Selection of reproductive partners in semi-feral horses (Equus caballus) is not influenced by major histocompatibility complex (MHC): A field study
Introduction
Reproduction is energetically expensive, starting from the production of gametes through pregnancy and offspring rearing (Hayward and Gillooly, 2011; Ramm and Stockley, 2014). To make this process worth the effort, humans and non-human animals are thought to deliberately choose their reproductive partners (Cluttonbrock and Vincent, 1991; Reznick et al., 2000; Speakman, 2008; Williams, 1966). By definition a mate choice occurs whenever reproductive investment such as courtship intensity or mate search is non-randomly distributed between members of the opposite sex (Edward, 2015). In a majority of animal species, reproductive effort is not equally shared between sexes: the role of males typically ends at conception, whereas females carry the burden of pregnancy and offspring rearing. Delivered genes are often the sole part the males share with females in species continuation. It has been assumed that this is the major reason for females to be selective about their breeding partners and the genes that they carry (Andersson and Simmons, 2006; Clutton-Brock and McAuliffe, 2009; Gavrilets et al., 2001; Jennions and Petrie, 2000).
In terms of genetic benefit to offspring, the major histocompatibility complex (MHC) is proposed as a criterion of mate choice (Drury, 2010; Eizaguirre et al., 2009; Milinski, 2006; Sommer, 2005). MHC genes are the group of polymorphic genes that play a fundamental role in immune defences in vertebral species (Janeway et al., 2001). Current hypotheses suggest females’ preferences for 1) a MHC-dissimilar partner, 2) a partner with a high diversity of MHC genes or 3) a partner with specific MHC genotype (Kamiya et al., 2014; Milinski, 2006; Ziegler et al., 2005) Every choice should result in the fitness of offspring (Trowsdale, 2011). However, several studies do not support the MHC-based mate choice hypothesis; thus, the phenomenon may not be universal across the species (Chaix et al., 2008; Havlicek and Roberts, 2008; Kamiya et al., 2014; Melendez-Rosa et al., 2018; Qiao et al., 2018; Yu et al., 2018).
In feral equines, where spontaneous selection is possible, the basic reproductive and social unit is a group that consists of several mares, their immature offspring and one stallion, rarely more. However, the stallion protects the mares from other stallions’ harassment, and even if subordinate stallions are present in a group, he exclusively mates harem mares (Berger, 1977; Linklater et al., 1999; Tyler, 1972). Sporadically, matings with subordinate stallions also occur (Bowling and Touchberry, 1990; Feh, 1999; Linklater et al., 1999). Peri-pubertal males and females disperse from the natal group. Young mature stallions either form their own group (harem) or join a multi-stallion group (bachelor band). Young mares typically adhere to a harem of an unfamiliar stallion (Feh, 1999; Linklater, 2000; Linklater and Cameron, 2009; Linklater et al., 1999; Monard and Duncan, 1996) Although horses reproduce seasonally, in feral conditions, mares and stallions remain together all year round (Berger, 1977; Linklater, 2000; Tyler, 1972). During the relatively long estrus period (5–7 days), mares exhibit proceptive behavior and receive sexual stimulation from the male, culminating with several copulations (Aurich, 2011; McDonnell, 2000). Usually, mares allow mating only harem stallions; however, it is suggested that they are selective about reproductive partners and may solicit more than one stallion during their breeding career (Burger et al., 2017a, b; Rubenstein and Nuñez, 2009)). The results of Burger et al. (2017a) suggest that the specific MHC of a stallion might be the factor that attracts a mare. Another study by Burger et al. (2017b) suggests that the MHC of the partner affects reproduction in horses. Clearly, the results are promising to equine industry; however, conditions of the experiments were neither natural nor the animals were allowed to contact directly. The question remains whether in conditions close to natural mares choose stallions based on MHC type.
The aim of the present study was to test the hypothesis that mares choose their mate depending on his MHC in horses allowed free choice of their reproductive partners from other equine groups present in available area. The present field study addresses the question of mate preferences according to two categories of MHC: a MHC-dissimilar and MHC-diverse partner. To the best of our knowledge, this was the first time that mare preferences regarding the MHC of stallions were studied in natural conditions.
Section snippets
Ethical note
The study involved an analysis of breeding records and regular observations of animals. Blood samples from mares and foals were taken during an annual parentage testing as required by studbook regulations. No experimentation was performed in view of European directive 2010/63/EU and the Polish laws related to ethics in animal experimentation. According to the European directive 2010/63/EU on the protection of animals used for scientific purposes chapter 1 article 1.5 “practices undertaken for
Choice of reproductive partner by mares
For all mares (n = 26), the reproductive partner was the current harem stallion. Altogether 2061 matings were observed, and in every time a mare mated with harem stallion. In total 126 foals were produced. No extra-harem matings were observed, but 11 mares changed harems; two of them changed harems twice to finally settle in a chosen harem. In the case of four mares, this change followed the death of a harem stallion (Stallion1) who was succeeded by another stallion (Stallion4) that assumed
Discussion
Our findings do not support the hypothesis that mares living under feral conditions mate preferentially to MHC-dissimilar stallions. In the investigated group of horses, MHC-dissimilarity between actual pairs of mares and stallions did not differ from that calculated for random mare-stallion dyads. Genetic similarity in the MHC between mares and stallions did not influence the possibility of choosing MHC dissimilar stallion by a mare. Interestingly, our results showed that MHC diversity of
Conclusion
In the present study, to the best of our knowledge, mate choice preferences of female horses were investigated under natural conditions for the first time. We conclude that MHC dissimilarity of a stallion may not be a decisive factor for semi-feral Konik Polski mares in the choice of reproductive partner. However, a tendency towards mating to MHC diverse stallions was detected. Nevertheless, under natural conditions, mares will usually breed to the current harem stallion. Moreover, we
Availability of data and materials
All data generated or analyzed during this study are included in this published article and its supplementary information files.
Authors’ contributions
JJ performed the laboratory work, analysed the data and wrote the manuscript. ZJ collected and analysed the data. DT performed the calculations in the Demerelate and Genhet packages. MS contributed to data collection. AGB supervised the work and contributed to the data analysis, manuscript writing and preparation. All authors critically revised and approved the final version of the manuscript.
Funding
This work was supported by Polish National Science Centre grant 2015/19/N/NZ5/00655, awarded to Joanna Jaworska.
Declaration of Competing Interest
We declare that there is no conflict of interest that could be perceived as prejudicing the impartiality of the research reported.
Acknowledgements
The Authors would like to thank Professor D.F. Antczak and Dr D.C. Miller from Baker Institute for Animal Health at the Cornell University for sharing their protocols of MHC microsatellites typing and helpful advices regarding MHC typing methodology. We are also grateful to Professor C. Aurich from the University of Veterinary Medicine in Vienna for helpful suggestions and comments which allowed improving the manuscript.
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