Adaptive divergence in reproductive seasonality and underlying physiological features fit Rattus norvegicus to live as opportunistic breeders

Abstract

How organisms respond to complex environments is one of the unsolved problems in ecology. Life history patterns of a species provide essential information on how different populations may respond and adapt to environmental changes. Compared to typical seasonal breeders, which have limited distributions, the worldwide distribution of brown rats (Rattus norvegicus) across highly complex and divergent habitats suggests they exhibit exceptional adaptiveness. However, the difference in physiological mechanisms by which brown rats respond and adapt to markedly different environments is seldom investigated. Here, we reveal a significant divergence in reproductive seasonality and environmental responses between two brown rat subspecies: one subspecies, R. n. caraco, lives in the temperate zone, and another subspecies, R. n. norvegicus, lives in the subtropical region. Although R. n. caraco displayed a significantly higher reproductive seasonality than R. n. norvegicus, both subspecies adapted to sub-optimal breeding conditions mainly by regulating the seminal vesicle rather than testis development. Especially in responding to severe winter conditions in high-latitude regions, bodyweight-dependent recovery of testicular development in adults enables R. n. caraco to initiate reproduction more rapidly when conditions are suited. These findings elucidate a regulatory process of how brown rats live as opportunistic breeders by benefiting from enhanced semen production.

Keywords

adaptation / brown rat / gonadal development / photoperiod / temperature / testis

References

[1] Bunn DW, Vassilopoulos AI (1993). Using group seasonal indices in multi-item short-term forecasting. International Journal of Forecasting 9, 517-526.

[2] Clarke JR (1985). The reproductive biology of the bank vole (Clethrionomys glareolus) and the wood mouse (Apodemus sylvaticus). Symposia of the Zoological Society of London 55, 33-59.

[3] Clermont Y (1972). Kinetics of spermatogenesis in mammals: Seminiferous epithelium cycle and spermatogonial renewal. Physiological Reviews 52, 198-236.

[4] Clermont Y, Harvey SC (1965). Duration of the cycle of the seminiferous epithelium of normal, hypophysectomized and hypophysectomized-hormone treated albino rats. Endocrinology 76, 80-89.

[5] Dadhich RK, Barrionuevo FJ, Real FM et al. (2013). Identification of live germ-cell desquamation as a major mechanism of seasonal testis regression in mammals: A study in the Iberian mole (Talpa occidentalis). Biology of Reproduction 88, 101.

[6] Dadhich RK, Real FM, Zurita F, Barrionuevo FJ, Burgos M, Jimenez R (2010). Role of apoptosis and cell proliferation in the testicular dynamics of seasonal breeding mammals: A study in the Iberian mole, Talpa occidentalis. Biology of Reproduction 83, 83-91.

[7] Dobson FS, Murie JO (1987). Interpretation of intraspecific life history patterns: Evidence from Columbian ground squirrels. American Naturalist 129, 382-397.

[8] Dobson FS, Oli MK (2007). Fast and slow life histories of mammals. Ecoscience 14, 292-299.

[9] Du A, Li L, Jiao Z, Zhu G, Peng T, Li H (2021). Protein expression pattern of calcium-responsive transactivator in early postnatal and adult testes. Histochemistry and Cell Biology 155, 491-502.

[10] Durairajanayagam D, Agarwal A, Ong C (2015). Causes, effects and molecular mechanisms of testicular heat stress. Reproductive Biomedicine Online 30, 14-27.

[11] Ellison PT (2003). Energetics and reproductive effort. American Journal of Human Biology 15, 342-51.

[12] English S, Bonsall MB (2019). Physiological dynamics, reproduction-maintenance allocations, and life history evolution. Ecology and Evolution 9, 9312-9323.

[13] Flatt T, Heyland A (2011). Mechanisms of Life History Evolution: The Genetics and Physiology of Life History Traits and Trade-offs. Oxford University Press, Oxford, UK.

[14] Furuta I, Porkka-Heiskanen T, Scarbrough K, Tapanainen J, Turek FW, Hsueh AJ (1994). Photoperiod regulates testis cell apoptosis in Djungarian hamsters. Biology of Reproduction 51, 1315-1321.

[15] Jiménez R, Burgos M, Sánchez A, Delaguardia R (1990). The reproductive cycle of Talpa occidentalis in the southeastern Iberian Peninsula. Acta Theriologica 35, 165-169.

[16] Kim B, Park K, Rhee K (2013). Heat stress response of male germ cells. Cellular and Molecular Life Sciences 70, 2623-36.

[17] Lane JE, Boutin S, Speakman JR, Humphries MM (2010). Energetic costs of male reproduction in a scramble competition mating system. Journal of Animal Ecology 79, 27-34.

[18] Macdonald DW, Mathews F, Berdoy M (1999). The behaviour and ecology of Rattus norvegicus: From opportunism to kamikaze tendencies. In: Singleton GR, Leirs H, Hinds LA, Zhang Z, eds. Ecologically-Based Rodent Management. Australian Centre for International Agricultural Research, Australia, pp. 49-80.

[19] Massoud D, Barrionuevo FJ, Ortega E, Burgos M, Jimenez R (2014). The testis of greater white-toothed shrew Crocidura russula in Southern European populations: A case of adaptive lack of seasonal involution? Journal of Experimental Zoology Part B: Molecular and Developmental Evolution 322, 304-315.

[20] Massoud D, Lao-Perez M, Ortega E, Burgos M, Jimenez R, Barrionuevo FJ (2021). Divergent seasonal reproductive patterns in syntopic populations of two murine species in southern Spain, Mus spretus and Apodemus sylvaticus. Animals 11, 243.

[21] McGuire B, Pizzuto T, Bemis WE, Getz LL (2006). General ecology of a rural population of Norway rats (Rattus norvegicus) based on intensive live trapping. The American Midland Naturalist 155, 221-236.

[22] Nau R (2020). Statistical forecasting: notes on regression and time series analysis. Available from URL: https://people.duke.edu/~rnau/411home.htm.

[23] Neaves WB (1973). Changes in testicular leydig cells and in plasma testosterone levels among seasonally breeding rock hyrax. Biology of Reproduction 8, 451-66.

[24] Picut CA, Dixon D, Simons ML, Stump DG, Parker GA, Remick AK (2015a). Postnatal ovary development in the rat: Morphologic study and correlation of morphology to neuroendocrine parameters. Toxicologic Pathology 43, 343-53

[25] Picut CA, Remick AK, De Rijk EP, Simons ML, Stump DG, Parker GA (2015b). Postnatal development of the testis in the rat: morphologic study and correlation of morphology to neuroendocrine parameters. Toxicologic Pathology 43, 326-42.

[26] Pontzer H (2015). Energy expenditure in humans and other primates: A new synthesis. Annual Review of Anthropology 44, 169-187.

[27] Pontzer H (2018). Energy constraint as a novel mechanism linking exercise and health. Physiology (Bethesda) 33, 384-393.

[28] Puckett EE, Munshi-South J (2019). Brown rat demography reveals pre-commensal structure in eastern Asia before expansion into Southeast Asia. Genome Research 29, 762-770.

[29] Rizzoto G, Sekhar D, Thundathil JC, Chelikani PK, Kastelic JP (2019). Calorie restriction modulates reproductive development and energy balance in pre-pubertal male rats. Nutrients 11, 1993.

[30] Schon J, Goritz F, Streich J, Blottner S (2004). Histological organization of roe deer testis throughout the seasonal cycle: Variable and constant components of tubular and interstitial compartment. Anatomy and Embryology 208, 151-159.

[31] Sinha Hikim AP, Bartke A, Russell LD (1988). The seasonal breeding hamster as a model to study structure-function relationships in the testis. Tissue & Cell 20, 63-78.

[32] Song Y, Lan Z, Kohn MH (2014). Mitochondrial DNA phylogeography of the Norway rat. PLoS ONE 9, e88425.

[33] Tait AJ, Johnson E (1982). Spermatogenesis in the grey squirrel (Sciurus carolinensis) and changes during sexual regression. Reproduction Fertility and Development 65, 53-8.

[34] Tian L, Li HC, Li JP et al. (2020). A preliminary study on the photorefractoriness in male Brandt's voles Lasiopodomys brandtii. Plant Protection 46, 61-66. (In Chinese.)

[35] Vadell MV, Villafañe IEG, Cavia R (2014). Are life-history strategies of Norway rats (Rattus norvegicus) and house mice (Mus musculus) dependent on environmental characteristics? Wildlife Research 41, 172-184.

[36] Van Rosmalen L, Hut RA (2021). Food and temperature change photoperiodic responses in two vole species. The Journal of Experimental Biology 224, jeb243030.

[37] Viger RS, Mertineit C, Trasler JM, Nemer M (1998). Transcription factor GATA-4 is expressed in a sexually dimorphic pattern during mouse gonadal development and is a potent activator of the Müllerian inhibiting substance promoter. Development 125, 2665-2675.

[38] Virtanen P, Gommers R, Oliphant TE et al. (2020). SciPy 1.0: Fundamental algorithms for scientific computing in Python. Nature Methods 17, 261-272.

[39] Wang DW, Cong L, Yue LF et al. (2011). Seasonal variation in population characteristics and management implications for brown rats (Rattus norvegicus) within their native range in Harbin, China. Journal of Pest Science 84, 409-418.

[40] Wang DW, Li N, Tian L et al. (2019). Dynamic expressions of hypothalamic genes regulate seasonal breeding in a natural rodent population. Molecular Ecology 28, 3508-3522.

[41] Williams CT, Klaassen M, Barnes BM et al. (2017). Seasonal reproductive tactics: Annual timing and the capital-to-income breeder continuum. Philosophical Transactions of the Royal Society B: Biological Sciences 372, 20160250.

[42] Wilson D, Reeder DM (2005). Mammal Species of the World: A Taxonomic and Geographic Reference, 3rd edn. Johns Hopkins University Press, Baltimore, MD.

[43] Withycombe R (1989). Forecasting with combined seasonal indices. International Journal of Forecasting 5, 547-552.

[44] Wu D (1982). On subspecific differentiation of brown rat (Rattus norvegicus Berkenhout) in China. Acta Theriologica Sinica 2, 107-112. (In Chinese.)

[45] Yao DD, Sui JJ, Feng ZY (2016). The population age and reproductive characteristics of Rattus norvegicus in Zhanjiang city. Chinese Journal of Vector Biology and Control 27, 454-458. (In Chinese.)

[46] Young KA, Zirkin BR, Nelson RJ (1999). Short photoperiods evoke testicular apoptosis in white-footed mice (Peromyscus leucopus). Endocrinology 140, 3133-3139. (In Chinese.)

[47] Zeng L, Ming C, Li Y et al. (2018). Out of Southern East Asia of the brown rat revealed by large-scale genome sequencing. Molecular Biology and Evolution 35, 149-158.

RIGHTS & PERMISSIONS

2024 The Author(s). Integrative Zoology published by International Society of Zoological Sciences, Institute of Zoology/Chinese Academy of Sciences and John Wiley & Sons Australia, Ltd.