Localized versus generalist phenotypes in a broadly distributed tropical mammal: how is intraspecific variation distributed across disparate environments?
© Alvarado-Serrano et al.; licensee BioMed Central Ltd. 2013
Received: 11 December 2012
Accepted: 10 July 2013
Published: 31 July 2013
The extent of phenotypic differentiation in response to local environmental conditions is a key component of species adaptation and persistence. Understanding the structuring of phenotypic diversity in response to local environmental pressures can provide important insights into species evolutionary dynamics and responses to environmental change. This work examines the influence of steep environmental gradients on intraspecific phenotypic variation and tests two hypotheses about how the tropical soft grass mouse, Akodon mollis (Cricetidae, Rodentia), contends with the disparate environmental conditions encompassed by its broad distribution. Specifically, we test if the species expresses a geographically unstructured, or generalist, phenotype throughout its range or if it shows geographically localized morphological differentiation across disparate environments.
Using geometric morphometric and ecomorphological analyses of skull shape variation we found that despite distinct environmental conditions, geographically structured morphological variation is limited, with the notable exception of a distinct morphological disjunction at the high-elevation forest-grassland transition in the southern portion of A. mollis distribution. Based on genetic analyses, geographic isolation alone does not explain this localized phenotype, given that similar levels of genetic differentiation were also observed among individuals inhabiting other ecosystems that are nonetheless not distinct morphologically.
Instead of phenotypic specialization across environments in these tropical mountains, there was limited differentiation of skull shape and size across the broad range of A. mollis, with the exception of individuals from the puna, the highest-elevation ecosystem. The high morphological variance among individuals, together with a weak association with local environmental conditions, not only highlights the flexibility of A. mollis’ skull, but also highlights the need for further study to understand what maintains the observed morphological patterns. The work also indicates that mechanisms other than processes linked to local ecological specialization as a driver of diversification may contribute to the high diversity of this tropical region.
Phenotypic differentiation among closely related taxa along environmental gradients is well documented (e.g., [1–3]). For example, across species there is a negative correlation between body size and environmental temperature (Bergmann’s rule ) and an association in mammals between precipitation and high degree of hypsodonty in species inhabiting arid and grassy regions [5, 6]. However, localized phenotypes may not necessarily be observed within a species, even if populations occur across steep environmental gradients and disparate ecosystems. Depending on the relative fitness trade-offs between alternative phenotypes, degree of population isolation, and the constancy and/or spatial heterogeneity of the environment [7–9], a geographically unstructured, generalist phenotype may be expressed throughout the species’ range that is capable of thriving in a wide variety of conditions.
Tropical montane ecosystems represent an ideal system to uncover the role of the environment in shaping intraspecific phenotypic variation as species experience substantial and often drastic different environmental conditions across montane ecosystems [10, 11]. Temperature, air pressure, solar radiation, precipitation, area, cloud cover, soil quality, and productivity change considerably with elevation [12, 13]. As a consequence, tropical mountains are characterized by a wide array of habitats with a highly patchy distribution given the high topographic heterogeneity of these mountains [11, 13]. Such disparity in environmental conditions, together with the temporal environmental stability of tropical mountains is expected to promote specialization to local conditions [14, 15], and hence, the expression of local phenotypes. Such a mechanism might promote speciation, generating the hyperdiversity observed in tropical mountains. However, other factors might counter the prevalence of local phenotypes. For example, depending on the degree of population connectivity across ecosystems and the extent of climate-induced distributional shifts associated with paleoclimatic conditions (e.g., ), a generalist phenotype strategy might be favored [8, 17, 18].
Using a geometric morphometric approach and ecomorphological analyses, we test for two contrasting patterns of phenotypic variation. Specifically, we test for (i) a geographically unstructured, generalist phenotype strategy of limited morphological differentiation between populations across environments, or (ii) a localized phenotype strategy with morphological differentiation between populations from different environments, with a strong association between skull morphology and local environmental conditions.
A visual examination of the extent of size and shape variation in the skulls of A. mollis individuals across environments indicates high intrapopulation variability, where size and shape variation was measured by the loge-transformed centroid size  and by all non-zero-variance principal components of a PCA on the covariance matrix of either the size-corrected (i.e., controlling for allometric effects; see Methods), or uncorrected, symmetric component of the landmark configuration , respectively. Moreover, limited morphological differentiation among populations and ecosystems is also apparent, with the exception of those from the highest ecosystem of the Central Andes – the wet puna (hereafter, referred to as puna; Figure 1); note that ecosystems correspond to biophysically defined regions (; see below for additional discussion between ecosystems and environmental conditions).
Sample size of individuals available for the analyses
No. of localities
No. of individuals
Mean no. of individuals per locality
No. individuals by locality (♀/♂)
A scatterplot of the first set of PLS components of the size analysis shows that the association of skull size with environment is mainly driven by the smaller size of the majority of puna individuals (the single PLS of morphology in this analysis is negatively associated with skull size) (Figure 3a). In contrast, scatterplots of the shape data for the first 2 sets of components show a linear pattern of covariation between morphological and environmental variation (Figure 3b, c). In this latter analyses, the first morphological PLS axis, which is significantly correlated with latitude (Pearson’s r = 0.42, p-value = 0.007), mostly reflects differences in the volume of the braincase (Figure 3d) and presents no obvious association with ecosystem. The second morphological PLS axis separates populations according to elevation (Pearson’s r = −0.55, p-value < 0.001) by differences associated with multiple regions of the skull that affect both the breadth of the braincase and the length of the rostrum (Figure 3d). The morphological distinctiveness of puna populations does not correspond to latitudinal environmental variation (see below for a discussion of the contribution of spatial and genetic isolation to the distinctiveness of the puna phenotype), but instead to differentiation of mid- and high-elevation habitats (Figure 3c). It is important to note that the fact that puna individuals appear as partially distinct only in the second set of PLS axes is not necessarily unusual because PLS axes are not expected to capture the main axis of morphological differentiation given that they do not maximize the within block variance [47, 48].
The analyses revealed limited support for local phenotypic structuring of the soft grass mouse, A. mollis, given the lack of consistent morphological differentiation of the skull across environments (Figures 2 and 3). Although a significant covariation trend between environmental and size and shape variation is recovered (Figure 4), it explains limited amount of the phenotypic variance, and is on the same order as the exclusive contribution of genetic and spatial isolation (Figure 4b). Moreover, the association between the environment and size and shape variation would no doubt be (at least in part) weakened if the extensive amount of local morphological variability was considered (Figure 3; as noted in the results and methods, population means instead of individuals were analyzed to avoid the confounding problems of population sample sizes). These findings suggest that A. mollis’ skull morphological variation related to local environmental conditions have a significant, but limited, effect on overall skull shape and size. The primary exception to what appears to be a geographically unstructured generalist phenotype is the high-elevation puna Andean ecosystem in the southern portion of A. mollis distribution. This group of individuals is consistently morphologically distinct from individuals from the other ecosystems across the majority of analyses – it even differs from populations from similar elevations but different ecosystem (i.e., páramo; Figure 2). Taken together, these results suggest that the skull of this species fits neither a strict generalist phenotype strategy (i.e., a geographically unstructured phenotype throughout its range) nor a strict localized phenotype strategy (i.e., different local phenotypes).
Limited morphological specialization in the skull?
The limited amount of geographically structured morphological differentiation observed throughout most of the broad environmental gradients A. mollis experience is noteworthy in light of previous studies that have shown that skulls commonly vary within species in response to environmental conditions [51, 52]. Not only have previous studies uncovered moderate to considerable levels of size and shape differences in vertebrate’s skulls due to diet, latitude, temperature, elevation, precipitation, seasonality, and/or productivity, or combinations of these variables [53–55], but mice in particular have been shown to experience significant and rapid morphological changes in response to changes in temperature, precipitation, and human population density over the last 100 years .
The weak environment-morphology association is not attributable to a general lack of morphological or genetic variation (Figure 5, see also Additional file 2). To the contrary, the species is characterized by substantial morphological variability (even if we exclude the differences between puna and the other populations, Figures 2 and 3; also see [23, 57, 58]) and genetic variation, with relatively large average pairwise sequence divergence between individuals (5.6 ± 4.9% for all data, and 4.83 ± 5.41% when puna individuals are excluded, Additional file 2). In contrast to other mice with broad geographic ranges that do show localized morphological differentiation (e.g., [25, 33]), the observed variation among individuals within populations suggests that the absence of local specialization may result from a relaxed association in A. mollis between skull morphology and ecological performance (cf. ) (i.e., relaxed selection), especially considering that the variation is present irrespective of whether individuals experience similar biotic and abiotic conditions (i.e., occur at the same locality). Under this hypothesis, environmental canalization of skull morphology would be relaxed due to weakened effective selection against alternative phenotypes, possibly because of small effective population size or by recent or frequent environmental changes , for instance, due to human-induced landscape changes or natural climatic events. Alternatively, the variability might reflect a general ecological plasticity in the species [21, 23], which might be favored to increase the species’ ecological breadth . In this case, the observed morphological variation among coexisting individuals could reflect a strategy to reduce intraspecific competition under high local abundances (typical of A. mollis) and maintain high adaptability potential [61, 62], as suggested for some other generalist vertebrate species [63, 64], including some species of mice . Under this latter scenario, the microhabitat experienced by an individual throughout development may be more important in determining skull variation in ecological-plastic species than macro-environmental conditions (i.e., the differences in habitat that is captured by the coarse-grained variables used here). Individual variation under this scenario could arise for instance from variation in individuals’ diet, as have been observed in feeding trials in deer mice . Testing of these alternatives (and at this point, speculative scenarios) requires detailed eco-morphological studies of multiple cohorts through time, and hence, goes beyond this contribution. Nevertheless, future studies on this topic might significantly add to our understanding of the role that environment plays in morphological evolution and ecological specialization.
It remains to be seen if similar patterns of morphological variation are observed in other tropical generalist species. It is possible that A. mollis may be exceptional among tropical species, especially considering the narrow elevation ranges and high species turnover typical of tropical mountains [11, 13, 66]. However, our results raise questions about the general expectation that locally adapted populations will necessarily predominate in the tropics [14, 15]. Moreover, our results pose the question of whether the general lack of strong geographically structured morphological variation observed in A. mollis (with the exceptions and possible caveats discussed above) may be in part responsible for its exceptional environmental tolerance and broad geographic distribution (cf. ), and highlight the contingency of eco-morphological patterns on the natural history and geographic setting of the species involved.
Uniqueness of puna individuals
Although A. mollis generally shows limited evidence for geographically structured morphological phenotypes (Figures 2 and 3), there is of course the exception of the morphological distinction between individuals from the puna ecosystem and the rest of populations. These distinct individuals are noticeably smaller and partially distinguishable both in uncorrected and size-corrected shape components of variation (most evidently so in the size-corrected dataset; Figure 2) – note that such distinction seems unlikely to be a sampling artifact given the magnitude of the size differences (Figure 2a). However, why such a morphological break is observed here, but not between other ecological transitions over environmental gradients that are just as extreme (Additional file 1) remains unexplained (see below for further discussion).
Summary of PLS axes for size and shape analyses
PC1 (mean temperature)
PC2 (annual precipitation)
PC3 (precipitation maximum)
PC4 (vegetation coverage)
PC5 (productivity + vegetation)
PC6 (seasonality + vegetation)
PC8 (temperature seasonality)
PC9 (summer precipitation)
PC10 (precipitation seasonality)
All these environmental changes, which are also associated with a significant turnover of resources that likely impact the diet of A. mollis, may contribute to different biomechanical pressures on puna individuals cf. [70, 71]. This possibility seems feasible when considering that a previous study of the diet of other species of Akodon in southwestern Peru revealed a significant relationship between the proportion of insects in the diet and elevation . Furthermore, similar changes in diet and associated morphological traits with elevation have also been observed in other cricetid mice [69, 73]. Thus, it is certainly plausible (although purely speculative at this point) that such interactions between direct physiological constraints imposed by the challenging environmental conditions of tropical highlands and indirect pressures imposed by dietary constraints might be partially responsible for the differences in skull morphology observed in the high-elevation populations of A. mollis, as in cricetid mice [25, 26].
Alternatively, it is possible that the morphological distinctiveness of the puna individuals is caused by some degree of genetic isolation of these highland populations. As seen in other systems, where steep ecological transitions are present, genetic isolation and strong phenotypic differences can arise and be maintained even between populations in close proximity [74–76]. Our preliminary exploration of levels of population genetic differentiation seems to partially support this possibility. However, unexplained patterns of genetic variation suggest that this alone cannot explain the morphological distinctiveness of puna populations. For example, the average cytochrome-b pairwise nucleotide differences between the populations for which we have genetic data showed that both puna and some high-elevation páramo populations differed markedly from the rest of populations (Additional 2). Moreover, these high-elevation páramo populations are genetically distinct from populations that are geographically proximate to them (and more so than the puna populations are from the other populations) (Figure 5b). Yet, unlike the puna individuals, there is only limited morphological differentiation between these high-elevation páramo populations and all other populations. These observations make it unlikely that the morphological distinction of puna individuals is exclusively driven by their degree of genetic isolation. Still, this question deserves further exploration given the claim that A. mollis may be a species complex has been made, albeit based on limited sampling .
Based on consideration of other genetically divergent populations, and in particular some populations from the páramo, it seems that the observed phenotypic distinctiveness of the puna individuals is not simply a function of the abiotic and biotic conditions unique to high elevation environments and their environmental isolation from lower environments , which could prevent the dilution effect of gene flow from lower populations . One possibility is that divergence of the puna populations reflects the interplay of stochastic and deterministic factors. For example, recent work demonstrates how species divergence may reflect an interaction of past demographic conditions (including the stochastic effects associated with changes in population size) that accompanies climate-induced distributional shifts and the ecological attributes of species (including whether the taxon tracks shifts in their habitat and whether they are spatially restricted owing to particular habitat affinities) . Hypothetically, for instance, if puna populations have been unable to migrate out of the puna due to its environmental isolation, it is plausible that they have been forced into a more specialized morphology due to the marked cycles of aridification this ecosystem experienced during the Pleistocene . Additional studies that specifically address the origin and phylogenetic relationships of these genetically distinct populations are required before a more definitive conclusion about the validity of this hypothesis is reached.
Even though high levels of ecological specialization has been proposed as a principal mechanism for generating tropical diversity [14, 15], the ecomorphological analyses suggest that morphological specialization in the skull of A. mollis is limited, except for the localized phenotype of individuals from the puna. This finding suggests that A. mollis’ skull does not fit either a strict generalist or localized phenotype strategy, but a mix of the two, with limited geographically structured morphological variation thorough most of its broad geographic range. Together these results offer insights into the processes that generate and maintain diversity in the tropical Andes, a region that has been previously proposed to be an important center of differentiation and diversification [79–81]. Aside from the morphological disjunction identified between puna populations and the rest of populations, the lack of consistent and strong morphological differentiation across environments, and wide geographic range of A. mollis suggest that additional mechanisms of diversification in tropical systems may deserve more attention than they have received. The geographic structure of phenotypic variation in the skull of A. mollis may be exceptional considering that other morphological structures of this species have not been studied in A. mollis and the wide ecological tolerance of this mouse compared to other tropical species. Nevertheless, with these caveats in mind (as well as those regarding the interpretation of results given the small sample sizes of some populations) our results also have important implications for understanding biological resilience to environmental change in tropical mountains. Specifically, even though tropical mountain habitats are predicted to be disproportionally susceptible to ongoing environmental changes [82, 83], the apparent adaptability of A. mollis suggest that it may be able to accommodate a broad range of conditions, and hence, be more resilient. Future studies that assess the generality of these findings and explore its mechanistic basis are expected to further advance our understanding of morphological evolution in one of the most diverse ecosystems on Earth.
Morphological variation was assessed in the complete skulls of 153 A. mollis individuals sampled across its entire geographic range in Peru (Figure 1; Table 1). Specimens were obtained from the Museo de Historia Natural “Javier Prado”, Universidad Nacional Mayor de San Marcos (UNMSM) in Lima, Peru and the Field Museum of Natural History in Chicago (FMNH), US, and collected by L.L. in northern Peru following the American Society of Mammalogists’ guidelines  and University approved procedures for the manipulation of mammals (see Appendix). Given the taxonomic complexity of the genus [58, 85, 86], and the poorly defined diagnosis available for A. mollis, we based our taxonomic identification of specimens on a combination of external and internal morphological characters (e.g., a robust braincase, short rostrum, zygomatic plate broad and not inclined [24, 57, 87, 88]). Only adult specimens were used to minimize the effects of ontogenetic differences [24, 89]. Adults were defined as individuals with all three molars completely erupted and with the posteroloph in the third molar eroded (which corresponds to ages 3 to 5 ). Sex and locality information was recorded for all 153 specimens from skin tags and collectors field notes. When available, the locality’s latitude and longitude was also recorded. Otherwise, specimens were georeferenced based on the collector’s notes following a point-radius method . We assessed the confidence of our georeferencing by contrasting the elevation given in the field and museum notes with one we obtained from a Digital Elevation Model (DEM) from the Shuttle Radar Topography Mission (SRTM ) based on the coordinates estimated.
For each locality we compiled information from 21 ecogeographical variables (Table 2) that have been shown to be of biological relevance in a wide variety of vertebrates [93, 94]. These variables include summaries of temperature and precipitation patterns , including both mean, maximum and minimum values, as well as vegetation cover  and productivity . To minimize the problem of collinearity among these environmental variables we run a PCA on these data and used the resultant orthogonal components in our analyses (Table 2). Because of the resolution of the ecogeographical data (climatic data: 1 km2, vegetation cover and productivity: 0.25 km2, and elevation: 0.02 km2), localities in close proximity (i.e., less than 1 km apart) were treated as a single locality, resulting in 40 unique localities (see Appendix). All geographic analyses were performed in ArcGIS v.9.3 .
In addition, for 95 individuals for which we were able to obtain tissues (these individuals were collected in 22 of the 40 populations) we extracted DNA using a Qiagen kit and amplified a 1123 bp-region of the mitochondrial cytochrome b gene following the procedures outlined by Smith and Patton . After sequencing, these fragments were cleaned in Sequencher v4.6  and aligned in MacClade v4 . A haplotype frequency matrix was extracted from the aligned sequences and used in a PCA on the covariance matrix (for details see ). Individuals’ scores on the first three principal components, which together accounted for 71.66% of the genetic variance, were averaged by population and used to control for the effect of genetic distance in the spatial regressions (see below). In addition, and in light of the eco-morphological results, we performed an Isolation By Distance analysis (IBD, ) using Mantel tests  based on 10000 permutations to assess the spatial structure of the morphological and genetic data.
The digitized landmarks were standardized using a full Procrustes superimposition followed by an orthogonal projection into the tangent space [105, 106] to remove the effects of position, size, and orientation [48, 107]. After superimposition, we searched for outliers in the dataset (i.e., individuals with landmarks that strongly deviate from the mean shape); outlier individuals were redigitized to assure they were not the product of digitizing error. We then used the vetted superimposed data to estimate size and shape skull components. Skull size was quantified as the centroid size of the superimposed landmark configuration, calculated as the square root of the sum of all squared distances between each landmark and the configuration centroid . To minimize departure from normality, the loge-transformed centroid size was used in all analyses. Skull shape was quantified using the symmetric component of the morphological variation to avoid redundancy and to control for assymmetric differences in the skull . Specifically, skull shape was quantified by all non-zero variance components of a Principal Component Analysis (PCA) on the covariance matrix of the symmetric coordinates.
Sexual dimorphism on size was assessed using a standard sex by locality ANOVA on the loge-transformed centroid size with locality as a block factor, whereas sexual dimorphism in shape was assessed by testing for differences in the scores on the shape principal components obtained using a sex by locality MANOVA. Both the ANOVA and MANOVA were run in R v2.15.1 . Because no sexual dimorphism was detected on size (F1 = 0.67, p = 0.42; p-value interaction term = 0.89) or shape (Wilks’ λ = 0.38, F54/38 = 1.15, p = 0.33; p-value interaction term = 0.09), all specimens were pooled for further analyses.
Allometric effects were assessed by running independent regressions of the symmetric coordinates onto loge centroid size for different sets of individuals grouped according to the ecosystem in which they were collected (ecosystems definitions followed ; Additional file 5). We verified the presence of similar allometric trajectories in all groups (i.e., similar regression slopes) in tpsRegr . Although differences in regression intercepts were recovered (Wilks’ λ < 0.01, F432/154.8 = 2.72, p < 0.01), no significant slope differences were found (Wilks’ λ <0.01, F432/138.8 = 0.98, p = 0.56). Because the redundancy of symmetric data might compromise the significance obtained, we verified the robustness of the results by running a Multivariate Analysis of Covariance (MANCOVA) on the non-zero variance principal components of shape using the loge-centroid size as a covariate and ecosystems as groups in R v2.15.1 . Since the results were consistent (i.e., neither the main effect of sex, nor the interaction term in the MANCOVA were significant , Wilks’ λ = 0.08, F260/453.83 = 0.98, p = 0.15), we used the residuals of a regression of the symmetric coordinates onto loge-transformed sized, pooling all individuals together, as a size-corrected shape component. We then run a PCA on the covariance matrix of these residuals and kept all non-zero variance components as our size-corrected shape component for all analyses.
The extent of among individual variability in skull size was visually assessed by plotting the loge-centroid size of specimens ordered according to the elevation at which they were collected; note that elevation is a well-suited proxy for environmental differences in tropical regions where elevation represents the most evident axis of climatic and ecological variation ; see Table 1). Uncorrected and size-corrected skull shape variation was visually assessed using between-groups PCA (BG-PCA, ), which is a modification of the most-commonly-used PCA that takes into account a priori individual grouping by identifying PCs from the variance-covariance matrix of group mean shapes and then projecting all individuals into these components . We chose this approach as it represents a compromise between a PCA, which is a suboptimal analyses for revealing group differentiation, and a Canonical Variate Analysis or Discriminant Analysis, which is prone to over-identify group differences . Specifically, we constructed BG-PCA axes using the ecosystem in which individuals were collected.
Given the highly unequal sample sizes across populations (Table 1), which reflects natural differences in the abundance of A. mollis, we averaged all size and shape data by population for the following analyses. In the case of shape data, we chose to average the scores of the uncorrected and size-corrected shape PCAs run on individuals (see details above) instead of averaging the landmark coordinates by population first and then running PCAs on the averaged data to avoid maximizing differences between populations. All analyses hereafter were performed on the population-averaged size and shape components. To explore the association between environmental conditions and morphological variation we performed 3 independent two-block Partial Least Squares analyses (PLS). We chose this method because it is robust to the underlying structure of the data as it does not rely on a particular variable model . The first two PLS analyses were based on the averaged-by-population PC scores of all non-zero-variance PCs from either uncorrected or size-corrected data (as one block) and the first 10 principal components of the standardized environmental data (as another block, see Data acquisition section), which together accounted for 99.91% of the environmental variance. We also performed a third PLS analysis between averaged loge centroid size and the same 10 principal components of the environmental data. In all three cases we summarized the overall strength of the association using the RV coefficient, which is a multivariate statistic analog to the squared correlation and ranges from 0 (uncorrelated) to 1 (completely correlated) [106, 111, 112].
In addition, to investigate the degree to which environmental conditions explain differences in skull size and shape after accounting for the effect of spatial autocorrelation (because skull similarity decreased as a function of distance between populations – evidenced by Moran’s I correlogram for size and Mantel’s correlogram for shape; results not shown), we run Spatial EigenVector Mapping regressions (SEVM; [49, 50]). We chose SEVM because it has been shown to minimize spatial autocorrelation more efficiently than other techniques . Using this spatially-explicit technique we performed a regression of the loge-transformed centroid size onto the first three principal components of the environmental data, which together accounted for 87.66% of the environmental variance, in SAM  –we chose 3 instead of 10 environmental components to minimize the risk of overfitting given our sample size. We then repeated these analyses on the population-averaged scores of all the non-zero-variance principal components of the uncorrected and size-corrected data. We combined the results of these regressions, separately for the uncorrected and size-corrected data, by adding the amount of variance explained by the SEVM regression on each component, weighted by the corresponding proportion of variance explained by each principal component. Finally, for the subset of our sample of populations for which we had genetic data (22 of 40 populations), we ran additional SEVM regressions that include the same first three principal components of the environmental data and additionally the first three principal components of the genetic data as predictors (see Data Acquisition section). For all SEVM analyses we used the automatic selection procedure of SAM to estimate the truncation distance and the spatial filters to use. We verified the effectiveness of these procedures by analyzing the degree of spatial autocorrelation of the regressions’ residuals using Moran’s I correlograms. Unless otherwise noted, all analyses were run in MorphoJ .
Appendix – specimens used in the analysis
The 153 specimens used in the analyses are listed below. Geographical coordinates and elevations were recovered from georeferencing collector’s notes using point-radius method described in the Methods section. Abbreviations: UMMZ (University of Michigan Museum of Zoology, Ann Arbor, Michigan), MUSM (Museo de Historia Natural Universidad Nacional Mayor de San Marcos, Lima, Peru), FMNH (Field Museum of Natural History, Chicago, Illinois); for specimens without a museum catalog number assigned, the collector number (in lowercase) is provided. Population numbers are listed in square brackets; numbers of populations with genetic data are in bold.
ANCASH: Huaraz, Tullparaju, 4300, -9.03; -77.67 (FMNH 81371, 81373) ; Huari, Canrash, 4370 m, -9.68; -77.05 (mcp 54, 55, 56, 59, 63) ; Huari, Chacacmonte, 4220 m, -9.68; -77.11 (mcp 34, 35, 36, 42) ; Huari, Jupro, 4000 m, -9.59; -77.08 (mcp 67, 68) ; Huari, Paccha, 4240 m, -9.63; -77.12 (mcp 04, 05, 11, 15, 18, 20) ; Huari, Pumahuain, 4250 m, -9.66; -77.13 (mcp 24) ; Huari, Río Mosna, between Chavín and San Marcos, 3100 m, -9.55;-77.17 (FMNH 129213, 129215, 129219, 129225) ; Santa, Macate, 2250 m, -8.77; -78.08 (FMNH 20899, 20905, 20909) .
CAJAMARCA: Cajamarca, Cajamarca, 2890 m, -7.17; -78.51 (FMNH 19275, 19277, 19281, 19283) ; Celendín, Hacienda Limón, 2750 m, -6.83; -78.08 (FMNH 19285, 19287) ; Contumaza, Bosque Cachil, entre Cascas y Contumaza, 3050 m, -7.39; -78.78 (jaa 178, vpt 1674) ; Cutervo, San Andrés de Cutervo, 2070 m, -6.24; -78.72 (llw 1197, 1212) ; Cutervo, San Andrés de Cutervo, Cutervo National Park, 100 m over El Tragadero, 2910 m, -6.25; -78.77 (llw 1085, 1086, 1087, 1088, 1089, 1093, 1094, 1095, 1096, 1098, 1100, 1102, 1106, 1108, 1109, 1112, 1114, 1115, 1120, 1122, 1126, 1131, 1132, 1136, 1140, 1143, 1145, 1148, 1151, 1153, 1154, 1155, 1161, 1164, 1165, 1166, 1167, 1169, 1173, 1174, 1179, 1180, 1181, 1183) ; Cutervo, San Andrés de Cutervo, 4 km W San Andrés de Cutervo, 2250 m, -6.26; -78.72 (jaa 135, 139, jlm 175, vpt 1597) ; San Ignacio, Tabaconas, Cerro Coyona (Tabaconas-Namballe National Sanctuary), 3310 m, -5.23; -79.28 (jaa 805) ; San Ignacio, Tabaconas, Piedra Cueva in Cerro Coyona (Tabaconas-Namballe National Sanctuary), 3010 m, -5.27; -79.27 (llw 926, 929, 930, 946, 967, 976) ; San Ignacio, Tabaconas, Cerro Coyona (Tabaconas-Namballe National Sanctuary), 2790 m, -5.27; -79.27 (llw 995) ; San Ignacio, Tabaconas, Cerro La Viuda (Tabaconas-Namballe National Sanctuary's Buffer Zone), Campamento 1, 2760 m, -5.29; -79.34 (llw 1003, 1004, 1013, 1023) ; San Ignacio, Tabaconas, Cerro La Viuda (Tabaconas-Namballe National Sanctuary's Buffer Zone), Campamento 2, 2240 m, -5.28; -79.32 (llw 1048, 1082) ; San Miguel, La Florida, Agua Azul, 1660 m, -6.89; -79.08 (llw 491, 503, 511) ; Santa Cruz, 2.5 km E Monteseco, 2120 m, -6.85; -79.09 (jlm 208, vpt 1636) ; Santa Cruz, Catache, 3.81 km NE from Monteseco, 2150 m, -6.82; -79.08 (lhl 92, 93, 116, llw 1241, 1248, 1249, 1273, 1274) .
LA LIBERTAD: Otuzco, Hacienda Llagueda, 2250 m, -7.72; -78.72 (FMNH 19317, 19321, 19325) ; Otuzco, Summit between Otuzco and Llagueda, 2850 m, -7.90; -78.58 (FMNH 19849, 19851) ; Sánchez Carrión, Sanagorán, 2850 m, -7.79; -78.14 (lhl 85, llw 1219, 1220, 1221, 1222, 1225, 1226, 1227, 1232) ; Sánchez Carrión, Sanagorán, 2750 m, -7.78; -78.15 (vpt 2251, 2252, 2263) ; Santiago de Chuco, Cachicadán, 2870 m, -8.06; -78.17 (vpt 2277) ; Santiago de Chuco, Campamento Callacuyán, Quebrada Quishuara Sur, 4040 m, -7.94; -78.23 (avg 143) ; Santiago de Chuco, Campamento Callacuyán, arriba de Laguna Negra, 4020 m, -7.95; -78.24 (mvc 313, 323) ; Santiago de Chuco, Campamento Callacuyán, hondonada Laguna Viscachas, 4110 m, -7.95; -78.23 (mvc 325, 326) ; Santiago de Chuco, Campamento Callacuyán, Bosque de Polylepis, 3990 m, -7.92; -78.25 (mvc 333) ; Santiago de Chuco, Campamento Callacuyán, Laguna Pozo Hondo, 4130 m, -7.95; -78.25 (vpt 2380, 2387, 2390) ; Trujillo, Menocucho, 540 m, -8.02; -78.8 (FMNH 19329, 19333, 19335, 19343) .
PIURA: Ayabaca, Ayabaca, 2870 m, -4.63; -79.72 (FMNH 81379) ; Huancabamba, Canchaque, 1200, -5.40; -79.60 (FMNH 81357) ; Huancabamba, 2 km S of Canchaque, 1320, -5.50; -79.60 (FMNH 83441) ; Huancabamba, El Carmen de la Frontera, Carmen de la Frontera, Alto Samaniego, 2360 m, -5.11; -79.35 (ucf 43) ; Huancabamba, Huancabamba, 2020 m, -5.23; -79.47 (FMNH 84203) ; Huancabamba, Huancabamba, km 30 on road to San Ignacio, 2430 m, -5.25; -79.48 (FMNH 81353, 81363, 81365, 81367) ; Huancabamba, Tambo, 2870 m, -5.35; -79.55 (FMNH 81359) .
We thank Andrea Cardini, María R. Marchán-Rivadeniera, Philip Myers, Leandro Monteiro and two anonymous reviewers for their comments and suggestions on previous versions of the manuscript, and Eladio J. Márquez for input on geometric morphometrics. We also thank Víctor Pacheco (Museo Javier Prado, Universidad Nacional Mayor de San Marcos, Lima) and Bruce Patterson (Field Museum of Natural History, Chicago) for granting access to specimens under their care, and Nina Cummings for access to the Field Museum photographic archives (Figure 1, photograph of Menocucho). Financial support was provided by University of Michigan Department of Ecology and Evolutionary Biology’s Block Grants and University of Michigan Museum of Zoology’s Hinsdale Walker Scholarships to D. Alvarado-Serrano and L. Luna, scholarships from The Society of Hispanic Professional Engineers (SHPE) and the Robert W. Storer Fund to L. Luna, and National Science Foundation grant (DEB-07-15487) to L. L. Knowles. Additional funds were provided by University of Michigan Museum of Zoology’s Mammal Division and Frederick M. Gaige Research Endowments. Collection permits were granted to L. Luna by the Instituto Nacional de Recursos Naturales, INRENA, Perú (N° 032 C/C-2006-INRENA-IANP; N° 070-2007-INRENA-IFFS-DCB).
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