Monogamy or monogamish? Re-examining monogamy in Peromyscus californicus

Authors

Keywords:

California deermouse, genetic monogamy, monogamy, paternity, Peromyscus californicus

Abstract

California mice have been widely recognized as one of the few examples of ‘true’ genetic monogamy in mammals and are one of only four mammalian species considered to be both genetically and socially monogamous. The mating system of this species, first described by David O. Ribble (1991), was initially investigated in a single population by integrating both behavioral data and DNA fingerprinting to classify P. californicus as monogamous. Here, we investigated the parentage of field sampled litters of California mice across 4 populations using both classic field methods and modern microsatellite analyses. We putatively identified male-female mouse pairs in the field using capture localities and transfer of fluorescent pigment between individuals. We then used microsatellite loci to genotype pregnant adult females, their embryos, and the adult males identified in the field as the partners of those females. We identified occurrences of extra-pair paternity in 3 out of the 4 populations of California mice, calling in to question the designation of this species as genetically monogamous (Figure 1 and Table 1). We suggest a careful re-examination of the mating system of this species using modern molecular methods to analyze a greater number of samples representing multiple sampling localities. Future studies of this species should prove particularly informative regarding the correlates of extra-pair mating and, hence, the adaptive bases for the maintenance of male-female pair bonds in the absence of true genetic monogamy.

References

BATEMAN, A. J. 1948. Intra-sexual selection in Drosophila. Heredity 2:349–368.

BESTER-MEREDITH, J. K., L. J. YOUNG, AND C. A. MARLER. 1999. Species differences in paternal behavior and aggression in Peromyscus and their associations with vasopressin immunoreactivity and receptors. Hormones and Behavior 36:25–38.

BOTERO, C. A., AND D. R. RUBENSTEIN. 2012. Fluctuating Environments, Sexual Selection and the Evolution of Flexible Mate Choice in Birds. Plos One 7, e32311.

BROTHERTON, P. N. M., ET AL. 1997. Genetic and behavioural evidence of monogamy in a mammal, Kirk’s dik-dik (Madoqua kirkii). Proceedings of the Royal Society B: Biological Sciences 264: 675–681.

BROUWER, L., AND S. C. GRIFFITH. 2019. Extraâ€pair paternity in birds. Molecular Ecology 28: 4864–4882.

CAMPI, K. L., C. E. JAMESON, AND B. C. TRAINOR. 2013. Sexual dimorphism in the brain of the monogamous California mouse (Peromyscus californicus). Brain Behavior Evolution 81:236–249.

CLUTTON-BROCK, T. H. 1989. Mammalian mating systems. Proceedings of the Royal Society B: Biological Sciences 236:339–372.

COHAS, A., AND D. ALLAINÉ. 2009. Social structure influences extra-pair paternity in socially monogamous mammals. Biology Letters 5: 313–316.

DOLOTOVSKAYA, S., C. ROOS, AND E. W. HEYMANN. 2020. Genetic monogamy and mate choice in a pair-living primate. Scientific Reports 10, 20328.

ELSTON, R. C., AND R. FORTHOFER. 1977. Testing for Hardy-Weinberg Equilibrium in Small Samples. Biometrics 33: 536.

EMLEN, S. T., AND L. W. ORING. 1977. Ecology, Sexual Selection, and the Evolution of Mating Systems. Science 197: 215–223.

FIETZ, J., ET AL. 2000. High rates of extra-pair young in the pair-living fat-tailed dwarf lemur, Cheirogaleus medius. Behavioral Ecology and Sociobiology 49:8–17.

FLANAGAN, S. P., AND A. G. JONES. 2019. The future of parentage analysis: from microsatellites to SNPs and beyond. Molecular Ecology 28:544–567.

FOLTZ, D. W. 1981. Genetic evidence for long-term monogamy in a small rodent, Peromyscus polionotus. The American Naturalist 117:665–675.

FROMHAGE, L., M. A. ELGAR, AND J. M. SCHNEIDER. 2005. Faithful without care: the evolution of monogyny. Evolution 59:1400–1405.

GIRMAN, D. J., ET AL. 1997. A molecular genetic analysis of social structure, dispersal, and interpack relationships of the African wild dog (Lycaon pictus). Behavioral Ecology and Sociobiology 40:187–198.

GOOSSENS, B., ET AL. 1998. Extra-pair paternity in the monogamous Alpine marmot revealed by nuclear DNA microsatellite analysis. Behavioral Ecology and Sociobiology 43:281–288.

GRIFFITH, S. C., I. F. P. OWENS, AND K. A. THUMAN. 2008. Extra pair paternity in birds: a review of interspecific variation and adaptive function: extra pair paternity in birds. Molecular Ecology 11:2195–2212.

GRINNELL, J., AND R. ORR. 1934. Systematic review of the californicus group of the rodent genus Peromyscus. Journal of Mammalogy 15:210–222.

GRINNELL, J., AND H. A. SWARTH. 1913. An account of the birds and mammals of the San Jacinto area of southern California with remarks upon the behavior of geographic races on the margins of their habitats. University of California Publications in Zoology 10:197–406.

GUBERNICK, D. J., AND J. C. NORDBY. 1993. Mechanisms of sexual fidelity in the monogamous California mouse, Peromyscus californicus. Behavioral Ecology and Sociobiology 32(3):211-219

HENNESSY, C. A., J. DUBACH, AND S. D. GEHRT. 2012. Long-term pair bonding and genetic evidence for monogamy among urban coyotes (Canis latrans). Journal of Mammalogy 93:732–742.

HUCK, M., ET AL. 2014. Correlates of genetic monogamy in socially monogamous mammals: insights from Azara’s owl monkeys. Proceedings of the Royal Society B: Biological Sciences 281:20140195–20140195.

JAMESON JR, E. W., AND H. J. PEETERS. 2004. Mammals of California, Revised Edition. ed, California Natural History Guides. University of California Press. Berkeley and Los Angeles, U.S.A.

JAŠAREVIĆ, E., ET AL. 2013. Evolution of monogamy, paternal investment, and female life history in Peromyscus. Journal of Comparative Psychology 127:91–102.

JOHNSON, S. A., ET AL. 2015. Disruption of Parenting Behaviors in California Mice, a Monogamous Rodent Species, by Endocrine Disrupting Chemicals. PLoS ONE 10, e0126284.

JONES, A.G., ET AL. 2010. A practical guide to methods of parentage analysis. Molecular Ecology Resources 10:6–30.

KALCOUNIS-RUEPPELL, M. C., AND D. O. RIBBLE. 2007. A Phylogenetic Analysis of the Socioecology of Neotomine-Peromyscine Rodents. Pp. 68-85, in Rodent Societies: An Ecological and Evolutionary Perspective. University of Chicago Press. Chicago, U.S.A.

KALCOUNIS-RÜPPELL, M. C., A. PATRICK, AND J. A. MILLAR. 2001. Effect of Fluorescent Powder Marking of Females on Mate Choice by Male White-Footed Mice (Peromyscus leucopus). The American Midland Naturalist 146:429–433.

KALINOWSKI, S. T., M. L. TAPER, AND T. C. MARSHALL. 2007. Revising how the computer program cervus accommodates genotyping error increases success in paternity assignment: Cervus Likelihood Model. Molecular Ecology 16:1099–1106.

KAPPELER, P. M. 2019. A framework for studying social complexity. Behavior Ecology and Sociobiology 73:13.

KEARSE, M., ET AL. 2012. Geneious Basic: an integrated and extendable desktop software platform for the organization and analysis of sequence data. Bioinformatics 28:1647–1649.

KING, J. A. 1968. Biology of Peromyscus (Rodentia). American Society of Mammalogists. Stillwater, U.S.A.

KLEIMAN, D. G. 1977. Monogamy in Mammals. The Quarterly Review of Biology 52:39–69.

LAMBERT, C. T., A. C. SABOL, AND N. G. SOLOMON. 2018. Genetic monogamy in socially monogamous mammals is primarily predicted by multiple life history factors: a meta-analysis. Frontiers in Ecology and Evolution 6:139.

LUKAS, D., AND T. H. CLUTTON-BROCK. 2012. Cooperative breeding and monogamy in mammalian societies. Proceedings of the Royal Society B: Biological Sciences 279:2151–2156.

LUKAS, D., AND T. H. CLUTTON-BROCK. 2013. The Evolution of Social Monogamy in Mammals. Science 341:526–530.

MAYER, C., AND G. PASINELLI. 2013. New support for an old hypothesis: density affects extraâ€pair paternity. Ecology and Evolution 3:694–705.

MELÉNDEZ-ROSA, J., K. BI, AND E. A. LACEY. 2020. Mating system is correlated with immunogenetic diversity in sympatric species of Peromyscine mice. Plos One 15,

MELÉNDEZâ€ROSA, J., K. BI, AND E. A. LACEY. 2019. Differential gene expression in relation to mating system in Peromyscine rodents. Ecology and Evolution 9: 5975–5990.

PETRIC, R., M. C. KALCOUNIS-RUEPPELL, AND C. A. MARLER. 2021. Testosterone induces a conditioned place preference to the nest of a monogamous mouse under field conditions (preprint). eLife 11:e65820.

PRINCE, K.L., T. C. GLENN, AND M. J. DEWEY. 2002. Cross-species amplification among peromyscines of new microsatellite DNA loci from the oldfield mouse (Peromyscus polionotus subgriseus). Molecular Ecology Notes 2:133–136.

PULTORAK, J. D., ET AL. 2015. Male fidelity expressed through rapid testosterone suppression of ultrasonic vocalizations to novel females in the monogamous California mouse. Hormones and Behavior 70:47–56.

RAYMOND, M., AND F. ROUSSET. 1995. GENEPOP (Version 1.2): Population Genetics Software for Exact Tests and Ecumenicism. Journal of Heredity 86:248–249.

RIBBLE, D. O. 2003. The evolution of social and reproductive monogamy in Peromyscus : evidence from Peromyscus californicus (the California mouse). Pp 81-92, in Monogamy: Mating Strategies and Partnerships in Birds, Humans, and Other Mammals (Reichard, U. H., and Boesch, C., eds.). Cambridge University Press. Cambridge, U.K.

RIBBLE, D. O. 1991. The monogamous mating system of Peromyscus californicus as revealed by DNA fingerprinting. Behavioral Ecology and Sociobiology 29:161–166.

RIBBLE, D.O., AND M. SALVIONI. 1990. Social organization and nest co-occupancy in Peromyscus californicus, a monogamous rodent. Behavioral Ecology and Sociobiology 26:9–15.

RIBBLE, D. O., AND S. STANLEY. 1998. Home ranges and social organization of syntopic Peromyscus boylii and P. truei. Journal of Mammalogy 79:932–941.

ROUSSET, F. 2008. Genepop’007: a complete re-implementation of the genepop software for Windows and Linux. Molecular Ecology Resources 8:103–106.

SABOL, A. C., X. SOLOMON, AND B. DANTZER. 2018. How to Study Socially Monogamous Behavior in Secretive Animals? Using Social Network Analyses and Automated Tracking Systems to Study the Social Behavior of Prairie Voles. Frontiers in Ecology and Evolution 6:178.

SIKES, R. S., THE ANIMAL CARE AND USE COMMITTEE OF THE AMERICAN SOCIETY OF MAMMALOGISTS, 2016. 2016 Guidelines of the American Society of Mammalogists for the use of wild mammals in research and education. Journal of Mammalogy 97:663–688.

SILLERO-ZUBIRI, C., D. GOTTELLI, AND D. W. MACDONALD. 1996. Male philopatry, extra-pack copulations and inbreeding avoidance in Ethiopian wolves (Canis simensis). Behavioral Ecology and Sociobiology 38:331–340.

SOLOMON, N. G., ET AL. 2004. Multiple paternity in socially monogamous prairie voles (Microtus ochrogaster). Canandian Journal of Zoology 82:1667–1671.

SOMMER, S., AND H. TICHY. 1999. Major histocompatibility complex (MHC) class II polymorphism and paternity in the monogamous Hypogeomys antimena, the endangered, largest endemic Malagasy rodent. Molecular Ecology 8:1259–1272.

TRAINOR, B. C., AND C. A. MARLER. 2001. Testosterone, Paternal Behavior, and Aggression in the Monogamous California Mouse (Peromyscus californicus). Hormones and Behavior 40:32–42.

TRIVERS, R. L. 1972. Parental investment and sexual selection. Pp. 136-179, in Sexual selection and the descent of man (Campbell, B., ed.). Aldine, U.S.A.

WAN, D., P. CHANG, AND J. YIN. 2013. Causes of extra-pair paternity and its inter-specific variation in socially monogamous birds. Acta Ecologica Sinica 33:158–166.

WASER K. B., ET AL. 1994. Subordinate reproduction in dwarf mongooses. Animal Behaviour 47:65–75.

WEBER, J. N., ET AL. 2010. Five hundred microsatellite loci for Peromyscus. Conservation Genetics 11:1243–1246.

WESTNEAT, D. F., AND P. W. SHERMAN. 1997. Density and extra-pair fertilizations in birds: a comparative analysis. Behavioral Ecology and Sociobiology 41:205–215.

WITTKE-THOMPSON, J. K., A. PLUZHNIKOV, AND N. J. COX. 2005. Rational Inferences about Departures from Hardy-Weinberg Equilibrium. The American Journal of Human Genetics 76:967–986.

WOLFF, J. 1989. Social Behaviour. Pp. 271-292, in Advances in the Study of Peromyscus (Rodentia; Kirkland, Jr, G. L., and J. N. Layne, eds.). Texas Tech University Press. Lubbock, U.S.A.

Downloads

Published

2022-11-22

Issue

Section

Articles