Mate-choice (sexual conflict)

One key decision in the life history of mammals is mate-choice. An individual’s success in obtaining a mate, particularly a high quality mate, influences reproductive success and thus the representation of each individual’s genes in future generations. It is now recognised that both sexes have a common, but not identical, interest in this decision and may apply different criteria. Therefore, mate-choice is considered to be a key element of an important intra-specific evolutionary conflict known as sexual conflict. In social mammalian species, intra-specific conflicts such as sexual conflict are often a more powerful force of selection than environmental factors. Thus, an understanding of the evolutionary effects of sexual conflict on behaviour, communication and reproductive success of individuals contributes to an understanding of the adaptive value of mammalian life histories.

Female mate choice rules

The more closely mate-choice and its rules are studied, the clearer it becomes that in many species decision making rules applied by females (female mate-choice) set the framework within which the evolution of reproductive tactics is best seen. For instance, in spotted hyenas, we demonstrated that male-biased dispersal resulted from an adaptive response by males to simple female mate-choice rules that have evolved to avoid inbreeding. All females preferred sires that were born into or immigrated into the female’s group after the female was born, and older females preferred long-tenured sires. By applying these rules, females effectively avoid inbreeding without the need to discriminate directly against close kin or favour immigrant males.

Olfactory signals

Pheromones are substances used for communication between animals. They are secreted to the outside of the body by an individual and received by conspecifics. As our work on a variety of species has shown, pheromones can code for species, subspecies, sexual identity, age and reproductive status, as well as motivational state.

Mate choice decisions are usually based on so-called honest signals, i.e., signals that are almost impossible to fake by the signaller. A prominent group of honest signals are pheromones in the form of volatiles that diffuse from the signaller (potential mate) to a receiving individual (a choosing female). Olfactory signals may code for the reproductive condition of a potential mate, and probably also their immunocompetence, parasite load and social status. For example, spotted hyena scent carries both an olfactory badge of status, group membership and individually distinct cues that are likely to be useful in the maintenance of a social network within their fission–fusion society. And in the blackbuck antelope, pheromones also signal the dominance status of males.

Scents often work as a composite trait, i.e., the volatiles encode a variety of information. For example scents produced by male greater sag-winged bats provide information about species and individual identity and reproductive condition. Animal volatiles can also be used by humans for monitoring the reproductive condition of wildlife species under captive management. Past research at the IZW has confirmed that volatiles are useful in predicting the time of parturition in larger herbivores (such as elephants).

Acoustic communication and sexual selection

In polygamous species few males get most of the matings. This favours the evolution of sexually dimorphic features, e.g. the evolution of specific male calls restricted to the rutting season. These rutting calls are of high relevance to male reproductive success and subjected to sexual selection both by male-male competition and female preference. As a consequence, the males of some polygamous mammalian species, independent of each other, evolved similar features of the vocal organs and associated mechanisms of vocal production. So far, such species have been found among two families of ruminants: cervids [subspecies of red deer (Cervus elaphus), fallow deer (Dama dama)] and bovids [goitred gazelle (Gazella subgutturosa) and Mongolian gazelle (Procapra gutturosa)]. Two major features of their evolutionarily specialized vocal organs are a low mid-neck resting position of the larynx and the capability of pronounced rapid larynx retractions with each emission of a rutting call. The resulting back-and-forth shifts of the larynx, and the corresponding intermittent elongations of the vocal tract decrease the vocal tract resonance frequencies (formants). These are used as cues to body size by conspecific males and females. Formant decrease exaggerates body size acoustically and, in a male-male competition context, may effectively deter rival males, particularly under low light conditions where visual estimation of another stag’s body size is difficult. Acoustically assessing a rival’s body size can reduce energy-costly and injury-inflicting fights. As neck size correlates with body size intra-specifically, calls with maximally retracted larynx are still an honest signal, although on a different level compared to the ancestral forms with undescended larynx. In a mate-choice context rutting calls attract potential female mating partners, particularly during oestrus. Playback experiments have demonstrated that females in oestrus do even prefer artificially generated roars indicative of larger males than naturally occurring. This impressively demonstrates the selective pressure provoked by female preference and, at the same time, suggests a trade-off between sexual selection and natural selection.

Influence of health status and pathogens on mate-choice

Genes of the major histocompatibility complex (MHC) play a pivotal role in the vertebrate immune system. The MHC can serve as a mate-choice cue because it is associated with a perceptible odour. We have produced evidence for MHC associated mate-choice comes from an obligate pair-living primate. The fat-tailed dwarf lemur (Cheirogaleus medius) maintains life-long pair bonds but has an extremely high rate of extra-pair paternity. Females that cuckolded their social partners were more similar to them than faithful females. In a closely related promiscuous lemur species, the mouse lemur (Microcebus murinus), females do not choose a specific individual male before copulation but mate with many males. Instead of pre-copulatory choice, cryptic post-copulatory mechanisms operate which optimise the genetic constitution of the offspring.

Mate-choice and its interactions with genetic diversity

Genetic diversity in MHC genes is essential in pathogen resistance and thus fitness relevant. We could demonstrate its functional importance of MHC diversity in a wide range of mammalian taxa in rodents, marsupials, bats, carnivores, and primates. Sexual selection has been proposed as an important selective force driving MHC polymorphism. Although bats (Chiroptera) represent the second largest mammalian order, we still know very little about the evolution of their MHC. We are investigating the relevance of MHC immune gene variation for pathogen resistance, for individual life-history decisions as well as its role in olfactory communication in new world bat species (Noctilio albiventris, Saccopteryx bilineata) and spotted hyenas. Immunological defence is costly both in terms of immediate activation and long-term maintenance. Consistent with the ‘good genes’ model, males of the neotropical bat (Noctilio albiventris) harbouring genotypes that qualify for a good disease resistance are able to allocate more resources to reproductive effort which favours the transmission of good alleles into future generations.

Selected publications

Frey R, Volodin I, Volodina E, Carranza J, Torres-Porras J (2012) Vocal anatomy, tongue protrusion behaviour and the acoustics of rutting roars in free-ranging Iberian red deer stags (Cervus elaphus hispanicus). J Anat 220: 271-292.

Schad J, Dechmann D, Voigt C, Sommer S (2012) Evidence for the ‘good genes’ model: Association of MHC Class II DRB alleles with ectoparasitism and reproductive state in the neotropical lesser bulldog bat, Noctilio albiventris. PLoS ONE 7: e37101.

Dehnhard M (2011) Mammal semiochemicals: understanding pheromones and signature mixtures for better zoo-animal husbandry and conservation. Int Zoo Yb 45: 1–2.

Efremova KO, Volodin IA, Volodina EV, Frey R, Lapshina EN, Soldatova NV (2011) Developmental changes of nasal and oral calls in the goitred gazelle Gazella subgutturosa, a nonhuman mammal with a sexually dimorphic and descended larynx. Naturwissenschaften 98: 919-931.

Frey R, Volodin I, Volodina E, Soldatova NV, Juldaschev ET (2011) Descended and mobile larynx, vocal tract elongation and rutting roars in male goitred gazelles (Gazella subgutturosa Güldenstaedt, 1780). J Anat 218: 566-585.

Burgener N, Dehnhard M, Hofer H, East ML (2009) Does anal gland scent signal identity in the spotted hyaena? Anim Behav 77: 707-715.

Caspers B, Schroeder FC, MeinwaldJ, Franke S, Streich WJ, VoigtCC (2009) Odour-based species recognition in two sympatric species of sac-winged bats (Saccopteryx bilineata, S. leptura): Combining chemical analysis, behavioral observation and odour preference tests. Behav Ecol Sociobiol 63: 741-749.

Caspers B, FrankeS, Voigt CC (2008) The wing-sac odour of male greater sac-winged bats Saccopteryx bilineata (Emballonuridae) as a composite trait: Seasonal and individual differences. In: Chemical Signals in Vertebrates XI. Eds Hurst J, Beynon R, Müller-Schwarze D, Springer, Berlin New York, 151-160.

Höner OP, Wachter B, East ML, Streich WJ, Wilhelm K, Burke T, Hofer H (2008) Do female hyaenas choose mates based on tenure? Reply to Van Horn et al. Nature 454: E2.

Schwensow N, Eberle M, Sommer S (2008) Compatibility counts: MHC-associated mate choice in a wild promiscuous primate. Proc R Soc Lond B 275: 555-564.

Schwensow N, Fietz J, Dausmann K and Sommer S (2008) MHC-dependent mating strategies and the importance of overall genetic diversity in a pair-living primate. Evol Ecol 22: 617-636.

Höner OP, Wachter B, East ML, Streich WJ, Wilhelm K, Burke T, Hofer H (2007) Female mate choice drives the evolution of male-biased dispersal in a social mammal. Nature 448: 798-801.