Skip to main content

Advertisement

Log in

Rapid morphological divergence in two closely related and co-occurring species over the last 50 years

  • Original Paper
  • Published:
Evolutionary Ecology Aims and scope Submit manuscript

Abstract

We studied morphological variation in two closely related and ecologically similar species of mice of the genus Peromyscus, the deer mouse (P. maniculatus) and white-footed mouse (P. leucopus), over the last 50 years in Southern Quebec. We found that contemporary populations of the two species are distinct in morphology and interpret this differentiation as a reflection of resource partitioning, a mechanism favouring their local coexistence. While there was no size trend, geographic or temporal, both species displayed a concomitant change in the shape of their skull over the last 50 years, although this change was much more apparent in the white-footed mouse. As a result, the two species diverged over time and became more distinct in their morphology. The observed changes in morphology are large given the short time scale. During this period, there was also a shift in abundance of the two species in Southern Quebec, consistent with the northern displacement of the range of the white-footed mouse in the last 15 years. Our study thus reports the changes in morphology of two co-occurring mammal species that were accompanied by changes in distribution and local abundance, potentially in response to rapid climate change.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

References

  • Adams DC, Otárola-Castillo E (2013) Geomorph: an R package for the collection and analysis of geometric morphometric shape data. Methods Ecol Evol 4:393–399

    Article  Google Scholar 

  • Alexander JM, Diez JM, Levine JM (2015) Novel competitors shape species’ responses to climate change. Nature 525:515–518

    Article  CAS  PubMed  Google Scholar 

  • Alhajeri BH, Steppan SJ (2015) Association between climate and body size in rodents: a phylogenetic test of Bergmann’s rule. Mamm Biol 81:219–225

    Article  Google Scholar 

  • Anderson CS, Cady AB, Meikle DB (2003) Effects of vegetation structure and edge habitat on the density and distribution of white-footed mice (Peromyscus leucopus) in small and large forest patches. Can J Zool 81:897–904

    Article  Google Scholar 

  • Aquadro CF, Patton JC (1980) Salivary amylase variation in Peromyscus: use in species identification. J Mammal 61:703–707

    Article  Google Scholar 

  • Ashton KG, Tracy MC, Queiroz A (2000) Is Bergmann’s rule valid for mammals? Am Nat 156:390–415

    Google Scholar 

  • Austin GE, Rehfisch MM (2005) Shifting nonbreeding distributions of migratory fauna in relation to climatic change. Glob Change Biol 11:31–38

    Article  Google Scholar 

  • Baker RH (1968) Habitats and distributions. In: King JA (ed) Biology of Peromyscus (Rodentia). The American Society of Mammalogists, Stillwater, pp 98–122

    Google Scholar 

  • Barun A, Simberloff D, Meiri S et al (2015) Possible character displacement of an introduced mongoose and native marten on Adriatic Islands, Croatia. J Biogeogr 42:2257–2269

    Article  Google Scholar 

  • Bates D, Maechler M, Bolker B et al (2015) Fitting linear mixed-effects models using lme4. J Stat Softw 67:1–48

    Article  Google Scholar 

  • Bengtsson J (1989) Interspecific competition increases local extinction rate in a metapopulation system. Nature 340:713–715

    Article  Google Scholar 

  • Blois JL, Zarnetske PL, Fitzpatrick MC et al (2013) Climate change and the past, present, and future of biotic interactions. Science 341:499–504

    Article  CAS  PubMed  Google Scholar 

  • Bocedi G, Atkins KE, Liao J et al (2013) Effects of local adaptation and interspecific competition on species’ responses to climate change. Ann N Y Acad Sci 1297:83–97

    PubMed  Google Scholar 

  • Bookstein FL (1991) Morphometric tools for landmark data: geometry and biology. Cambridge University Press, Cambridge

    Google Scholar 

  • Brown WL, Wilson EO (1956) Character displacement. Syst Zool 5:49–64

    Article  Google Scholar 

  • Caumul R, Polly PD (2005) Phylogenetic and environmental components of morphological variation: skull, mandible, and molar shape in marmots (Marmota, Rodentia). Evolution 59:2460–2472

    Article  PubMed  Google Scholar 

  • Chen I-C, Hill JK, Ohlemüller R et al (2011) Rapid range shifts of species associated with high levels of climate warming. Science 333:1024–1026

    Article  CAS  PubMed  Google Scholar 

  • Choate JR (1973) Identification and recent distribution of white-footed mice (Peromyscus) in New England. J Mammal 54:41–49

    Article  Google Scholar 

  • Choate JR, Dowler RC, Krause JE (1979) Mensural Discrimination between Peromyscus leucopus and P. maniculatus (Rodentia) in Kansas. Southwest Nat 24:249–258

    Article  Google Scholar 

  • Cox PG, Rayfield EJ, Fagan MJ et al (2012) Functional evolution of the feeding system in rodents. PLoS ONE 7(4):e36299

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Cramer MJ (2014) Seeds of doubt: feeding preferences of white-footed deer mice (Peromyscus leucopus noveboracensis) and woodland deer mice (Peromyscus maniculatus gracilis) on maple (genus Acer) seeds. Can J Zool 92:771–776

    Article  Google Scholar 

  • Davis MB, Shaw RG (2001) Range shifts and adaptive responses to Quaternary climate change. Science 292:673–679

    Article  CAS  PubMed  Google Scholar 

  • Davis MB, Shaw RG, Etterson JR (2005) Evolutionary responses to changing climate. Ecology 86:1704–1714

    Article  Google Scholar 

  • Dayan T, Simberloff D (2005) Ecological and community-wide character displacement: the next generation. Ecol Lett 8:875–894

    Article  Google Scholar 

  • Diffenbaugh NS, Field CB (2013) Changes in ecologically critical terrestrial climate conditions. Science 341:486–492

    Article  CAS  PubMed  Google Scholar 

  • Dray S, Dufour A-B (2007) The ade4 package: implementing the duality diagram for ecologists. J Stat Softw 22:1–20

    Article  Google Scholar 

  • Drickamer LC (1972) Experience and selection behavior in the food habits of Peromyscus: use of olfaction. Behaviour 41:269–287

    Article  CAS  PubMed  Google Scholar 

  • Eiserhardt WL, Borchsenius F, Plum CM et al (2015) Climate-driven extinctions shape the phylogenetic structure of temperate tree floras. Ecol Lett 18:263–272

    Article  PubMed  Google Scholar 

  • Fiset J, Tessier N, Millien V et al (2015) Phylogeographic structure of the white-footed mouse and the deer mouse, two Lyme disease reservoir hosts in Quebec. PLoS ONE 10:e0144112

    Article  PubMed  PubMed Central  Google Scholar 

  • Gaitan J, Millien V (2016) The effect of stress level and parasite load on movement pattern in a small mammal reservoir host for Lyme disease. Can J Zool 94:565–573

    Article  Google Scholar 

  • Gardner JL, Peters A, Kearney M et al (2011) Declining body size: a third universal response to warming? Trends Ecol Evol 26:285–291

    Article  PubMed  Google Scholar 

  • Gienapp P, Teplitsky C, Alho JS et al (2008) Climate change and evolution: disentangling environmental and genetic responses. Mol Ecol 17:167–178

    Article  CAS  PubMed  Google Scholar 

  • Gingerich PD (1993) Quantification and comparison of evolutionary rates. Am J Sci 293A:453–478

    Article  Google Scholar 

  • Grant PR (1976) An 11-year study of small mammal populations at Mont St. Hilaire, Quebec. Can J Zool 54:2156–2173

    Article  Google Scholar 

  • Grant PR, Grant BR (2006) Evolution of character displacement in Darwin’s Finches. Science 313:224–226

    Article  CAS  PubMed  Google Scholar 

  • Graves S, Maldonado J, Wolff JO (1988) Use of ground and arboreal microhabitats by Peromyscus leucopus and Peromyscus maniculatus. Can J Zool 66:277–278

    Article  Google Scholar 

  • Haldane JBS (1949) Suggestions as to quantitative measurement of rates of evolution. Evolution 3:51–56

    Article  CAS  PubMed  Google Scholar 

  • Hamilton WJ Jr (1941) The food of small forest mammals in eastern United States. J Mammal 22:250–263

    Article  Google Scholar 

  • Hedrick PW (2013) Adaptive introgression in animals: examples and comparison to new mutation and standing variation as sources of adaptive variation. Mol Ecol 22:4606–4618

    Article  PubMed  Google Scholar 

  • Herrel A, Huyghe K, Vanhooydonck B et al (2008) Rapid large-scale evolutionary divergence in morphology and performance associated with exploitation of a different dietary resource. Proc Natl Acad Sci 105:4792–4795

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hibbard CW (1968) Paleontology. In: King JA (ed) Biology of Peromyscus (Rodentia). The American Society of Mammalogists, Stillwater, pp 6–26

    Google Scholar 

  • Holmes MW, Boykins GK, Bowie RC, Lacey EA (2016) Cranial morphological variation in Peromyscus maniculatus over nearly a century of environmental change in three areas of California. J Morphol 277:96–106

    Article  PubMed  Google Scholar 

  • Holt RD (1990) The microevolutionary consequences of climate change. Trends Ecol Evol 5:311–315

    Article  CAS  PubMed  Google Scholar 

  • Hughes L (2000) Biological consequences of global warming: is the signal already apparent? Trends Ecol Evol 15:56–61

    Article  CAS  PubMed  Google Scholar 

  • James FC (1970) Geographic size variation in birds and its relationship to climate. Ecology 51:365–390

    Article  Google Scholar 

  • Johansson J (2008) Evolutionary responses to environmental changes: how does competition affect adaptation? Evolution 62:421–435

    Article  PubMed  Google Scholar 

  • Kamler JF, Pennock DS, Welch C et al (1998) Variation in morphological characteristics of the white-footed mouse (Peromyscus leucopus) and the deer mouse (P. maniculatus) under allotopic and syntopic conditions. Am Midl Nat 140:170–179

    Article  Google Scholar 

  • Landry P, Lapointe F-J (2001) Within-population craniometric variability of insular populations of deer mice, Peromyscus maniculatus, elucidated by landscape configuration. Oikos 95:136–146

    Article  Google Scholar 

  • Ledevin R, Michaux JR, DeFontaine V, Henttonen H, Renaud S (2010) Evolutionary history of the banl vole Myodes glareolus: a morphometric perspective. Biol J Linn Soc 100:681–694

    Article  Google Scholar 

  • Ledevin R, Millien V (2013) Congruent morphological and genetic differentiation as a signature of range expansion in a fragmented landscape. Ecol Evol 3:4172–4182

    Article  PubMed  PubMed Central  Google Scholar 

  • Ledevin R, Quéré J-P, Michaux JR et al (2012) Can tooth differentiation help to understand species coexistence? The case of wood mice in China. J Zool Syst Evol Res 50:315–327

    Article  Google Scholar 

  • Leibold MA, McPeek MA (2006) Coexistence of the niche and neutral perspectives in community ecology. Ecology 87:1399–1410

    Article  PubMed  Google Scholar 

  • Leo ST, Millien V (2016) Microsatellite markers reveal low frequency of natural hybridization between the white-footed mouse (Peromyscus leucopus) and deer mouse (Peromyscus maniculatus) in southern Quebec, Canada. Genome 60:454–463

    Article  PubMed  Google Scholar 

  • Logan T, Charron I, Chaumont D, Houle D (2011) Atlas of climate scenarios for Québec forests. Techical Report ISBN 978-2- 923292-11-3. Produced by Ouranos for Ministère des Ressources naturelles and de la Faune du Québec, pp 1–132

  • Long CA (1996) Ecological replacement of the deer mouse, Peromyscus maniculatus, by the white-footed mouse, P. leucopus, in the Great Lakes Region. Can Field Nat 110:271–277

    Google Scholar 

  • MacArthur R, Levins R (1964) Competition, habitat selection, and character displacement in a patchy environment. Proc Natl Acad Sci 51:1207–1210

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Marrotte R, Gonzalez A, Millien V (2014) Landscape resistance and habitat combine to provide an optimal model of genetic structure and connectivity at the range margin of a small mammal. Mol Ecol 23:3983–3998

    Article  CAS  PubMed  Google Scholar 

  • Martin PR, Martin TE (2001) Ecological and fitness consequences of species coexistence: a removal experiment with wood warblers. Ecology 82:189–206

    Article  Google Scholar 

  • Meiri S, Dayan T (2003) On the validity of Bergmann’s rule. J Biogeogr 30:331–351

    Article  Google Scholar 

  • Millar JS (1989) Reproduction and development. In: King JA (ed) Biology of Peromyscus (Rodentia). The American Society of Mammalogists, Stillwater, pp 169–232

    Google Scholar 

  • Millien V (2006) Morphological evolution is accelerated among island mammals. PLoS Biol 4:e321

    Article  PubMed  PubMed Central  Google Scholar 

  • Millien V, Lyons SK, Olson L et al (2006) Ecotypic variation in the context of global climate change: revisiting the rules. Ecol Lett 9:853–869

    Article  PubMed  Google Scholar 

  • Myers P, Lundrigan BL, Gillespie BW, Zelditch ML (1996) Phenotypic plasticity in skull and dental morphology in the prairie deer mouse (Peromyscus maniculatus bairdii). J Morphol 229:229–237

    Article  CAS  PubMed  Google Scholar 

  • Myers P, Lundrigan BL, Hoffman SMG et al (2009) Climate-induced changes in the small mammal communities of the Northern Great Lakes region. Glob Change Biol 15:1434–1454

    Article  Google Scholar 

  • Ouranos (2015) Vers l’adaptation. Synthèse des connaissances sur les changements climatiques au Québec, Montréal

    Google Scholar 

  • Parmesan C (2006) Ecological and evolutionary responses to recent climate change. Annu Rev Ecol Evol Syst 37:637–669

    Article  Google Scholar 

  • Pelletier F, Garant D, Hendry AP (2009) Eco-evolutionary dynamics. Philos Trans R Soc Lond B 364:1483–1489

    Article  CAS  Google Scholar 

  • Pergams ORW, Ashley MV (1999) Rapid morphological change in island deer mice. Evolution 53:1573–1581

    Article  PubMed  Google Scholar 

  • Pergams ORW, Lacy RC (2008) Rapid morphological and genetic change in Chicago-area Peromyscus. Mol Ecol 17:450–463

    Article  CAS  PubMed  Google Scholar 

  • Pergams ORW, Lawler JJ (2009) Recent and widespread rapid morphological change in rodents. PLoS ONE 4:e6452

    Article  PubMed  PubMed Central  Google Scholar 

  • Pergams ORW, Nyberg D (2001) Museum collections of mammals corroborate the exceptional decline of prairie habitat in the Chicago region. J Mammal 82:984–992

    Article  Google Scholar 

  • Pinheiro J, Bates D, DebRoy S, Sarkar D, R Core Team (2014) nlme: linear and nonlinear mixed effects models. R package version 3.1-117. Available from https://CRAN.R-project.org/package=nlme. Accessed July 2017

  • R Core Team (2014) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna

    Google Scholar 

  • Reed AW, Kennedy PK, Beck ML et al (2004) Using morphologic characters to identify Peromyscus in sympatry. Am Midl Nat 152:190–195

    Article  Google Scholar 

  • Rich SM, Kilpatrick W, Shippee JL et al (1996) Morphological differentiation and identification of Peromyscus leucopus and P. maniculatus in Northeastern North America. J Mammal 77:985–991

    Article  Google Scholar 

  • Rogic A, Tessier N, Legendre P et al (2013) Genetic structure of the white-footed mouse in the context of the emergence of Lyme disease in southern Québec. Ecol Evol 3:2075–2088

    Article  PubMed  PubMed Central  Google Scholar 

  • Rohlf FJ, Slice D (1990) Extensions of the procrustes method for the optimal superimposition of landmarks. Syst Zool 39:40–59

    Article  Google Scholar 

  • Roy-Dufresne E, Logan T, Chmura G et al (2013) Poleward expansion of the white-footed mouse (Peromyscus leucopus) under climate change and implications for the spread of Lyme disease. PLoS ONE 8:e80724

    Article  PubMed  PubMed Central  Google Scholar 

  • Schlager S (2015) Morpho: calculations and visualizations related to Geometric Morphometrics. R package version 2.3.0. Available from https://CRAN.R-project.org/package=Morpho. Accessed July 2017

  • Seifert VA, Clarke BL, Crossland JP et al (2016) A method to distinguish morphologically similar Peromyscus species using extracellular RNA and high-resolution melt analysis. Anal Biochem 508:65–72

    Article  CAS  PubMed  Google Scholar 

  • Simberloff D, Dayan T, Jones C et al (2000) Character displacement and release in the small Indian mongoose, Herpestes javanicus. Ecology 81:2086–2099

    Article  Google Scholar 

  • Slatkin M (1980) Ecological character displacement. Ecology 61:163–177

    Article  Google Scholar 

  • Snijders TAB, Bosker RJ (2012) Multilevel analysis: an introduction to basic and advanced multilevel modeling, 2nd edn. Sage Publishers, London

    Google Scholar 

  • Souto-Lima R, Millien V (2014) The influence of environmental factors on the morphology of red-backed voles Myodes gapperi (Rodentia, Arvicolinae) in Quebec and Western Labrador. Biol J Linn Soc 112:204–218

    Article  Google Scholar 

  • Stuart YE, Losos JB (2013) Ecological character displacement: Glass half full or half empty? Trends Ecol Evol 28:402–408

    Article  PubMed  Google Scholar 

  • Stuart YE, Campbell TS, Hohenlohe PA et al (2014) Rapid evolution of a native species following invasion by a congener. Science 346:463–466

    Article  CAS  PubMed  Google Scholar 

  • Teplitsky C, Millien V (2013) Climate warming and Bergmann’s rule through time: is there any evidence? Evol Appl 7:156–168

    Article  PubMed  PubMed Central  Google Scholar 

  • Tessier N, Noel S, Lapointe F-J (2004) A new method to discriminate the deer mouse (Peromyscus maniculatus) from the white-footed mouse (Peromyscus leucopus) using species-specific primers in multiplex PCR. Can J Zool 82:1832–1835

    Article  CAS  Google Scholar 

  • Theurillat J, Guisan A (2001) Potential impact of climate change on vegetation in the european Alps: a review. Clim Change 50:77–109

    Article  CAS  Google Scholar 

  • Thompson TG, Conley W (1983) Discrimination of coexisting species of Peromyscus in South-Central New Mexico. Southwest. Nat 28:199–209

    Article  Google Scholar 

  • Tobias JA, Cornwallis CK, Derryberry EP et al (2013) Species coexistence and the dynamics of phenotypic evolution in adaptive radiation. Nature 506:359–363

    Article  PubMed  Google Scholar 

  • VanValkenburgh B, Theodor J, Friscia A et al (2004) Respiratory turbinates of canids and felids: a quantitative comparison. J Zool 264:281–293

    Article  Google Scholar 

  • Walsh RE, Aprigio Assis AP, Patton JL, Marroig G, Dawson TE, Lacey EA (2016) Morphological and dietary responses of chipmunks to a century of climate change. Glob Change Biol 22:3233–3253

    Article  Google Scholar 

  • Walther G, Post E, Convey P et al (2002) Ecological responses to recent climate change. Nature 416:389–395

    Article  CAS  PubMed  Google Scholar 

  • Wolf M, Friggens M, Salazar-Bravo J (2009) Does weather shape rodents? Climate related changes in morphology of two heteromyid species. Naturwissenschaften 96:93–101

    Article  CAS  PubMed  Google Scholar 

  • Wolff JO (1985) The effects of density, food, and interspecific interference on home range size in Peromyscus leucopus and Peromyscus maniculatus. Can J Zool 63:2657–2662

    Article  Google Scholar 

  • Wolff JO, Freeberg MH, Dueser RD (1983) Interspecific territoriality in two sympatric species of Peromyscus (Rodentia: Cricetidae). Behav Ecol Sociobiol 12:237–242

    Article  Google Scholar 

  • Wolff JO, Dueser RD, Berry KS et al (1985) Food habits of sympatric Peromyscus leucopus and Peromyscus maniculatus. J Mammal 66:795–798

    Article  Google Scholar 

  • Yom-Tov Y, Geffen E (2006) Geographic variation in body size: the effects of ambient temperature and precipitation. Oecologia 148:213–218

    Article  PubMed  Google Scholar 

Download references

Acknowledgements

We are grateful to landowners and park managers, the staff at the Gault Nature Reserve, field-work assistants and the many graduate students who participated in specimen collection, A. Howell for his help with the Redpath Museum specimens, K. Khidas at the Canadian Museum of Nature, R. Smith who collected the data used in Fig. S2, A. Cardini, the editor and associate editor, and two anonymous reviewers for comments on a previous draft of this manuscript. This work was supported by a FQRNT Team Grant #147236 to VM and AG, NSERC Discovery Grants # 341918-2012 to VM and # 2014-05840 to AG, a Canada Research Chair Tier 1, a Liber Ero Chair and Killam Fellowship to AG, and support from the LabEx Sciences archéologiques de Bordeaux (#ANR-10-LABX-52) to RL.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Virginie Millien.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Fig. S1

Position of the 20 landmarks digitized on the left ventral view of the skull. (1) Anterior extremity between both incisors in the premaxilla; (2) Antero-lateral extremity of left incisor alveolus; (3) Anterior extremity of left incisive foramen; (4) Anterior lateral extremity swelling of the rostrum corresponding to the premaxilla-maxilla suture; (5) Contact point between the maxillary arm and the rostrum; (6) Anterior extremity of the zygomatic arc; (7) Posterior extremity of anterior incisive foramen; (8) Anterior extremity of dental tooth row located on the left first upper molar; (9) Labial-side point inserted between left first and second upper molars; (10) Posterior foramen palatine; (11) Posterior extremity of dental tooth row; (12) Posterior extremity of palatine; (13) Anterior maximum point of curvature of the squamosal; (14) Foramen ovale; (15) Meeting point between the basiphenoid, basioccipital and tympanic bulla; (16) Mid-point of the basioccipital-basisphenoid suture; (17) Posterior tip of the external auditory meatus; (18) Mid-basioccipital point; (19) Anterior extremity of foramen magnum; (20) Internal flexion of the occipital condyle (PDF 138 kb)

Fig. S2

Proportion of small mammal species collected for historical (1959, 1960 and 1966; 284 specimens total) and recent (2007 to 2013; 332 specimens) field surveys conducted at sites MSH, MR and MY in Southern Quebec. All specimens are housed at the Redpath Museum, McGill University. Although these collection surveys are not an accurate estimate of actual species abundance, these data clearly show a shift from communities dominated by the deer mouse, P. maniculatus (in dark orange), to communities dominated by the white-footed mouse, P. leucopus (in dark blue) (PDF 79 kb)

Fig. S3

Mean monthly temperature from 1913 to 2016 at the Weather station of Drumondville (45.53 N, 72.29 W, Climate Identifier: 7022160). Temperature increased between 1913 and 2016 for all 12 months of the year (all P < 0.01). Source of data: Government of Canada, Environment and natural resources, https://www.canada.ca/en/services/environment.html (PDF 57 kb)

Table S1

This table contains all the specimen data: centroid size, PC shape axes and raw coordinates of the rotated configurations projected into tangent space, body mass (in gram) and head-and-body length (in mm). VM, QC and RM specimens are from the Redpath Museum, McGill University, and CMN specimens are from the Canadian Museum of Nature, Ottawa (XLSX 377 kb)

Table S2

Eigenvalue, percent variance explained and loadings of the first 11 PCA axes (XLSX 57 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Millien, V., Ledevin, R., Boué, C. et al. Rapid morphological divergence in two closely related and co-occurring species over the last 50 years. Evol Ecol 31, 847–864 (2017). https://doi.org/10.1007/s10682-017-9917-0

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10682-017-9917-0

Keywords

Navigation