse (2)                     0.038               9
Black-crested titmouse (3)              0.050               9


                               Mean     0.036


References: I. Zink and Avise (1990), 2. Rising and Avise (1993),
3. Avise and Nelson (1989), 4. Zink (1994), 5. Zink (unpubl.),
6. Van Wagner and Baker (1990), 7. Zink et al. 1991b, 8. Gill et
al.
(1993), 9. Gill and Slikas (1992), 10. Ball et al. (1988),
11. Lanyon (pers. comm. 1994), 12. Zink and Dittmann (1993a),
13. Zink and Dittmann (1993b).


Historical Factors. - Degree of genetic differentiation, as measured by the number of phylogeographic subdivisions within species, is perhaps related to species' estimated age (Table 1). Geographic subdivision in mtDNA was found in the fox sparrow and Canada goose, species that are relatively distant from their nearest (extant) relatives. The red-winged blackbird stands in contrast. The prediction that number of subspecies or phylogeographic subdivisions is a function of distance to nearest congener is, of course, arguable. Intra-specific differentiation is probably related to how long a species has been widespread, which distance to nearest congener might not reflect. The red-winged blackbird might be "old" but only recently become widespread, with phenotypic differentiation proceeding more rapidly than mtDNA. Coalescence theory (e.g., Slatkin and Maddison 1989, Neigel and Avise 1986) shows that the time to common ancestry between two haplotypes can predate the speciation event. Hence, the mtDNA distance to nearest ancestor could be an overestimate of species "age," but Moore (1995) suggests that on average, it will be a relatively good indicator because coalescence times within avian species are much less than those between species. An expanded survey (Table 3) suggests a tendency for bird species relatively more distant from their extant sister species to exhibit geographic differentiation in mtDNA. One might expect this result because of the general accumulation of molecular divergence over time. Although the use of mtDNA distance data to measure species' age remains tentative, the species studied here without geographic variation in mtDNA appear to be relatively "young."

The depth of haplotype trees can vary considerably because of stochastic lineage sorting (Ball et al. 1990). That is, by chance alone one could expect haplotype trees of different depths. However, characteristics of trees that differ by chance lineage sorting do not include the differences between fox sparrow and Canada goose and the other species. In particular, one would expect older mtDNA haplotype lineages to be more geographically dispersed than younger ones (J. E. Neigel, pers. comm., 1993), but this is not the case.

Episodes of directional selection might obscure patterns of geographic variation. However, similar average numbers of haplotypes per individual indicate genetic variability, and suggest that any such episodes likely were not recent.

Comparative Phylogeography

The phylogeographic pattern in the fox sparrow provides a context for evaluating the other species. Each of the other four species currently has breeding populations in at least three of the four areas occupied by distinct mtDNA clades of fox sparrows without evidence of mtDNA differentiation. If one forced the data for each species onto the topology of the fox sparrow tree, each tree would be much less parsimonious. Thus, in five widespread and currently codistributed biological species of birds, the geography of mtDNA variation lacks common genetic (or phenotypic) patterns that could be attributed to a given set of vicariance events. The five species likely had different histories, which would not have been apparent until basic phylogeographic comparisons were made.

The origin of the four fox sparrow lineages (arrows in Fig. 1) and the two goose lineages predates the age of the oldest extant haplotypes in the other species. Thus it might not be surprising that different phylogeographic structures were observed. However, the other three species "existed" during the period when the fox sparrow and Canada goose ancestral lineages were subdivided. For example, the most divergent chipping sparrow haplotypes are 0.6%, whereas this species differs by 3.6% sequence divergence from its nearest extant relative. The origin of the four fox sparrow lineages occurred at approximately 1.2 to 1.9% sequence divergence; hence, chipping sparrows, or their immediate ancestors, existed during the time that differentiation occurred in fox sparrows (extinction of haplotypes explains why the tree appears pruned at greater levels of haplotype divergence). Events that led to the evolution of geographically structured groups of mtDNA haplotypes in the fox sparrow and Canada goose did not affect the other species; i.e., they were not general. Again, this conclusion assumes that rates of molecular evolution do not differ substantially.

These five species might have been historically codistributed and responded to events idiosyncratically (fox sparrow and Canada goose) or not at all (red-winged blackbird, chipping sparrow, song sparrow), or were simply not historically codistributed. Examination of differences in depth of haplotype trees offers a potential explanation. The three species without geographic variation in mtDNA have unstructured haplotype trees. Shallow unstructured trees are consistent with recent population expansion (Rogers and Harpending 1992), suggested also for red-winged blackbirds (Avise et al. 1988) and the song sparrow (Zink and Dittmann 1993b) from different analyses. I suggest that the fox sparrow and Canada goose were once more widely distributed than the other species, or at least occupied different historical refugia. The chipping sparrow, song sparrow, and red-winged blackbird likely expanded into their current range after the historical geological and environmental events that led to the origin of the fox sparrow and Canada goose lineages. Thus the three species without mtDNA phylogeographic structure were probably "not present" when and where historical events fragmented ancestral populations of the fox sparrow and Canada goose, and therefore were not part of the same historical avian community. Given the similarity in distribution, habitat and propensity for phenotypic differentiation in fox and song sparrows (Swarth 1920), lack of phylogeographic congruence was surprising (Zink 1991, 1994; Zink and Dittmann 1993b).

Comparative phylogeographic studies should determine if haplotype trees of codistributed species without geographic variation generally are shallower than those with geographic patterns (Rogers and Harpending 1992). For example, at least two species that did not fit the general pattern in the southeastern U.S., hardhead catfish (Arius felis) and American eel (Anguilla rostrata) exhibited relatively shallow haplotype trees (Avise 1992). This is evidence that lack of phylogeographic pattern results from lack of historical coassociation, rather than nonresponses to common historical events.

Lastly, the phylogeographic comparisons provide perspective on the evolution of phenotypic variation. In particular, one could ask why the five species have different numbers of subspecies over a similar area. The factors listed in Table 1 reveal no general explanations. For example, one might predict lower levels of dispersal for the song sparrow (34 subspecies) than the chipping sparrow (seven subspecies), but such was not the case. One might predict that the chipping sparrow was simply not old enough to have undergone "sub-speciation"; however, it is no less distant from its nearest extant congener than the song sparrow. A nonsignificant rank-order correlation coefficient (r = -0.18) was computed between number of subspecies and distance to nearest congener, which might imply a stochastic element to rate of phenotypic differentiation. The fact that subspecies boundaries are not congruent (Zink, unpubl. data) suggests that each species perceives environmental gradients differently. Overall, the data suggest that phenotypic and mtDNA evolution can be decoupled and proceed at different rates.

MTDNA Patterns in Other North American Birds

The lack of congruent historical patterns in the five species discussed above raises the question of generality. The mtDNA data suggest that the five codistributed species reached their current distributions at different times and possibly via different historical routes, and were subject to different historical events. If there were a strong historical component to phylogeographies of North American birds, one would have at least expected that the three sparrows compared above would exhibit evidence of it. Nonetheless, the sample of five species might be too small to detect common [TABULAR DATA FOR TABLE 4 OMITTED] patterns, and further studies are needed to determine if the North American avifauna consists of relatively small groups of species with common genetic patterns (such as, for example, those found in the fox sparrow and Canada goose), or mostly species without well structured patterns.

The species listed in Table 4 have been surveyed for geographic variation to varying extent (number of locales and individuals) and for various areas of North America. To assess whether phylogeographic patterns emerge, I considered species that are significantly codistributed in western North America, arid regions, eastern North America (including Newfoundland), northwestern North America and the taiga. Comparisons are made to the five species discussed above when appropriate. Some species in Table 4 are not discussed below because they are not codistributed with other surveyed species, but would be relevant to future comparisons.

Several species (other than those in Fig. 1) have been surveyed over part of their continental ranges, including the downy woodpecker, mallard, northern flicker, and yellow warbler. There is little evidence for mtDNA differentiation in the first two species, which is consistent with the lack of phylogeographic pattern in the chipping and song sparrows.

In the western United States, the common yellow throat and rufous-sided towhee show marked mtDNA differentiation between Washington and Minnesota, the exact location of the phylogeographic break being unclear (Ball and Avise 1992), and the yellow warbler shows an incomplete division (Klein and Brown 1994; their Fig. 3). The two subspecies groups of the plain titmouse, two samples of the mountain chickadee, brown-headed cowbird, and the megarhyncha and schistacea groups of the fox sparrow, exhibit extensive mtDNA differentiation between coastal and interior populations, whereas these east-west splits are not evident in the mourning dove, downy woodpecker, song sparrow, and chipping sparrow. Possibly, the minor southwestern differentiation in the red-winged blackbird and northern flicker is coincident with this general pattern. Thus, nearly 70% (9 of 13) of the taxa surveyed exhibit evidence of a phylogeographic break in western North America; this break also is apparent in phenotypic characteristics of many avian taxa (Johnson 1978).

Several aridlands species have been compared. Between Texas and southern California, mtDNA restriction site studies reveal no geographic differentiation in the verdin, black-tailed gnatcatcher, or cactus wren. However, between southern Texas and Arizona, both the curve-billed thrasher and canyon towhee exhibit mtDNA differentiation (Table 4).

Comparisons of several species reveal no mtDNA differentiation within and between the southeastern and midwestern United States (Table 4), suggesting this area has not been subjected to recent historical isolating events. However, Gill et al. (1993) report a significant phylogeographic break in the Carolina chickadee at the Tombigbee River/Mobile Bay. Also, Avise and Nelson (1989) noted a mtDNA break in the seaside sparrow consistent with differentiation in many other nonavian coastal species (Avise 1992). Zink et al. (1991 a) found no phylogeographic structure among the bronzed and purple forms (once considered separate species) of the common grackle. In addition, grackles from North Carolina and Louisiana showed no division such as that found in the Carolina chickadee and seaside sparrow, indicating that the effect Avise (1992) documented was perhaps limited to coastal species. Within the midwestern United States and north central Canada, no phylogeographic structure was found within or among three species of prairie grouse (Tympanuchus) (Ellsworth et al. 1994). Thus, there is little evidence for common mtDNA phylogeographic divisions east of the Rocky Mountains. Instead, idiosyncratic patterns are found in some species.

Across the continental taiga, fox sparrows show no mtDNA differentiation, whereas two distinct groups of the sharp-tailed sparrow exist (Rising and Avise 1993). Two species exhibit divergent mtDNA patterns in Newfoundland, the black-capped chickadee and boreal chickadee (Gill et al. 1993). Zink and Dittmann (1993b) suggested that Newfoundland was a probable Pleistocene refuge for the song sparrow, and Zink (1994) noted that fox sparrows from Newfoundland were possibly distinct. The role of Newfoundland in avian phylogeography deserves additional attention.

In the Pacific Northwest, several species exhibit morphological variation (Zink and Remsen 1986), but few have been examined for mtDNA variation. Within southeastern Alaska and British Columbia, the fox sparrow exhibits evidence of multiple mtDNA groups [ILLUSTRATION FOR FIGURE 1 OMITTED], whereas the song and chip-ping sparrows, and downy woodpeckers do not.

Comparison of several sets of codistributed bird species does not reveal extensive phylogeographic congruence. This initial study ([ILLUSTRATION FOR FIGURE 1 OMITTED], Table 4) suggests that the North American avifauna is composed of groups of species with idiosyncratic historical connections (Mayr 1946), although a broader data base is necessary. If this result is corroborated, it will indicate that one cannot assume that currently cod-istributed species have had a long history of coassociation.

CONCLUSIONS

A little explored aspect of phylogeography involves comparisons of species that are currently codistributed but which lack congruent patterns. An advantage of comparative phylogeography is that with data on levels of genetic variation and gene flow, population structure, and evolutionary distance from nearest ancestor, one can begin to sort out the reasons for incongruence. Such an understanding reveals the relative roles of different factors causing geographic variation. Furthermore, comparison of phylogeographies offers insight into the recent history of communities themselves. Thus, if community composition has not been stable enough to permit evolution of congruent phylogeographic patterns, perhaps it has not been stable enough to permit coevolution among currently sympatric species.

ACKNOWLEDGMENTS

I thank D. L. Dittmann for expertly gathering many of the data used in this analysis. The following persons provided important advice, assistance or comments on the manuscript: J. C. Avise, A. J. Baker, G. F. Barrowclough, J. M. Bates, E. C. Birney, J. Cracraft, S. Degnan, T Garland, D. A. Good, S. J. Hackett, J. T. Klicka, M. S. Hafner, K. P. Johnson, W. S. Moore, D. P. Pashley, J. V. Remsen, D. Schluter, J. Slowinski, G. Vermeij, and S. J. Weller. Participants in the LSU Molecular Evolution Seminar are gratefully acknowledged. I am grateful to J. E. Neigel for providing the program to estimate dispersal distances. The assistance of J. McIlhenny is gratefully acknowledged. Financial support was provided by NSF grant BSR-8906621 and Louisiana Board of Regents grant LEQSF #86-LBR-(048)-08.

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Author:Zink, Robert M.
Publication:Evolution
Date:Feb 1, 1996
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