Elsevier

Behavioural Processes

Volume 51, Issues 1–3, 5 October 2000, Pages 111-134
Behavioural Processes

The role of mating preferences in shaping interspecific divergence in mating signals in vertebrates

https://doi.org/10.1016/S0376-6357(00)00123-6Get rights and content

Abstract

Vertebrates represent one of the best-studied groups in terms of the role that mating preferences have played in the evolution of exaggerated secondary sexual characters and mating behaviours within species. Vertebrate species however, also exhibit enormous interspecific diversity in features of mating signals that has potentially led to reproductive isolation and speciation in many groups. The role that sexual selection has played in interspecific divergence in mating signals has been less fully explored. This review summarizes our current knowledge of how mating preferences within species have shaped interspecific divergence in mate recognition signals among the major vertebrate groups. Certain signal modalities appear to characterize mating signal diversification among different vertebrate taxa. Acoustic signals play an important role in mating decisions in anuran amphibians and birds. Here, different properties of the signal may convey information regarding individual, neighbor and species recognition. Mating preferences for particular features of the acoustic signal have led to interspecific divergence in calls and songs. Divergence in morphological traits such as colouration or ornamentation appears to be important in interspecific diversity in certain groups of fishes and birds. Pheromonal signals serve as the primary basis for species-specific mating cues in many salamander species, most mammals and even some fishes. The evolution of interspecific divergence in elaborate courtship displays may have played an important role in speciation of lizards, and particular groups of fishes, salamanders, birds and mammals. While much research has focused on the importance of mating preferences in shaping the evolution of these types of mating signals within species, the link between intraspecific preferences and interspecific divergence and speciation remains to be more fully tested. Future studies should focus on identifying how variation in mating preferences within a species shapes interspecific diversity in features of mating signals in order to better understand how sexual selection may have led to speciation 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

References (311)

  • S. Castellano et al.

    Stabilizing and directional female choice for male calls in the European green toad

    Anim. Behav.

    (1998)
  • T.P. Cox

    Ethological isolation between local populations of house mice (Mus musculus) based on olfaction

    Anim. Behav.

    (1984)
  • M.-D. Crapon de Caprona et al.

    Conspecific mate recognition in swordtails, Xiphophorus nigrensis and X. pygmaeus (Poeciliidae): olfactory and visual cues

    Anim. Behav.

    (1990)
  • E.M. Dawley

    Recognition of individual, sex and species odours by salamanders of the Plethodon glutinosusP. jordani complex

    Anim. Behav.

    (1984)
  • J.A. Farr et al.

    Behavioural allometry and interdemic variation in sexual behaviour of the sailfin molly Poecilia latipinna (Pisces: Poeciliidae)

    Anim. Behav.

    (1986)
  • H.C. Gerhardt et al.

    Female treefrogs do not avoid heterospecific calls as they approach conspecific calls; implications for mechanisms of mate choice

    Anim. Behav.

    (1994)
  • H.C. Gerhardt

    Mating behavior and male mating success in the green treefrog

    Anim. Behav.

    (1987)
  • H.C. Gerhardt

    Female mate choice in treefrogs: static and dynamic acoustic criteria

    Anim. Behav.

    (1991)
  • H.C. Gerhardt

    Multiple messages in acoustic signals

    Neurosciences

    (1992)
  • H.C. Gerhardt

    Reproductive character displacement of the grey treefrog Hyla chrysoscelis

    Anim. Behav.

    (1994)
  • H.L. Gibbs

    Cultural evolution of male song types in Darwin's medium ground finches, Geospiza fortis

    Anim. Behav.

    (1990)
  • G. Abt et al.

    Mate choice and fitness in a hybrid frog: Rana esculenta females prefer Rana lessonae males over their own

    Behav. Ecol. Sociobiol.

    (1993)
  • R.V. Alatalo et al.

    Hybridization between pied and collared flycatchers — sexual selection and speciation theory

    J. Evol. Biol.

    (1990)
  • A.C. Alberts

    Constraints on the design of chemical communication systems in terrestrial vertebrates

    Am. Nat.

    (1992)
  • S. Andersson

    Sexual selection and cues for female choice in leks of Jackson's widowbird Euplectes jacksoni

    Behav. Ecol. Sociobio.

    (1989)
  • M. Andersson

    Sexual Selection

    (1994)
  • A. Arak

    Female mate selection in the natterjack toad: active choice or passive attraction?

    Behav. Ecol. Sociobiol.

    (1988)
  • E.A. Armstrong

    Bird Display and Behaviour

    (1965)
  • S.J. Arnold et al.

    Courtship pheromones: evolution by natural and sexual selection

  • S.J. Arnold et al.

    The evolution of asymmetry in sexual isolation: a model and a test case

    Evolution

    (1996)
  • M.C. Baker et al.

    Reproductive behavior of female buntings: isolating mechanisms in a hybridizing pair of species

    Evolution

    (1990)
  • M.C. Baker et al.

    Early experience determines song dialect responsiveness of female sparrows

    Science

    (1981)
  • M.C. Baker

    Vocal dialect recognition and population genetic consequences

    Am. Zool.

    (1982)
  • M.C. Baker

    The behavioral response of female Nuttall's white-crowned sparrows to male songs of natal and alien dialects

    Behav. Ecol. Sociobiol.

    (1983)
  • M.C. Baker

    Response of male indigo and lazuli buntings and their hybrids to song playback in allopatric and sympatric populations

    Behaviour

    (1991)
  • E. Balaban

    Bird song syntax: learned intraspecific variation is meaningful

    Proc. Natl. Acad. Sci. U.S.A.

    (1988)
  • E. Balaban

    Behavioral salience of geographical song variants

    Behaviour

    (1988)
  • J.S. Balsano et al.

    Reproductive behavior and maintenance of all-female Poecilia

    Environ. Biol. Fish.

    (1985)
  • K.E. Barlow et al.

    Differences in songflight calls and social calls between two phonic types of the vespertilionoid bat Pipistrellus pipistrellus

    J. Zool.

    (1997)
  • G.W. Barlow

    Is mating different in a monogamous species? The midas cichlid as a case study

    Am. Zool.

    (1992)
  • A.L. Basolo

    Female preference predates the evolution of the sword in swordtail fish

    Science

    (1990)
  • A.L. Basolo

    Phylogenetic evidence for the role of a pre-existing bias in sexual selection

    Proc. R. Soc. London B

    (1995)
  • C.L. Baube et al.

    The mechanisms of colour-based mate choice in female threespine sticklebacks: hue, contrast and configurational cues

    Behaviour

    (1995)
  • P.H. Becker

    Verhalten auf lautäusserungen der zwillingsart, interspezifische territorialität und habitatansprüche von Winterund Sommergoldhänchen (Regulus regulus, R. ignicapillus)

    J. Ornithol.

    (1977)
  • D.J. Bell

    Mate choice in the European rabbit

  • V.L. Bels

    The mechanisms of dewlap extension in Anolis carolinensis (Reptilia: Iguanidae) with histological analysis of the hyoid apparatus

    J. Morph.

    (1990)
  • P.R.Y. Blackwell et al.

    Mate choice in the neotropical frog, Hyla ebraccata: sexual selection, mate recognition and signal selection

    Anim. Behav.

    (1993)
  • S.D. Blum

    Osteology and phylogeny of the Chaetodontidae (Pisces: Perciformes)

    (1988)
  • C.R.B. Boake et al.

    Is sexual selection and species recognition a continuum? Mating behavior of the stalk-eyed fly Drosophila heteroneura

    Proc. Natl. Acad. Sci. U.S.A.

    (1997)
  • G. Borgia

    Complex male display and female choice in the spotted bowerbird: specialized functions for different bower decorations

    Anim. Behav.

    (1995)
  • Cited by (120)

    • Acoustic signals produced by Nile tilapia Oreochromis niloticus and black-chinned tilapia Sarotherodon melanotheron during intra- and interspecific pairings

      2020, Zoology
      Citation Excerpt :

      Tilapia species of these last two groups belong to the Oreochromini tribe (Dunz and Schliewen, 2013). Although reproductive behaviours can show differences between tilapia genera, hybridization between some species is possible (Toguyeni et al., 2009), implying that the reproductive barrier is not impermeable (Ptacek, 2000). This is true, for example, between black-chinned tilapia Sarotherodon melanotheron Rüppell 1852, a species with paternal or biparental mouthbrooding, and O. niloticus, a strictly maternal mouthbrooder (Trewavas, 1983) although the two species are phylogenetically close (Dunz and Schliewen, 2013) and separated some 2.3 millions years ago (Nagl et al., 2001).

    • Weak premating isolation between two parapatric brocket deer species

      2017, Mammalian Biology
      Citation Excerpt :

      Postmating–prezygotic mechanisms have been shown to effectively reduce gene flow and thus act to maintain species boundaries if fertilization success in conspecific matings is relatively greater than that in heterospecific ones (Howard et al., 2009). Sexual selection has an important role in maintaining species isolation by the evolution of signal divergence between species (Ptacek, 2000). Female choice is an important mechanism of both species recognition and intraspecific mate selection (Andersson, 1994; Kokko et al., 2003).

    View all citing articles on Scopus
    View full text