The role of mating preferences in shaping interspecific divergence in mating signals in vertebrates
Introduction
One of the critical components to understanding the process of speciation is determining which factors promote and maintain divergence in mate recognition systems. For species where mate recognition occurs primarily through non-behavioural mechanisms, such as in broadcast-spawning marine invertebrates (reviewed in Palumbi, 1994), selection favors gamete compatibility signals designed to avoid wasted matings between heterospecific gametes. The species-specific recognition between sperm bindin or lysin proteins and conspecific egg membranes is a good example of such a mating signal (Minor et al., 1989, Vacquier et al., 1990, Glabe and Clark, 1991, Lee et al., 1995, Swanson and Vacquier, 1995, Metz and Palumbi, 1996). In species with this type of mating system, species recognition signals evolve primarily as a result of intrasexual selection (sperm competition) for gamete recognition and possibly natural selection against hybrid offspring that result from heterogametic pairings (Palumbi, 1994). However, in species where mate recognition occurs primarily through premating courtship signals, mating preferences in one sex (female mate choice) can strongly influence the evolution of mating signals in the opposite sex, resulting in intersexual selection promoting divergence in mate recognition signals.
Evolutionary biologists have long been interested in how female mating preferences shape the evolution of male mating signals (Andersson, 1994). Studies however, have often focused either on the evolution of signal properties that serve as species isolating cues (species recognition) or properties of mating signals that indicate male quality within a species (intersexual selection) (Ryan and Rand, 1993a and citations therein). Few studies have focused on the interrelation between sexual selection and species recognition (but see Wiernasz, 1989, Wiernasz and Kingsolver, 1992, Boake et al., 1997). The traditional view of mating signal evolution suggests that certain features of the mating signal serve for species recognition; stabilizing selection decreases variance in these properties making them reliable species indicators (Waage, 1975, Kyriacou and Hall, 1982, Claridge et al., 1984, Butlin et al., 1985, Gerhardt, 1991, Barlow and Siri, 1997). Females use a different set of components of the mating signal when making intraspecific mating decisions and strong directional selection often shapes the evolution of these properties (Møller, 1988, Andersson, 1989, Zuk et al., 1990, Reynolds and Gross, 1992, Ryan and Keddy-Hector, 1992, Thompson et al., 1997). While this distinction in how selection shapes the evolution of different properties of a mating signal may be true for many multivariate signals (Pfennig, 1998), it implies that mate choice operates as a two step process. In the first step, a decision is made about species identity and the second step then involves a decision about mate quality. This distinction between interspecific mate recognition and intraspecific mate recognition however, is not likely to be a realistic process when females assess a potential mate. A more realistic view of mate choice argues that female mating preferences evolve as a direct consequence of selection of the ‘best’ mate among the available choices. Certainly, being a conspecific is one important aspect of being the best mate, but the process of mate choice is the same at all levels of discrimination (both intraspecific and interspecific) and thus, species recognition is a consequence of finding the best mate (Littlejohn, 1999). In this context, divergence in species recognition properties of mating signals may merely be an epi-phenomenon of intraspecific sexual selection (Gerhardt, 1982).
This continuum between sexual selection and species recognition is becoming the focus of more recent studies (Wiernasz and Kingsolver, 1992, Boake et al., 1997, Ptacek, 1998, Verrell, 1999). A number of authors have argued that sexual selection and species recognition are both essentially problems in animal communication (Verrell, 1988, Ryan and Rand, 1993a, Endler and Houde, 1995, Boake et al., 1997, Littlejohn, 1999). This implies that the same forces of evolution that influence signal properties used in species recognition also influence features of the signal that make the signaler a more attractive mate and that these signal features are not mutually exclusive. Thus mating preferences for certain features of a mating signal can promote divergence at both the intra- and interspecific levels. Divergence in mate recognition signals among populations within a species can lead ultimately to reproductive isolation and speciation (Lande, 1981, Thornhill and Alcock, 1983, West-Eberhard, 1983, West-Eberhard, 1984, Kaneshiro and Boake, 1987, Iwasa and Pomiankowski, 1995, Payne and Krakauer, 1997).
In order to demonstrate a link between mating preferences and species recognition, studies must ask whether the same male traits that are preferred by females within a species also function to distinguish conspecific from heterospecific males (i.e. traits that confer high mating success also confer a high degree of sexual incompatability). Only a few studies have directly tested this hypothesis (Wiernasz, 1989, Wiernasz and Kingsolver, 1992, Boake et al., 1997). Wiernasz (1989) demonstrated in Pieris butterflies that females of P. occidentalis use the same male character, dorsal forewing melanin pattern, to discriminate between potential conspecific mates and between conspecific and heterospecific males. In contrast, Boake et al. (1997) found that females of the stalk-eyed fly Drosophila heteroneura preferred males with broader heads, but did not use this trait when distinguishing between conspecific males and males of D. silvestris.
Mating signals are often complex traits where different components of the signal provide information to the receiver concerning species identity, gender, readiness to mate, individual identity and even mate quality (e.g. Crapon de Caprona and Ryan, 1990, Barlow, 1992, Rand et al., 1992, Gerhardt, 1994a, McLennan and Ryan, 1997, McLennan and Ryan, 1999). Determining the message and meaning of a mating signal and how mating preferences have shaped various components of the signal is necessary for us to better understand the relationship between intra- and interspecific mate choice.
In this review I explore how intraspecific mating preferences have shaped interspecific divergence in properties of mating signals in major groups of vertebrate taxa. While a number of studies have focused on mating preferences within species or on how mating signals function in species recognition (recently reviewed by Andersson, 1994), fewer have explored the role of mating preferences in the simultaneous divergence of both intra- and interspecific signal properties. First, I outline studies in different vertebrate groups that have focused on how mating preferences have shaped the evolution of interspecific divergence in mating signals. These include studies that have examined mating preferences for traits that reduce the possibility of heterospecific matings and studies in which traits that are the basis of mating preferences within species also function as species recognition signals. Second, I discuss how geographic variation in mating preferences among conspecific populations can potentially shape divergence of mate recognition signals and the potential role of such mating preferences in leading to speciation. I illustrate this point with a specific example from my own work on the poeciliid fishes commonly known as mollies.
Section snippets
Fishes
Teleost fishes represent one of the most species-rich vertebrate taxa, yet studies of mating preferences have concentrated on only a few groups (poeciliids: Crapon de Caprona and Ryan, 1990, Endler and Houde, 1995, Magurran et al., 1996, Warburton and Lees, 1996, McLennan and Ryan, 1997, McLennan and Ryan, 1999, Ptacek, 1998, cichlids: Barlow et al., 1990, Barlow and Siri, 1997, Karino, 1997, Seehausen et al., 1997a, Seehausen and van Alphen, 1998, Seehausen et al., 1999; hamlets: Fischer, 1980
Anuran amphibians
Frogs and toads communicate primarily through vocalizations given by males. The most common vocalization, termed the ‘advertisement call’ (Wells, 1977a, Wells, 1977b), signals a male's presence to reproductive females and in most taxa is the primary component of species recognition. Advertisement calls also function in interactions between males for acquisition and defense of territories that may contain oviposition sites (Howard, 1978, Duellman and Trueb, 1986), calling sites (Wells, 1977a,
Salamanders
Pheromones serve as a primary mating signal in salamanders (reviewed by Arnold and Houck, 1982; also see Houck and Reagan, 1990, Kikuyama et al., 1995). There is considerable evidence that chemical cues are important in species recognition and maintenance of reproductive isolation between sympatric species of salamanders and newts (e.g. Malacarne and Vellano, 1982, Dawley, 1984, Dawley, 1986, Verrell, 1986, Cogalniceanu, 1992). Males use pheromonal cues emitted by females to locate conspecific
Reptiles
Very few studies have attempted to examine mating preferences in reptiles, especially among snakes and crocodilians, which are often difficult experimental subjects (Tokarz, 1995). Most studies have focused on lizards, which exhibit a rich repertoire of highly conspicuous display behaviours (Carpenter and Ferguson, 1977, Jenssen, 1977, Carpenter, 1978, Martins and Lamont, 1998), and especially among Anolis lizards, which display a remarkable diversity in dewlap configuration including
Birds
Song, plumage patterns and courtship displays all appear to play a role in species recognition in birds. It has been difficult to tease apart the relative importance of each of these traits in species recognition since females are seldom exposed to just one feature at a time. Additionally, studies of female mating preferences in birds have been hampered to some degree by the fact that in many temperate species, females do not sing. Very few studies of mating preferences have been conducted on
Mammals
Communication among mammals usually entails olfactory, acoustic, visual and tactile signals. Scent plays a major role in social communication in mammals (e.g. Doty, 1976, Brown and MacDonald, 1985, Alberts, 1992), and the importance of olfactory perception for precopulatory recognition between members of the same and related species, especially in rodents, has been suggested by a number of studies (e.g. Parkes and Bruce, 1961, Moore, 1965, Smith, 1965, Bowers and Alexander, 1967, Doty, 1973,
Mating preferences, population divergence and speciation
An important role for mating preferences in shaping phenotypic trait distributions within species has considerable empirical support and is a major focus of many studies of sexual selection (reviewed by Andersson, 1994). However, the importance of sexual selection as an evolutionary force leading to speciation is still a subject of debate among evolutionary biologists. It has been theoretically demonstrated that sexual selection can lead to speciation when premating reproductive isolation
Conclusions
Mating preferences within species of vertebrates have been shown to lead to a wide variety of acoustic, visual, olfactory and tactile signals, many of which have important functions in species recognition. This implies an important role for sexual selection in signal divergence and speciation in vertebrates. More work is needed in order to fully understand the basis for mating preferences in many vertebrate species. As we begin to further explore the relationship between mating preferences and
Acknowledgements
The ideas on mate choice presented in this review have been formulated through helpful discussions with F. Breden, M. Childress, M. Dyson, H. C. Gerhardt, F. H. Rodd, J. Travis and C. Trost. I am indebted to a number of people for their insightful comments on an earlier version of the manuscript, including S. A. Foster, H. C. Gerhardt, T. Pitcher, C. Trost, P. Verrell and the two reviewers, P. Joly and M. Lambrechts. I am especially grateful for the many hours that S. Strzalkowska spent in
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