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Female Receptivity, Embryonic Diapause, and Superfetation in the European Badger (Meles Meles): Implications for the Reproductive Tactics of Males and Females

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Female Receptivity, Embryonic Diapause, and Superfetation in the European Badger (Meles Meles): Implications for the Reproductive Tactics of Males and Females University of Groningen Female receptivity embryonic diapause, and superfetation in the European badger (Meles Meles): Implications for the reproductive tactics of males and females Yamaguchi, N; Dugdale, Hannah L.; Macdonald, DW Published in: Quarterly review of biology DOI: 10.1086/503923 IMPORTANT NOTE: You are advised to consult the publisher's version (publisher's PDF) if you wish to cite from it. Please check the document version below. Document Version Publisher's PDF, also known as Version of record Publication date: 2006 Link to publication in University of Groningen/UMCG research database Citation for published version (APA): Yamaguchi, N., Dugdale, H. L., & Macdonald, DW. (2006). Female receptivity embryonic diapause, and superfetation in the European badger (Meles Meles): Implications for the reproductive tactics of males and females. Quarterly review of biology, 81(1), 33-48. https://doi.org/10.1086/503923 Copyright Other than for strictly personal use, it is not permitted to download or to forward/distribute the text or part of it without the consent of the author(s) and/or copyright holder(s), unless the work is under an open content license (like Creative Commons). The publication may also be distributed here under the terms of Article 25fa of the Dutch Copyright Act, indicated by the “Taverne” license. More information can be found on the University of Groningen website: https://www.rug.nl/library/open-access/self-archiving-pure/taverne- amendment. Take-down policy If you believe that this document breaches copyright please contact us providing details, and we will remove access to the work immediately and investigate your claim. Downloaded from the University of Groningen/UMCG research database (Pure): http://www.rug.nl/research/portal. For technical reasons the number of authors shown on this cover page is limited to 10 maximum. Volume 81, No. 1 THE QUARTERLY REVIEW OF BIOLOGY March 2006 FEMALE RECEPTIVITY, EMBRYONIC DIAPAUSE, AND SUPERFETATION IN THE EUROPEAN BADGER (MELES MELES): IMPLICATIONS FOR THE REPRODUCTIVE TACTICS OF MALES AND FEMALES Nobuyuki Yamaguchi Wildlife Conservation Research Unit, University of Oxford Tubney House, Abingdon Road, Tubney, Abingdon OX13 5QL United Kingdom e-mail: [email protected] Hannah L. Dugdale Wildlife Conservation Research Unit, University of Oxford Tubney House, Abingdon Road, Tubney, Abingdon OX13 5QL United Kingdom e-mail: [email protected] David W. Macdonald Wildlife Conservation Research Unit, University of Oxford Tubney House, Abingdon Road, Tubney, Abingdon OX13 5QL United Kingdom e-mail: [email protected] keywords blastocyst, delayed implantation, mate guarding, progesterone, superfecundation abstract The European badger Meles meles is thought to mate throughout the year, with two mating peaks occurring in late winter/spring and summer/autumn. After mating, fertilized ova enter embryonic diapause (delayed implantation) at the blastocyst stage, which lasts up to eleven months. Even if mating is successful, however, the estrous cycle may continue during embryonic diapause, which sug- gests that female badgers are capable of superfetation (conception during pregnancy). This may increase female fitness by facilitating polyandry, and reduce the risk of infanticide by resident males through paternity confusion. Detailed understanding of female receptivity, specifically the association of super- fetation with embryonic diapause, may explain field observations of seemingly inconsistent reproductive The Quarterly Review of Biology, March 2006, Vol. 81, No. 1 Copyright ᭧ 2006 by The University of Chicago. All rights reserved. 0033-5770/2006/8101-0002$15.00 33 This content downloaded from 129.125.136.103 on June 13, 2018 01:26:22 AM All use subject to University of Chicago Press Terms and Conditions (http://www.journals.uchicago.edu/t-and-c). 34 THE QUARTERLY REVIEW OF BIOLOGY Volume 81 tactics of male badgers with regard to, for instance, whether or not they guard mates or defend territories. The combination of embryonic diapause and superfetation may occur in other mustelids; if so, the sociobiology of mustelids will need re-evaluating, and the Mustelidae may prove to be a good model taxon for studies of sexual conflict in the reproduction of eutherian mammals. ATURAL SELECTION and sexual se- flict in American mink reproduction, and this N lection act on both sexes. However, em- phenomenon may occur in other members of phasis on sexual selection as a directional evo- the Mustelidae (Thom et al. 2004b; Yamagu- lutionary force acting on males has diverted chi et al. 2004). The Mustelidae is unusual attention from the selective processes acting amongst eutherian families (placental mam- on females, whose discrete mating tactics may mals), as not only is it comprised of approxi- have masked the extent of the potential for mately one-third of the species known to reproductive conflict between the sexes (Zeh exhibit embryonic diapause (Mead 1981; and Zeh 2003). Recent evidence suggests Sandell 1990; Ben-David 1998; Renfree and that the reproductive interests of males and Shaw 2000; Thom et al. 2004a), but also all females frequently differ, thereby generat- additional transitions of the evolution of em- ing sexual conflict rather than cooperation bryonic diapause amongst the Carnivora oc- (Chapman et al. 2003; Montrose et al. 2004). cur within the Mustelidae (Lindenfors et al. This is highlighted in polyandrous mating sys- 2003). The possible connections between tems, which may be the norm across various embryonic diapause and superfetation, and taxa (Chapman et al. 2003; Zeh and Zeh their importance with regards to sexual con- 2003). Such sexual conflict is manifested as a flict in the Mustelidae, merit consideration. “tug-of-war” at both precopulatory and post- The aim of this paper is to shed light on the copulatory stages, with males attempting to importance of female reproductive physiol- monopolize access to the females’ ova and ogy for the evolution of reproductive tactics manipulate their physiology, while females at- of both sexes by focusing on another mus- tempt to control their own reproductive op- telid, the European badger Meles meles, for tions (Chapman et al. 2003; Zeh and Zeh which relatively robust information is avail- 2003; Hosken and Stockley 2004; Martin et al. able in terms of its ecology, behavior, and re- 2004). Therefore, it is important to under- productive physiology. stand the mechanisms through which males and females achieve reproductive success Distribution and Social Organization (Zeh and Zeh 2003). The European badger (Meles meles)isa Understanding sociobiology requires knowl- large, stocky mustelid that weighs around 10 edge of the tactics that maximize individual kg. It is widely distributed across Eurasia, survival and reproductive success, which are from the U.K. to Japan and from Palestine to determined by the availability of food and the Russian Arctic Circle. It exhibits large shelter for both sexes and the receptivity of variation in social organization, being solitar- females for males (Macdonald 1983; Sandell ily, pair, or small group living in many parts 1989). In spite of the theoretically accepted of Eurasia and group living in parts of the importance of the pattern of female receptiv- U.K. This is unique among badgers as all oth- ity, empirical information, particularly on re- ers are solitary (e.g., the American badger productive physiology and endocrinology, is Taxidea taxus; Macdonald 2001). Social groups rudimentary for many species. Furthermore, of badgers can be composed of up to 30 in- it has recently been suggested that the un- dividuals that share a large communal “sett” usual reproductive phenomenon of superfe- or den (a network of underground tunnels tation (conception during pregnancy; Shack- and chambers; Neal and Cheeseman 1996; elford 1952) that occurs in female American Johnson et al. 2002). However, cooperative mink Mustela vison may, in combination with behaviors amongst group members are less embryonic diapause (delayed implantation developed than those seen in highly social of embryos), play a crucial role in sexual con- mammalian species such as wolves Canis lupus This content downloaded from 129.125.136.103 on June 13, 2018 01:26:22 AM All use subject to University of Chicago Press Terms and Conditions (http://www.journals.uchicago.edu/t-and-c). March 2006 EUROPEAN BADGER REPRODUCTION 35 (da Silva et al. 1994; Woodroffe and Macdon- ald 2000; Macdonald et al. 2002b; Revilla and Palomares 2002; Rogers et al. 2003). Cur- rently a considerable bias exists in the litera- ture on Meles meles because a disproportionate number of studies have been conducted in the U.K. where these badgers live in social groups. The reported reproductive biology thus may not be applicable throughout its range (Neal and Cheeseman 1996; Johnson et al. 2002). The identity of the population Figure 1. Seasonal Variation in Testes Weight from which data were derived is therefore and the Proportion of Males with Spermatozoa specified throughout this paper. The generally high levels of testicular activity as shown by testes weight (bar chart) and the proportion Mating and Birth of animals with spermatozoa (solid line) among adult Since the classic work of Neal and Harrison males in their third year or older. Testes weight is the (1958), based on about 85 animals from average wet weight of testes combined with epididy- southern England, post mortem studies of mides, both with and without spermatozoa. the reproductive
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