Skip to main content
SpringerLink
Log in

Inter- and intraspecific diversity of ontogeny and fecundity patterns in relation to reproductive strategy choice in Myomorpha (Rodentia: Calomyscidae, Cricetidae, Muridae)

  • Original Paper
  • Published:
Mammal Research Aims and scope Submit manuscript

Abstract

Studying the life history of various organisms is essential for ecological and evolutionary inferences. However, publications regarding models of evolutionary shifts to either r- or K-reproductive strategies are scarce. Here, the combined original and previously published data on reproduction and development of Goodwin’s brush-tailed mouse (Calomyscus elburzensis), golden hamster (Mesocricetus auratus), and house mouse (Mus musculus) were compared. An adult male and female in estrous state (from each species) were coupled with each other for a night and embryos were harvested at embryonic days (E) 10–17 from pregnant females. The mean gestation period in Goodwin’s brush-tailed mouse was 31.5 ± 2.1 days; growth was rapid at the first half of this period and after that it was reduced by half. During the postnatal period, growth was rapid up to weaning, but after day 35, the rate of growth decreased abruptly. Growth rate of head and body length was very rapid prior to weaning (PN35) in comparison with weight but the rates of the two characters were inversed following weaning. Totally, weight gain was more dynamic in rate, as compared with head and body length, up to adultness. For golden hamster and house mouse, gestation period was 15.6 ± 0.8 and 20.8 ± 0.8 days, respectively. Growth was slow during approximately the first half of the gestation period in both species but increased during the second half. During postnatal period in golden hamster, growth rate of head and body length was rapid both before and after weaning as compared with that of weight. However, head and body length showed a stable rate of growth before and after weaning (around PN15), but for body weight, the growth rate was slightly faster after weaning. Similarly, changes in head and body length in house mouse were rapid both before and after weaning (PN16) as compared with that of weight. Since approximately two-fold increases were observed in the growth rates of weight and head and body length in the second stage of postnatal development (PN16-adult) compared with the rates during the first stage (PN0-PN16), both showed dynamic changes during the postnatal development in this species. Typically, r-strategic house mouse appeared to be more similar in early morphological development to comparatively K-strategic Goodwin’s brush-tailed mouse, than to comparatively r-strategic golden hamster. Nevertheless, growth rate and pattern were different in the three species after birth. Hence, results showed that peculiarities of association between an ontogenetic pattern and a tendency in reproductive strategy can differ in diverse groups of myomorph rodents.

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

Access this article

Log in via an institution

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

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

References

  • Angelini F, Ghiara G (1984) Reproductive modes and strategies in vertebrate evolution. Ital J Zool 51(1–2):121–203

    Google Scholar 

  • Asdell SA (1946) Patterns of mammalian reproduction. Comstock Publishing Co.

  • Banks RE, Sharp JM, Doss SD, Vanderford DA (2010) Exotic small mammal care and husbandry. John Wiley & Sons, pp 103–114

  • Bastir M, Rosas A (2004) Facial heights: evolutionary relevance of postnatal ontogeny for facial orientation and skull morphology in humans and chimpanzees. J Hum Evol 47:359–381

    PubMed  Google Scholar 

  • Bronson FH (1979) The reproductive ecology of the house mouse. Q Rev Biol 54(3):265–299

    CAS  PubMed  Google Scholar 

  • Bulygina E, Mitteroecker P, Aiello L (2006) Ontogeny of facial dimorphism and patterns of individual development within one human population. Am J Phys Anthropol 131:432–443

    CAS  PubMed  Google Scholar 

  • Cardini A, O’Higgins P (2005) Postnatal ontogeny of the mandible and ventral cranium in Marmota species (Rodentia, Sciuridae): allometry and phylogeny. Zoomorphology 124:189–203

    Google Scholar 

  • Champlin AK, Dorr DL, Gates AH (1973) Determining the stage of the estrous cycle in the mouse by the appearance of the vagina. Biol Reprod 8(4):491–494

    CAS  PubMed  Google Scholar 

  • Creighton GK, Strauss RE (1986) Comparative patterns of growth and development in cricetine rodents and the evolution of ontogeny. Evolution 40:94–106

    PubMed  Google Scholar 

  • Cubo J, Ventura J, Casinos A (2006) A heterochronic interpretation of the origin of digging adaptations in the northern water vole, Arvicola terrestris (Rodentia: Arvicolidae). Biol J Linn Soc 87:381–391

    Google Scholar 

  • Denys C, Taylor PJ, Aplin KP (2017) Family Muridae (true mice and rats, gerbils and relatives). In: Wilson DE, Lacher TE Jr, Mittermerier RA (eds) Handbook of mammals of the world, Rodents II, vol 7. Lynx Editions, Barcelona, Spain, pp 536–884

    Google Scholar 

  • Dobson FS, Oli MK (2008) The life histories of orders of mammals: fast and slow breeding. Curr Sci 95(7):862–865

    Google Scholar 

  • Dobzhansky T (1950) Evolution in the tropics. Am Sci 38(2):209–221

    Google Scholar 

  • Eilam D (1997) Postnatal development of body architecture and gait in several rodent species. JEB 200:1339–1350

    CAS  Google Scholar 

  • Fadda C, Leirs H (2009) The role of growth stop as a morphogenetic factor in Mastomys natalensis (Rodentia: Muridae). Biol J Linn Soc 97:791–800

    Google Scholar 

  • Feoktistova NY, Meschersky IG, Surov AV, Bogomolov PL, Tovpinetz NN, Poplavskaya NS (2016) Genetic structure of urban population of the common hamster (Cricetus cricetus). Genetika 52(2):221–230 [In Russian with English summary]

    PubMed  Google Scholar 

  • Fisher RA (1930) The genetical theory of natural selection. Oxford. xiv + 272 p.

  • Gattermann R, Fritzsche P, Nwumann K, Al-Hussein L, Kayer A, Abiad M, Yakti R (2001) Notes on the current distribution and the ecology of wild golden hamsters (Mesocricetus auratus). ZSL 254:359–365

    Google Scholar 

  • Hamidi K, Darvish J, Matin MM, Malikov VG (2015) A field behavioral study of Calomyscus elburzensis (Rodentia: Calomyscidae); the effects of sexual and seasonal variations in the trapping success. Acta Zool Bulg 67:521–528

    Google Scholar 

  • Hamidi K, Darvish J, Matin MM (2017a) Ecological survey of two Calomyscidae species; Goodwin’s brush-tailed mouse and Hotson’s brush-tailed mouse (Rodentia) in the eastern parts of Iran. Acta Ecol Sin 37(2):105–114

    Google Scholar 

  • Hamidi K, Darvish J, Matin MM, Javanmard AS, Kilpatrick CW (2017b) Tooth morphogenesis and FGF4 expression during development of molar tooth in three muroid rodents: Calomyscus elburzensis (Calomyscidae), Mesocricetus auratus (Cricetidae) and Mus musculus (Muridae). Anat Rec 300(12):2138–2149

    CAS  Google Scholar 

  • Hamidi K, Darvish J, Matin MM (2018) Potential use of brush-tailed mice for evolutionary developmental biology studies: Calomyscus elburzensis an appropriate rodent species. JWB 2(2):6–14

    Google Scholar 

  • Hayssen V, Tienhoven A, Tienhoven A (1993) Asdell’s patterns of mammalian reproduction: a compendium of species-specific data. Revised Edition, Cornell University Press

  • Kaufmann MH (2008) The atlas of mouse development. London: Elsevier Academic Press

  • Kaufmann MH, Bard JBL (1999) The anatomical basis of mouse development. San Diego: Academic Press

  • Kilpatrick CW (2017) Family Calomyscidae (brush-tailed mice). In: Wilson DE, Lacher TE Jr, Mittermerier RA (eds) Handbook of mammals of the world, Rodents II, vol 7. Lynx Editions, Barcelona, Spain, pp 144–155

    Google Scholar 

  • Kotenkova EV, Priluzskaya LI (1994) Ecological characteristics of species, in: The house mouse; origin, distribution, systematics, behavior. 267 p. [In Russian, Synopsis in English].

  • Krebs CJ, Myers JH (1974) Population cycles in small mammals, in: Advances in ecological research, Vol. 8, Academic Press, pp. 267–399

  • Laurie EM (1946) The reproduction of the house-mouse (Mus musculus) living in different environments. Proc R Soc Lond B 133(872):248–281

    CAS  PubMed  Google Scholar 

  • Lay MD (1967) A study of the mammals of Iran resulting from the street expedition. Fieldiana Zoology, No. 54, 282 p

  • MacArthur RH, Wilson EO (1967) The theory of island biogeography. Princeton University Press

  • Magomedov MR, Omarov KZ (1995) Feeding behavior and the state of populations of cis-caucasian hamster (Mesocricetus raddei avaricus) in mountain agroecosystems. Zool Zh 74(3):123–133 [In Russian with English summary]

    Google Scholar 

  • Malikov VG, Meyer MN (1990) The characters of breeding and postnatal ontogeny of mountain and plain voles (Rodentia, Arvicolinae) in connection with their distribution. USSR Academy of Sciences. Proc Zool Inst 225:21–33 [In Russian with English summary]

    Google Scholar 

  • Marcondes FK, Bianchi FJ, Tanno AP (2002) Determination of the estrous cycle phases of rats: some helpful considerations. Braz J Biol 62(4A):609–614

    CAS  PubMed  Google Scholar 

  • Marroig G (2007) When size makes a difference: allometry, life-history and morphological evolution of capuchins (Cebus) and squirrels (Saimiri) monkeys (Cebinae, Platyrrhini). BMC Evol Biol 7(1):20

    PubMed  PubMed Central  Google Scholar 

  • Meyer MN, Malikov VG (1996) Peculiarities of biology and postnatal ontogenesis in Calomyscus (Cricetinae, Calomyscus). Proc. Zool. Inst., RAS 75(12):1852–1862 [In Russian with English summary]

    Google Scholar 

  • Monteiro LR, Cavalcanti MJ, Sommer HJS (1997) Comparative ontogenetic shape change in the skull of Caiman species (Crocodylia, Alligatoridae). J Morphol 231:53–62

    CAS  PubMed  Google Scholar 

  • Musser GG, Carleton MD (2005) Subfamily Murinae. In: Wilson DE, Reeder DM (eds) Mammal species of the world: a taxonomic and geographic reference, vol 2, Third edn. The Johns Hopkins University Press, Baltimore 480 pp

    Google Scholar 

  • O’Higgins P, Chadfield P, Jones N (2001) Facial growth and the ontogeny of morphological variation within and between the primates Cebus apella and Cercocebus torquatus. J Zool 254:337–357

    Google Scholar 

  • Olenev GV (2002) Alternative types of ontogeny in cyclomorphic rodents and their role in population dynamics: an ecological analysis. RUSS J ECOL 33 (5): 321-330. Translated from Ekologiya 5: 341–350

  • Olio RL, Favaron PO, Lobo LM, de Lima Will SEA, Santos AC, Viana DC, de Oliveira MF, Miglino MA (2014) Characterization of embryonic and fetal development of Necromys lasiurus (Rodentia, Cricetidae). J Cytol Histol 5:242

    Google Scholar 

  • Pianka ER (1970) On r- and K-selection. Am Nat 104(940):592–597

    Google Scholar 

  • Pianka ER (2000) Evolutionary ecology, 6th edition Benjamin-Cummings, Addison-Wesley Longman, San Francisco

  • Pocock MJ, Searle JB, White PC (2004) Adaptations of animals to commensal habitats: population dynamics of house mice Mus musculus domesticus on farms. J Animal Ecol 73(5):878–888

    Google Scholar 

  • Reznick D, Bryant MJ, Bashey F (2002) r- and K-selection revisited: the role of population regulation in life-history evolution. Ecology 83(6):1509–1520

    Google Scholar 

  • Roff DA (2002) Life history evolution, 2nd edition Sunderland: Sinauer Associates

  • Rugh R (1968) The mouse: its reproduction and development. Minneapolis: Burgess. 430 p

  • Sánchez-Villagra MR (2010) Developmental palaeontology in synapsids: the fossil record of ontogeny in mammals and their closest relatives. Proc. R. Soc. Lond. [Biol. Sci.] 277:1139–1147

    Google Scholar 

  • Sardi ML, Ventrice F, Ramírez Rozzi F (2007) Allometries throughout the late prenatal and early postnatal human craniofacial ontogeny. Anat Rec 290(9):1112–1120

    Google Scholar 

  • Singleton M (2002) Patterns of cranial shape variation in the Papionini (Primates: Cercopithecinae). J Hum Evol 42:547–578

    PubMed  Google Scholar 

  • Stearns SC (2000) Life history evolution: successes, limitations, and prospects. Naturwissenschaften 87:476–486

    CAS  PubMed  Google Scholar 

  • Suckow MA, Danneman P, Brayton C (2000) The laboratory mouse (laboratory animal pocket reference series). CRC press LLC, USA, 167 p

  • Surov AV, Poplavskaya NA, Bogomolov PL, Kropotkina MV, Tovpinets NN, Katsman EA, Feoktistova NY (2015) Sin urbanization of common hamster (Cricetus cricetus l., 1758). Russ. J Biol Invasions 4:105–117 [In Russian]

    Google Scholar 

  • Valentine H, Daugherity EK, Singh B, Maurer KJ (2012) The experimental use of Syrian hamsters, in: Suckow MA, Stevens KA, Wilson RP (Eds.), The laboratory rabbit, guinea pig, hamster and other rodents, 1st edition, Elsevier Academic Press, Amsterdam

    Google Scholar 

  • Vinicius L (2005) Human encephalization and developmental timing. J Hum Evol 49(6):762–776

    PubMed  Google Scholar 

  • Volf J, Volf P (2003) Der Mausartige Zwerghamster (Calomyscus bailwardi Thomas, 1905) und seine Zucht in Menschenobhut [the mouse-like hamster (Calomyscus bailwardi Thomas, 1905) and its captive breed]. Zool Gart 73(3):147–157

    Google Scholar 

  • Weber EM, Olsson IA (2008) Maternal behavior in Mus musculus sp.: an ethological review. Appl Anim Behav Sci 114(1–2):1–22

    Google Scholar 

  • Weston EM (2003) Evolution of ontogeny in the hippopotamus skull: using allometry to dissect developmental change. Biol J Linn Soc 80(4):625–638

    Google Scholar 

  • Wilson LAB (2011) Comparison of prenatal and postnatal ontogeny: cranial allometry in the African striped mouse (Rhabdomys pumilio). J Mammal 92(2):407–420

    Google Scholar 

  • Wilson LAB, Sánchez-Villagra MR (2010) Diversity trends and their ontogenetic basis: an exploration of allometric disparity in rodents. Proc R Soc Lond [Biol Sci] 277:1227–1234

    Google Scholar 

  • Wilson LA, Macleod N, Humphrey LT (2008) Morphometric criteria for sexing juvenile human skeletons using the ilium. J Forensic Sci 53:269–278

    PubMed  Google Scholar 

  • Yigit N, Kryštufek B (2008) Mesocricetus auratus, golden hamster. The IUCN red list of threatened species. Available from: http://www.iucnredlist.org/ [Accessed 17 May 2019]

  • Zelditch ML, Lundrigan BL, Sheets D, Garland JR (2003a) Do precocial mammals develop at a faster rate? A comparison of rates of skull development in Sigmodon fuliviventer and Mus musculus domesticus. J. Evol Biol 16:708–720

    PubMed  Google Scholar 

  • Zelditch ML, Sheets HD, Fink WL (2003b) The ontogenetic dynamics of shape disparity. Paleobiology 29:139–156

    Google Scholar 

  • Zoccolan D, Oertelta N, DiCarlob JJ, Coxa DD (2009) A rodent model for the study of invariant visual object recognition. PNAS 106(21):8748–8753

    CAS  PubMed  Google Scholar 

  • Zollikofer CP, de León MS (2010) The evolution of hominin ontogenies, in: Seminars in cell and developmental biology 21 (4): 441–452. Academic Press

Download references

Acknowledgments

The authors wish to express their sincere thanks to H. Mozaffari and A. Hamidi for their help in field studies and S. Mohammadi for providing valuable comments on an earlier draft of the manuscript. We are also grateful to Prof. C. W. Kilpatrick for providing invaluable feedback on multiple versions of this manuscript and for his numerous supports and contributions to our understanding of the evolution of brush-tailed mice. We thank the anonymous reviewers for their valuable comments and scientific advice which greatly improved the content.

Funding

This research was funded by Ferdowsi University of Mashhad (FUM) (Grant number 3/29121), also was partially supported by the Russian Foundation of Basic Research (project 19-04-00557-а), and ZIN RAS Theriology Laboratory’s Governmental Task (ZIN RAS number AAAA-A17-117022810195-3).

Author information

Authors and Affiliations

  1. Department of Biology, Faculty of Science, Ferdowsi University of Mashhad, Mashhad, Iran

    Kordiyeh Hamidi, Maryam M. Matin & Jamshid Darvish

  2. Novel Diagnostics and Therapeutics Research Group, Institute of Biotechnology, Ferdowsi University of Mashhad, Mashhad, Iran

    Maryam M. Matin

  3. Research Group of Rodentology, Institute of Applied Zoology, Ferdowsi University of Mashhad, Mashhad, Iran

    Jamshid Darvish

  4. Laboratory of Theriology, Zoological Institute of the Russian Academy of Sciences 1, Universitetskaya emb, Saint-Petersburg, Russia

    Vladimir G. Malikov

Author notes

  1. Jamshid Darvish is deceased. This paper is dedicated to his memory.

    • Jamshid Darvish
Authors
  1. Kordiyeh Hamidi
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Maryam M. Matin
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Jamshid Darvish
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Vladimir G. Malikov
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

KH designed the study, collected the samples and conducted laboratory procedures, wrote the manuscript, and provided the figures. MMM conducted the methodology and inferences and also had valuable discussions about the content. JD conceived and designed the study and also stimulated the interest in brush-tailed mice study. VGM had valuable discussions about the content. All authors contributed in proofreading.

Corresponding author

Correspondence to Maryam M. Matin.

Ethics declarations

Conflict of interest

The authors declare that they have no conflict of interest.

Ethical approval

All applicable international, national, and/or institutional guidelines for the care and use of animals were followed. All procedures performed in studies involving animals were in accordance with the ethical standards of Ferdowsi University of Mashhad.

Additional information

Communicated by: Shuiqiao Yuan

Publisher’s note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Hamidi, K., Matin, M.M., Darvish, J. et al. Inter- and intraspecific diversity of ontogeny and fecundity patterns in relation to reproductive strategy choice in Myomorpha (Rodentia: Calomyscidae, Cricetidae, Muridae). Mamm Res 65, 277–288 (2020). https://doi.org/10.1007/s13364-019-00460-3

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s13364-019-00460-3

Keywords

Search

Navigation