Community-wide character displacement in the presence of clines: A test of Holarctic weasel guilds

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1 Journal of Animal Ecology 2011, 80, doi: /j x Community-wide character displacement in the presence of clines: A test of Holarctic weasel guilds Shai Meiri 1 *, Daniel Simberloff 2 and Tamar Dayan 1 1 Department of Zoology, Tel Aviv University, Tel Aviv 69978, Israel; and 2 Department of Ecology and Evolutionary Biology, University of Tennessee, Knoxville, TN 37996, USA Summary 1. Competition is thought to be a major influence on community assembly, ecology and evolution; presence of competitors may cause divergence in traits related to resource use (character displacement). 2. Such traits, however, often vary clinally, and this phenomenon may be independent of the presence or absence of competing species. 3. The presence of such clines can either obscure the effects of competition, or create an impression that competition is operating when, in fact, it is not. 4. We corrected for clinal variation while testing for character displacement in two well-studied weasel (Mustela) guilds, in the Nearctic and the west Palaearctic. 5. Without accounting for clines, our results agreed with previous studies suggesting character displacement in these guilds. 6. However, when we corrected for clines, predictions of competition theory were not met and often we obtained evidence for character convergence in sympatry. 7. This may suggest that the nature of the resource base may be more important than interspecific competition in shaping morphology and size in these carnivores. 8. Our results highlight the need to account for geographic variation when studying character displacement and cast some doubt on prevailing ideas regarding the effect of competition on morphological evolution. Key-words: canines, character convergence, character displacement, competition, geographic clines Introduction Competition is often treated as one of the main forces affecting animal behaviour and evolution, as well as the assembly of natural communities. Brown & Wilson (1956) hypothesized that competitors similar to one another in allopatry will diverge in sympatry by a process they termed character displacement. The reciprocal of character displacement, character release (Grant 1972), is defined as convergent evolution in allopatry of competitors that diverge in sympatry (reviewed by Dayan & Simberloff 2005). Brown & Wilson (1956) used two species of nuthatches (Sitta) to introduce character displacement: relative to regions of allopatry, in the zone of overlap the smaller species decreases in size, whereas the larger species increases. Brown and Wilson saw this divergence as reducing competition. Grant (1972, see also Grant 1975), however, showed that sizes of both species increase clinally from east to west. He calculated (without statistically comparing) very similar *Correspondence author. uncshai@post.tau.ac.il slopes and intercepts in zones of allopatry and sympatry for a size longitude relationship in one species and argued that both species show clines but no character displacement. Grant (1972, Figs 3 and 4) asserted that, in the presence of a geographic cline in the size of the focal trait, a change in intercept implies character displacement. While geographic size clines are common (Rosenzweig 1968; Ralls & Harvey 1985; Meiri & Dayan 2003; Meiri, Dayan & Simberloff 2005a; Meiri, Yom-Tov & Geffen 2007b; Haba et al. 2008; Gür 2010), few studies have tried to correct for their presence while studying character displacement. Dunham, Smith & Taylor (1979) examined character displacement in Catostomus fishes, controlling for geographic clines tracking several variables (e.g. latitude, elevation). They analysed allopatric and sympatric populations of each species separately and interpreted significant responses of morphology to the environmental variables in sympatry but not in allopatry as signals of character displacement (Dunham, Smith & Taylor 1979; p 886). Dayan et al. (1989a), studying clinal size variation in Palaearctic red foxes (Vulpes vulpes [L.]), concluded that this species decreases in Ó 2011 The Authors. Journal of Animal Ecology Ó 2011 British Ecological Society

2 Character displacement and clines 825 size from north to south in accordance with Bergmann s rule. In the southern part of its range, where V. vulpes is sympatric with the smaller Rueppell s sand fox (V. rueppellii, Schinz), Dayan et al. (1989a) found significantly shallower size-latitude clines than those for allopatric populations. They concluded that this difference in slopes is evidence that character displacement prevents the red fox from evolving to be smaller in the presence of a smaller competitor. Recently, Goldberg & Lande (2006), stressing the importance of accounting for clines while studying character displacement, identified just two studies that have done so (Grant 1975; Dayan et al. 1989a). Adams & Collyer (2007) then developed a test incorporating clines in character displacement studies. Their test randomizes residuals of a general linear model in which sizes of two competitors are compared in sympatry and allopatry, and environmental gradients can be used as covariates (and are assumed identical for both species). Randomization results are compared with the actual data (Adams & Collyer (2007). Several statistical tests (Poole & Rathcke 1979; Simberloff & Boecklen 1981; Marchinko, Nishizaki & Burns 2004; Montoya & Burns 2007) suggested that competition should even out size ratios between sympatric, adjacent size-ranked guild members (a phenomenon termed community-wide character displacement by Strong, Szyska & Simberloff 1979). Because these tests look only at guild members in an area of sympatry, a significant result, while implying that character displacement (or species sorting) is operating, does not explicitly address the geographic context of trait divergence in sympatry vs. allopatry. Nor do these tests account for the presence of clines. Here, we used a different multiple regression approach from that of Dunham, Smith & Taylor (1979) to test for community-wide character displacement in the presence of clines. We examined each guild member in turn and tested for differences in size in response to differences in community composition, while controlling for a cline (here a latitudinal cline) and examining the interaction of community composition and the geographic gradient. Non-latitudinal variation may often be present and, indeed, dominant. For instance, size can change longitudinally or with distance to range core. The method we used to correct for a cline may be used for any hypothesis regarding clinal spatial structure, and several clines may be corrected for simultaneously if there are enough data. We focused here on a latitudinal cline (Mayr 1956; Meiri 2011), because it has often been featured (but never explicitly tested) in discussion of size clines in weasels (McNab 1971; Ralls & Harvey 1985; Dayan & Tchernov 1988; Dayan et al. 1989b). THE STUDY SPECIES We tested for character displacement in three-species guilds of New World and western Palaearctic weasels of the genus Mustela. In both regions, the smallest guild member is the least weasel, Mustela nivalis L., followed by the stoat, M. erminea L. The largest guild members are the polecat, M. putorius L., in the Palaearctic and the long-tailed weasel, M. frenata Lichtenstein, in the New World. All are small, long-bodied, short-legged carnivores that prey mostly on vertebrates, often taking prey larger than themselves (King 1983; Sheffield & King 1994; Sheffield & Thomas 1997; Nowak 1999; Lode 2003). They kill prey by biting the occipital region, crushing the base of the skull or severing the spinal cord using the upper canines, making canine size a good indicator for the size of the prey, and hence for the study of character displacement (Dayan et al. 1989b). Competition between sympatric members of these species has been intensively studied (e.g., King & Moors 1979; Simms 1979; Dayan et al. 1989b; McDonald 2002; Aunapuu & Oksanen 2003; St-Pierre, Ouellet & Crete 2006). McNab (1971) interpreted geographic clines as evidence for character displacement and release in weasels, claiming that M. erminea increases in size with increasing latitude only in the northern parts of its Nearctic range where M. frenata is absent. He likewise suggested that M. nivalis is largest in the absence of erminea, and the latter is smallest where nivalis is absent. Ralls & Harvey (1985), however, showed that erminea increases in size with increasing latitude even when sympatric with frenata. Thus, they viewed the fact that erminea is larger where the larger competitor is absent simply as a manifestation of Bergmann s rule and not as evidence of character release. They argued that there is no evidence for character displacement in North America or for character release in Ireland (see also McDonald 2002; Meiri, Dayan & Simberloff 2007a; cf. Dayan & Simberloff 1994). Palaearctic M. nivalis decreases markedly in size with increasing latitude (Sheffield & King 1994; Meiri, Dayan & Simberloff 2004), opposite to the expectations of Bergmann s rule. Because nivalis ranges furthest south and is the smallest member of its guild, this cline may imply character release in the south (Dayan & Tchernov 1988). Here, we tested for community-wide character displacement by examining canine diameter in each species in relation to guild composition and a geographic cline. We made the following predictions about how competition will affect maximum canine diameters: 1. Mustela nivalis canines will be largest in allopatry. We predict that such character release will be more evident in males (females are smaller than males in all these species), because they more closely resemble the larger species in size and therefore are under greater selection pressure to reduce size (although sizes of the two sexes are probably correlated to some extent, Lande 1980). Mustela nivalis will be smallest when sympatric with erminea, especially if the latter already is small in the presence of a larger species. 2. Mustela frenata will be smallest in the southern parts of its range, where it is allopatric (M. putorius always overlaps with either nivalis or both nivalis and erminea. Similarly nivalis is never allopatric in America). Both frenata and putorius will be larger when nivalis is present and larger still when erminea is present.

3 826 S. Meiri, D. Simberloff & T. Dayan 3. Mustela erminea will be larger in the presence of nivalis and smaller in the presence of frenata or putorius than in allopatry. We predicted either no size differences between allopatric erminea and erminea in the full three-species guild or that in allopatry, males will be larger and females smaller relative to erminea in the full guild. Materials and methods GUILD COMPOSITION We examined the three smallest Mustela species in both the New World (nivalis, erminea and frenata) and the western Palaearctic (nivalis, erminea and putorius). These guilds may include a few larger species. Mink (M. lutreola L. in Europe and M. vison Schreber in North America) overlap geographically with the species we study. However, mink depend much more on aquatic habitats (Youngman 1990; Larivie` re 1999) and were therefore omitted from most previous work on character displacement in the small Mustela. Other short-legged, long-bodied, vertebrate-eating species that may be members of the small mustelid guild are spotted skunks (Spilogale spp.), steppe and marbled polecats (Mustela eversmannii Lesson and Vormela peregusna Güldenstädt, respectively), and the black-footed ferret, Mustela nigripes Audubon and Bachman (Verts, Fig. 2. Ranges of the Western Palaearctic species. Dark grey: Mustela nivalis alone; diagonal lines: putorius and nivalis; black: all three species, crosshatch: erminea and nivalis; light grey: erminea and putorius;dots:erminea alone. Fig. 1. Ranges of the North American species. Light grey: Mustela frenata alone; diagonal lines: frenata and nivalis; dark grey: frenata and erminea; black: all three species, crosshatch: erminea and nivalis; dots: erminea alone. Fig. 3. Re-scaling latitude. a hypothetical example of a species following Bergmann s rule in allopatry (solid line), but not in sympatry (dashed line). Even though at similar latitudes (within the circle) the sympatric populations have smaller canines, their intercept will be higher than for the allopatric populations, and we will therefore wrongly infer that competition causes the species to become large. rescaling latitude: a species can be part of up to four communities: in allopatry, sympatric with any one species, or sympatric with both (arbitrarily, all are portrayed with a slope of 0). Here, we rescale latitudes by finding the latitudes over which the largest number of such combinations overlap (here between latitudes 1 and 2). We subtract from each actual latitude the midpoint of this range ([Lat 1 + Lat 2] Lat 2).

4 Character displacement and clines 827 Carraway & Kinlaw 2001; Gorsuch & Larivière 2005; Lanszki & Heltai 2007). We have previously found evidence for character displacement in less tightly defined guilds that included American mink (Dayan & Simberloff 1994), marbled polecats (Dayan et al. 1989b) and western spotted skunks (S. gracilis; Meiri, Dayan & Simberloff 2007a). Nonetheless, it is the three small weasel species on both continents that have received the most attention, overlap the most geographically and, except for M. putorius vs. M. eversmannii, are also the most morphologically, phylogenetically and ecologically similar. European mink and black-footed ferrets are rare and have restricted ranges, American mink are much more aquatic, M. eversmannii occurs only at the eastern-most parts of the range we examine, and Vormela and skunks are larger and phylogenetically quite distant. While we view it as likely that mink competes with M. frenata (S. Meiri, unpublished data) and M. putorius (Dayan & Simberloff 1994), we chose to focus here on the part of the guild that has received the vast majority of research effort. DATA We measured the maximum anterior posterior diameter of the upper canines of Mustela specimens in natural history museums (Appendix S1), using only wild-caught, sexed specimens with fully erupt permanent canines. Studies of morphological character displacement in mammals often use skull length, a common index of body size. Davies et al. (2007) recently used upper carnassial lengths to study morphological divergence. Our preliminary results (not shown) suggested that different indices (skull length, carnassial length and canine diameter) show very similar patterns, and we therefore used canine diameters alone here. We obtained sympatry data by overlaying Geographic information system (GIS) distribution maps of all species (from Meiri et al. 2009) and examining which species overlap in the geographic location of each specimen. ANALYSIS Treating sexes as distinct morphospecies, we used ancova to examine the effects of geography and community composition on each morphospecies. Latitude was the clinal covariate, and community composition (which of the three species are found in each locality) was the main effect. We interpreted significant differences in modified intercepts between composition levels as evidence for character displacement or release. Finally, we included an interaction term between community composition and latitude. Here too, significant differences in slopes of size vs. latitude for different community compositions were taken as evidence for character displacement (Dayan et al. 1989a; Goldberg & Lande 2006; Adams & Collyer 2007). Although longitudinal size clines are sometimes reported (e.g., Grant 1972; Motokawa 2003; Meiri, Dayan & Simberloff 2005a), we refrained from using longitude, because even at the same latitude and community composition populations can be highly disjunct (e.g., communities of M. putorius in the presence of nivalis but not erminea inhabit southern Iberia, Italy and the Balkans, and M. erminea occurs in the presence of frenata but not nivalis in New England and northwestern USA, but not in between; Figs 1 and 2). We restricted our sampling in the Palaearctic to longitudes west of 44 east, because our sampling intensity declined rapidly further east. ancova compares main effects as intercepts, i.e. when the continuous predictor is zero. With canine diameters and latitudes, this means that we compared the expected sizes predicted by the latitudinal clines to occur at the equator (latitude zero). In the guilds we studied, however, only Mustela frenata reaches this far south, and obviously, no species overlap at the equator. Because we viewed changes in the size latitude slope (=interactions) as possible evidence for competition, such a comparison of intercepts would be potentially misleading. This is because if slopes differ between community composition categories, then a shallow slope would likely result in a high value at Table 1. Responses to community composition, size clines and their interaction for all morphospecies Species Sex Response to community composition Response to latitude Composition latitude interaction New World nivalis Female No effect No effect No effect nivalis Male en > efn = fn No effect No effect erminea Female efn > allopatric Bergmann s rule No effect erminea Male Allopatric = efn > en, ef Bergmann s rule Slope shallower in allopatry than in sympatry frenata Female Allopatric > ef, efn Bergmann s rule or no effect Bergmann s rule in sympatry, no cline in allopatry frenata Male Allopatric > ef, efn All possibilities Opposite to Bergmann s rule in allopatry, no cline (fn guild), Bergmann s rule (ef, efn guilds) Old World nivalis Female epn > allopatric Opposite to Bergmann s rule or no effect nivalis Male Allopatric < sympatric Opposite to Bergmann s rule or Bergmann s rule erminea Female enp > allopatric > en Bergmann s rule No effect erminea Male Allopatric > en, enp No effect No effect putorius Female No effect No effect No effect putorius Male np > enp Bergmann s rule No effect Steepest slope in allopatry, shallower in en, enp guilds, no cline (np guild) Bergmann s rule (np guild) or opposite (elsewhere) The results are a qualitative representation of data presented in the text. Community composition codes: e = Mustela erminea; f = M. frenata; n = M. nivalis; p = M. putorius. Thus, e.g. efn is a guild containing erminea, frenata and nivalis; the np guild contains nivalis and putorius, etc.

5 828 S. Meiri, D. Simberloff & T. Dayan the equator (=higher intercept) if size increased with latitude, whereas a steep slope would result in a low, potentially even a negative, intercept (Fig. 3a). To overcome this problem, we first noted that a species can be part of up to four communities: it can be allopatric, sympatric with any one species or sympatric with both. We therefore found the latitudes over which the largest number of these community composition combinations overlap (Fig. 3b). We then subtracted from each actual latitude the midpoint of this range (e.g. if this occurs between latitudes 36 and 44, we subtracted 40 from the actual latitude value of each specimen), thus setting zero latitude as the midpoint of the latitudes where most combinations overlap, and then ran the ancova normally. The intercepts thus pointed to latitudes where multiple community combinations occur, and necessarily to realistic values for canine diameters. We used specimens latitudes to derive the rescaling latitudes. The resulting rescaling coefficients were 44, 49Æ5 and 53Æ5 for Nearctic frenata, erminea and nivalis, respectively, and 43, 55Æ5 and 43Æ5 for Palaearctic putorius, erminea and nivalis, respectively. All analyses were conducted in R (R Development Core Team, 2009) with both untransformed and log-transformed canine diameters. These gave qualitatively similar results, and we thus report only the former, except as indicated below for male New World M. erminea. We used a backwards elimination procedure to arrive at minimum adequate models for each morphospecies continent combination. Results Our sample sizes for the Palaearctic were 522 putorius, 751 erminea and 1168 nivalis specimens. In the New World, the analogous numbers were 198 nivalis, 866 frenata and 1741 erminea specimens. Qualitative results of all models are shown in Table 1. NEW WORLD Mustela nivalis Nearctic nivalis do not occur allopatrically. Female canines (n = 82) showed no response to either community composition (F =1Æ48, P =0Æ23) or latitude (F =0Æ10, P =0Æ75) and no latitude combination interaction (F = 1Æ75, P =0Æ18, Fig. 4a). Male canines (n = 116, Fig. 4b), on the other hand, were larger in the guild containing erminea than in the full guild (by 0Æ14 ± 0Æ03 mm, t =5Æ31, P <0Æ0001). Canine size of male nivalis in the latter guild did not differ from that in a guild containing nivalis and frenata (t =0Æ98, P = 0Æ33). Latitude did not affect male canine diameters. Thus, New World least weasels did not follow the predictions of character displacement. Fig. 4. Canine diameters of a. female and b. male New World Mustela nivalis as a function of latitude and community composition. Fig. 5. Canine diameters of a. female and b. male New World Mustela erminea as a function of latitude and community composition.

6 Character displacement and clines 829 Mustela erminea Female canine diameter increased with latitude (slope = 0Æ015 ± 0Æ001, t =10Æ82, P <0Æ0001, n = 527, Fig. 5a), with no interaction with community composition (F = 1Æ10, P =0Æ35). Female canines were larger in the full guild than in allopatry (by 0Æ06 ± 0Æ03 mm, t = 2Æ08, P = 0Æ038). Male canines (n = 1214, Fig. 5b) increased less with latitude (slope = 0Æ011 ± 0Æ002, t =6Æ76 P <0Æ0001) in allopatry than in all sympatry categories (respective slopes for ermineafrenata, the full guild and erminea-nivalis: 0Æ026, 0Æ023 and 0Æ024, t =3Æ46, 2Æ55 and 5Æ82, P <0Æ001, 0Æ01 and <0Æ001). Male canines were larger in allopatry than in sympatry with either frenata (by 0Æ07±0Æ02 mm, t =3Æ09, P =0Æ02) or nivalis (by 0Æ04±0Æ02 mm, t =2Æ10, P =0Æ04) alone, but not than male canines in the full guild (difference: 0Æ001 ± 0Æ02 mm, t =0Æ07, P =0Æ94). With log-transformed canine diameters, however, they were larger in allopatry than in the full guild (difference: 0Æ003 ± 0Æ001, t =2Æ53, P =0Æ01). Thus, Nearctic erminea responded to competitors in a way that is difficult to interpret in the context of character displacement: responding to frenata as expected, but responding to nivalis opposite to expected. Mustela frenata Female canines (n = 283, Fig. 6a) were larger in allopatry than in guilds containing erminea, either alone or as part of the three-species guild (both by 0Æ14 mm; respectively, t =3Æ79 and 3Æ01, P =0Æ0002 and 0Æ003). Size in the guild containing only nivalis did not differ significantly from that in allopatry (difference: 0Æ11 ± 0Æ08 mm, t = 1Æ39, P = 0Æ17). There was no latitudinal cline in allopatry (slope = )0Æ02±0Æ02, t =0Æ86, P =0Æ39), but canine diameter increased with latitude in all three sympatric guilds (slopes of 0Æ01 to 0Æ06, all significant). Results were similar for male canines (n = 583, Fig. 6b). Canines were larger in allopatry than in guilds containing erminea, either alone (by 0Æ08 ± 0Æ03 mm, t =2Æ93, P =0Æ035) or as part of the three-species guild (by 0Æ09 ± 0Æ03 mm, t =2Æ93, P =0Æ035), but no larger than in guilds containing only nivalis (difference: )0Æ001 ± 0Æ1 mm,t =2Æ93, P =0Æ035). There was a significant, negative, latitudinal cline in allopatry (slope = )0Æ005 ± 0Æ001, t =3Æ95, P <0Æ0001), with no cline in the guild containing both frenata and nivalis (slope = 0Æ039 ± 0Æ034, t =1Æ14, P =0Æ26) and positive clines in both guilds that contained erminea (slopes 0Æ008 ± 0Æ003 Females Females Males Males Fig. 6. Canine diameters of a. female and b. male New World Mustela frenata as a function of latitude and community composition. Fig. 7. Canine diameters of a. female and b. male Old World Mustela nivalis as a function of latitude and community composition.

7 830 S. Meiri, D. Simberloff & T. Dayan and 0Æ032 ± 0Æ003, t = 2Æ25 and 5Æ26, P = 0Æ025 and <0Æ0001, for a guild of frenata and erminea, and the threespecies guild, respectively). The results for the frenata nivalis guild should be treated with caution, however, as they rest on only eight female and 17 male specimens. In sum, frenata became smaller in the presence of the smaller erminea opposite to the predictions of character displacement. WEST PALAEARCTIC Mustela nivalis When we corrected for the geographic cline, female canines (n = 323, Fig. 7a) increased significantly in diameter in the full guild relative to allopatry (by 0Æ19±0Æ06 mm, t =2Æ93, P =0Æ004), but non-significantly in two-species guilds (0Æ18±0Æ25 and 0Æ12±0Æ07, t =0Æ74 and 1Æ62, P =0Æ46 and 0Æ11 in guilds with erminea and putorius, respectively). Female canines decreased rapidly in size with increasing latitude in allopatry (slope = )0Æ06 ± 0Æ01, t = 9Æ22, P < 0Æ0001), less so in the full guild (slope = )0Æ02 ± 0Æ003, t = 8Æ02, P < 0Æ0001), marginally in sympatry with erminea only (slope = )0Æ02 ± 0Æ01, t =1Æ70, P =0Æ09) and not at all in the presence of putorius alone (slope = )0Æ01 ± 0Æ02, t = 0Æ64, P =0Æ52). Male canine diameters showed similar patterns but were always larger in allopatry (for the full guild and in the presence of erminea and putorius, respectively, by 0Æ12 ± 0Æ04, 0Æ36 ± 0Æ16 and 0Æ31±0Æ05 mm; t =2Æ91, 2Æ25 and 6Æ86; P =0Æ004, 0Æ025 and <0Æ0001, Fig. 7b). Male canine diameters decreased with increasing latitude in allopatry, in the presence of erminea, and in the full guild (respective slope = )0Æ05 ± 0Æ005, )0Æ04 ± 0Æ008 and )0Æ02 ± 0Æ002, t =10Æ32, 5Æ53 and 11Æ53, P <0Æ0001 in all cases) but increased with increasing latitude (slope 0Æ02 ± 0Æ009) in the nivalis-putorius guild (t = 2Æ39, P = 0Æ017). Palaearctic nivalis was thus larger than expected in the presence of larger competitors contrary to the predictions of competitive character displacement. Mustela erminea Correcting for a marginally positive latitudinal cline (slope 0Æ007 ± 0Æ004, t = 1Æ94, P = 0Æ054, Fig. 8a), we found female canines (n = 276) were smaller in the presence of nivalis (by 0Æ15±0Æ06 mm, t =2Æ55, P =0Æ01) but larger Females Females Males Males Fig. 8. Canine diameters of a. female and b. male Old World Mustela erminea as a function of latitude and community composition. Fig. 9. Canine diameters of a. female and b. male Old World Mustela putorius as a function of latitude and community composition.

8 Character displacement and clines 831 in the full guild than in allopatry (by 0Æ14 ± 0Æ03 mm, t = 4Æ11, P < 0Æ0001). Male canines (n = 475, Fig. 8b), however, were smaller in the presence of nivalis alone (by 0Æ30 ± 0Æ004 mm, t = 7Æ00, P < 0Æ0001) and in the full guild (by 0Æ05 ± 0Æ02 mm, t =2Æ25, P =0Æ025), relative to allopatry. There was no latitudinal cline (slope 0Æ005 ± 0Æ003, t = 1Æ54, P = 0Æ13). Here too, we found sizes that were more similar to those of the competitor (nivalis) in sympatry than in allopatry contrary to the predictions of competitive character displacement. Mustela putorius In none of the models were latitude, community composition or their interaction significant predictors of canine diameter in female (n = 198, Fig. 9a) polecats. Males (n = 324, Fig. 9b), however, had larger canines (by 0Æ31 ± 0Æ09 mm, t = 3Æ34, P = 0Æ0009) where present with nivalis alone than where all three species were present. A positive latitudinal size cline was apparent for males in both guilds, but it was marginally (t =1Æ71, P =0Æ088) stronger (slope 0Æ071 ± 0Æ031 vs. 0Æ016 ± 0Æ006) in the nivalis putorius guild than in the full guild. Polecats thus had larger canines when their nearestsized smaller competitor (erminea) was absent than they were when it was present opposite to what would be expected under character displacement. Discussion Our results strikingly departed from the predictions of character displacement in a guild in which competition has been perceived previously as a strong structuring force, leading to morphological co-evolution. Competition in the small Mustela guilds we studied has been extensively studied since the seminal work of Hutchinson (1959). Rosenzweig (1966) and Simms (1979) believed that frenata is a poor competitor for food but can exclude smaller weasels through interference (see also St-Pierre, Ouellet & Crête 2006). Simms (1979) and King & Moors (1979) thought the small diameter of rodent tunnels enables the small species to obtain prey unavailable to larger ones. Aunapuu & Oksanen (2003) similarly believed that nivalis is a more efficient rodent hunter and that stoats can coexist with it because they also take other prey. Many size patterns in these species have been ascribed to competition. Dayan et al. (1989b) and Dayan & Simberloff (1994) found equal size ratios in American and British guilds consisting of the focal Mustela species for both canine diameters and skull length. Meiri, Dayan & Simberloff (2007a) obtained similar results for skull lengths, but not for canines, in mainland guilds, although ratios were usually unequal in island guilds. McDonald (2002) argued that British and Irish mustelids do not partition prey along a size axis, and hence, equal size ratios likely result from interspecific aggression. In the context of geographic clines, McNab (1971) claimed that Bergmann s rule in North American M. erminea and M. nivalis is an artefact of release from competition with frenata. Dayan & Tchernov (1988) invoked character release to explain the reverse of Bergmann s rule: the large size of M. nivalis in southern Europe and North Africa. The notion that size clines and competition interact is thus widely held for weasels. Our findings, however, offer a different interpretation. In the west Palaearctic, Mustela nivalis is allopatric in the south and decreases sharply in size northwards. However, this decrease slows, and size actually increases in southern Europe with the addition of putorius. Still further north, where the third species, M. erminea enters the guild, nivalis is larger rather than smaller. While female erminea canines are indeed relatively large in the three-species European guild, male canines are small. This is not the result of competition with polecats, as male erminea canines are also small further north in the presence of nivalis alone. In this northern assemblage, male nivalis have large canines, and female erminea have small ones. Mustela erminea are smaller in the presence of nivalis than in allopatry. Most of these patterns are exactly opposite to those predicted by competitive character displacement. In America, it is the largest species, M. frenata, that ranges furthest south. This species is smaller when sympatric with its two smaller congeners. While canines of the medium-sized erminea are indeed smaller in the presence of frenata, they were also smaller in the presence of nivalis only than in allopatry. Mustela nivalis itself is small in the presence of frenata but large in the presence of erminea only. Thus, several patterns in canine diameters of American weasels are opposite to what competitive character displacement would predict. As all weasels eat mostly rodents and lagomorphs and have greatly overlapping diets (Rosenzweig 1966; Simms 1979; McDonald 2002), it is perhaps unsurprising that their sizes tend to converge rather than diverge in sympatry. Character convergence because of shared ecological selection in sympatry may be common (e.g. Grant 1972; Abrams 1996; Rosenblum 2006) and reflect similar responses to the same selection pressures. In the context of canine diameters, convergence is possibly a response to the use of similar resource bases. Our previous finding that carnivore intra-population variability and size dimorphism are usually lower where the resource base is narrower (e.g. on islands, Meiri, Dayan & Simberloff 2005b) is in line with this interpretation. Detailed studies of the prey spectra of different species in the same community vs. prey spectra in allopatry, however, will be needed to address this issue fully. It may also be possible that sympatric weasels segregate into different microhabitats, i.e. show microallopatry of the sort that our methods would not detect, or that they are influenced by the presence of larger guild members which we excluded from our models. Moors (1980) has suggested that sexual dimorphism in mustelids is driven by the degree of polygamy, with more polygamous species being more dimorphic. He ascribed less importance to resource segregation, a conclusion also embraced by Gittleman & Van Valkenburgh (1997). This reasoning has often led to an a priori rejection of ecological character displacement as a mechanism affecting the evolution of size and size dimorphism in carnivores, but we argue that the two phenomena are not mutually exclusive. While the polyg-

9 832 S. Meiri, D. Simberloff & T. Dayan amous mating system of weasels predisposes all species to strong male-biased sexual dimorphism (Moors 1980; Gittleman & Van Valkenburgh 1997), no studies, to our knowledge, demonstrate clines in intraspecific geographic variation in the degree of polygamy of any species. Nor do we envision a mechanism whereby the presence or absence of congenerics will influence the mating system of a population of another species. Because all four species we study share a similar polygamous reproductive strategy, it is likely that this leads to their all being highly dimorphic, with males the larger sex. The geographic variation in size and size dimorphism within species, however, likely reflects geographic variation in ecology against a background of common reproductive strategy. Our results amply demonstrate the need to correct for size clines when comparing sizes of allopatric and sympatric populations in seeking evidence for competition. Results for four of the 12 focal morphospecies (3 species*2 sexes*old and New World) change dramatically when such clines are not corrected for. Predictably, it is the species showing strong size clines that are affected most: Nearctic erminea are largest when sympatric with nivalis alone (compared to allopatry, by 0Æ06 ± 0Æ02 and 0Æ13 ± 0Æ02 mm in females and males, respectively, P <0Æ01), but correcting for the strong tendency of erminea to follow size clines within all community types shows that at similar latitudes this community composition category contains relatively small ermines. Overall, Palaearctic M. nivalis are largest in allopatry (e.g. larger by 0Æ45±0Æ04 and 0Æ38 ± 0Æ02 mm in females and males, respectively, than in the full guild, P < 0Æ001), but taking size clines into account we show that in fact, when communities are compared at similar latitudes, the species is actually larger in the presence of larger congeners. Our results appear to counter those of many previous studies, in which various authors, ourselves included, found strong evidence for community-wide character displacement: non-random size ratios between canine diameters of the morphospecies studied here (Dayan et al. 1989b; Dayan & Simberloff 1994; Meiri, Dayan & Simberloff 2007a). Thus, the lack of evidence for character displacement (sensu Brown & Wilson 1956 and Grant 1972) comes as a surprise. How can we understand this discrepancy? One possibility is that species sorting rather than morphological displacement has occurred; only species that exhibited some minimal size difference from the others could enter the community (although we note that these differences may well be very small, Meiri, Dayan & Simberloff 2007a). Alternatively, it could be argued that the size clines we correct for are compromises between different selective forces, mainly competition and whatever environmental factors select for Bergmann s rule, so that for example M. nivalis in the western Palearctic is large in the south in absence of larger congeners but this trend disappears in the extreme north (Fig. 7) in response to cold climate. It could also be argued that if these size clines were primarily driven by competition, as previously suggested (McNab 1971), then correcting for clines removes the signal of competition, and this is why we find no evidence for character displacement. The role of competition in generating clines is, however, not readily testable. We note further that the clines shown are not always in the direction predicted by competitive character displacement (e.g. those for Mustela putorius males) and that size clines also occur within community composition categories. Our method has some disadvantages. Specimens in some overlap categories (e.g. from areas where frenata and nivalis but not erminea overlap) are rare in museum collections, resulting in wide confidence intervals for parameter estimates. Adding additional covariates (as in Dunham, Smith & Taylor 1979) greatly exacerbates this problem. When community composition and latitude are highly co-linear, it is also difficult to establish whether a cline is independent of community composition, as we assume here. Estimating clines for each community independently, as we do, overcomes this problem. The method we use thus provides a simple way to detect (or refute) morphological responses to differences in community composition. Our method allows for testing the effects of multiple potential covariates (provided sample sizes are large enough). Further, we are not forced to assume that all species vary clinally in the same way (cf. Adams & Collyer 2007) or even that within the same species clines are stationary across the geographic domain. In fact, we explicitly test and refute both the assumption of similarity between species and that of stationary geographic clines. Another advantage relates to the fact that many existing tests of character displacement (Poole & Rathcke 1979; Simberloff & Boecklen 1981; Marchinko, Nishizaki & Burns 2004; Montoya & Burns 2007) cannot distinguish between symmetric character displacement, in which all species evolve in response to the presence of competitors, and asymmetric character displacement, in which some species respond to the presence of competitors and others do not. Our method does not assume that responses of all community members to the presence or absence of competitors are symmetric or that the degree of sexual dimorphism is uniform. Character displacement requires that species be morphologically more similar in allopatry than in sympatry (Brown & Wilson 1956) and thus must be sought while taking into account geographic size variation that is unrelated to competition (Grant 1972). Tests of this theory that do not account for such variation are likely to provide misleading answers if geographic variation is strong (Goldberg & Lande 2006; Adams & Collyer 2007). In weasels, some of which show strong clinal variation, we find that there is no evidence for character displacement when latitudinal clines are accounted for. In fact, these carnivores show some evidence for morphological convergence in canine diameters, suggesting that all species adapt locally to similar prey species. Competition may still be a strong force affecting the microhabitat preferences, activity times and demography of weasels in the guilds we study although we have no data to suggest this is happening. Interference competition may likewise allow the larger species to coexist with the smaller ones even if they are inferior hunters (assuming prey are a limiting factor, which is uncertain). Our results

10 Character displacement and clines 833 show, however, that sympatric weasels are often morphologically more similar than allopatric populations of the same species. We suspect that the force driving canine size evolution may be local adaptation for hunting similar resources. Acknowledgements We thank Emma Goldberg, Jonathan Davies, Russ Lande and Ally Bede Phillimore for valuable discussion. We thank David Orme for help with R code and Rich Grenyer for help with mapping ranges and identifying areas of overlap. Shay Barkan kindly helped us with graphic issues. 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11 834 S. Meiri, D. Simberloff & T. Dayan Verts, B.J., Carraway, L.N. & Kinlaw, A. (2001) Spilogale gracilis. Mammalian Species, 674, Youngman, P.M. (1990) Mustela lutreola. Mammalian Species, 362, 1 3. Received 15 November 2010; accepted 7 February 2011 Handling Editor: Stan Boutin Supporting Information Additional Supporting Information may be found in the online version of this article. Appendix S1. Museums and specimens. As a service to our authors and readers, this journal provides supporting information supplied by the authors. Such materials may be re-organized for online delivery, but are not copy-edited or typeset. Technical support issues arising from Supporting Information (other than missing files) should be addressed to the authors.