Elsevier

Animal Behaviour

Volume 104, June 2015, Pages 203-212
Animal Behaviour

Genetic variation in male sexual behaviour in a population of white-footed mice in relation to photoperiod

https://doi.org/10.1016/j.anbehav.2015.03.026Get rights and content

Highlights

  • We examined sexual behaviour of short-day responder vs nonresponder male mice.

  • Short, winter-like daylength repressed sexual behaviour only in the responder line.

  • Sexual behaviour was eliminated only if males had very low or zero sperm counts.

  • Odour cues from females enhanced sexual maturation in the nonresponder line.

  • In nature, genetically responder mice could lack sexual behaviour in winter.

In natural populations, genetic variation in seasonal male sexual behaviour could affect behavioural ecology and evolution. In a wild-source population of white-footed mice, Peromyscus leucopus, from Virginia, U.S.A., males experiencing short photoperiod show high levels of genetic variation in reproductive organ mass and neuroendocrine traits related to fertility. We tested whether males from two divergent selection lines, one that strongly suppresses fertility under short photoperiod (responder) and one that weakly suppresses fertility under short photoperiod (nonresponder), also differ in photoperiod-dependent sexual behaviour and responses to female olfactory cues. Under short, but not long, photoperiod, there were significant differences between responder and nonresponder males in sexual behaviour and likelihood of inseminating a female. Males that were severely oligospermic or azoospermic under short photoperiod failed to display sexual behaviour in response to an ovariectomized and hormonally primed receptive female. However, on the day following testing, females were positive for spermatozoa only when paired with a male having a sperm count in the normal range for males under long photoperiod. Males from the nonresponder line showed accelerated reproductive development under short photoperiod in response to urine-soiled bedding from females, but males from the responder line did not. The results indicate genetic variation in sexual behaviour that is expressed under short, but not long, photoperiod, and indicate a potential link between heritable neuroendocrine variation and male sexual behaviour. In winter in a natural population, this heritable behavioural variation could affect fitness, seasonal life history trade-offs and population growth.

Section snippets

Selection Lines of Peromyscus leucopus

Detailed descriptions of the selection lines used in this study are available elsewhere (Broussard et al., 2009, Heideman et al., 1999, Heideman and Pittman, 2009); here we provide a brief description. Two artificial selection lines and an unselected control line were established in 1995 from 208 offspring of 48 wild-caught mice. These 208 offspring were conceived under long photoperiod and transferred at birth to short photoperiod. At an age of 67–73 days, body mass and reproductive

Experiment 1: Variability and Phenotypic Plasticity in Sexual Behaviour, Reproductive Organs and Body Mass

Testes and seminal vesicles were larger in nonresponder mice than in responder mice (Fig. 1a, b, Table 1). In both lines, testes and seminal vesicles were significantly larger under long photoperiod than under short photoperiod (Fig. 1a, b, Table 1). Although testes mass of nonresponder mice in the short-day group was similar to that of responder mice in the control group (Fig. 1a), nonresponder mice in the short-day group had smaller seminal vesicles (Fig. 1b). Body mass of adult males was

Discussion

Our results demonstrate heritable variation in male sexual behaviour under short photoperiod. Short photoperiod caused lower reproductive organ mass and sperm counts in both lines (Fig. 1), indicating that both lines detect and respond to a seasonal photoperiod signal. Male sexual behaviour was strongly reduced only in the responder line under short photoperiod (Fig. 3a), in which male sexual behaviour did not occur on the test night below defined thresholds of reproductive organ mass and sperm

Acknowledgments

We thank Donald Dewsbury for valuable insights into scoring sexual behaviours of Peromyscus, Eric Bradley and Daniel Cristol for useful comments on the experimental design and analyses. We thank Lisa Moore and Lydia Wright-Jackson for animal care. Two anonymous referees and the editor provided invaluable suggestions to improve the manuscript. Funding was provided by the National Institutes of Health (R15-HD068962) and the College of William and Mary.

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  • 1

    E-mail address: [email protected] (K. Sharp).

    2

    E-mail address: [email protected] (D. Bucci)

    3

    E-mail address: [email protected] (P. K. Zelensky).

    4

    E-mail address: [email protected] (A. Chesney).

    5

    E-mail address: [email protected] (W. Tidhar).

    6

    E-mail address: [email protected] (D. R. Broussard).

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