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The Phylogenetic Distribution of a Female Preference University of Nebraska - Lincoln DigitalCommons@University of Nebraska - Lincoln Faculty Publications in the Biological Sciences Papers in the Biological Sciences 1996 The Phylogenetic Distribution of a Female Preference Alexandra Basolo University of Nebraska - Lincoln, [email protected] Follow this and additional works at: https://digitalcommons.unl.edu/bioscifacpub Part of the Life Sciences Commons Basolo, Alexandra, "The Phylogenetic Distribution of a Female Preference" (1996). Faculty Publications in the Biological Sciences. 45. https://digitalcommons.unl.edu/bioscifacpub/45 This Article is brought to you for free and open access by the Papers in the Biological Sciences at DigitalCommons@University of Nebraska - Lincoln. It has been accepted for inclusion in Faculty Publications in the Biological Sciences by an authorized administrator of DigitalCommons@University of Nebraska - Lincoln. Syst. Biol. 45(3):290-307, 1996 THE PHYLOGENETIC DISTRIBUTION OF A FEMALE PREFERENCE ALEXANDRA L. BASOLO Nebraska Behavioral Biobgy Group, University of Nebraska, Lincoln, Nebraska 68510, USA; E-mail: [email protected] Abstract.—Robust phylogenetic information can be instrumental to the study of the evolution of female mating preferences and preferred male traits. In this paper, the evolution of a preexisting female bias favoring a sword in male swordtail fish and the evolution of the sword, a complex character, are used to demonstrate how the evolution of mating preferences and preferred traits can be examined in a phylogenetic context. Phylogenetic information suggests that a preference for a sword arose prior to the evolution of the sword in the genus Xiphophorus and that the sword was adaptive at its origin. A phylogenetic approach to the study of female preferences and male traits can also be informative when used in conjunction with mate choice theory in making predictions about evolutionary changes in an initial bias, both prior to the appearance of the male trait it favors and subsequent to the appearance of the trait. [Mate choice; female preference; preexisting biases; Priapella; swordtail; sword; Xiphophorus.] The study of the evolution of mating who have genotypes of higher viability. preferences is an area of much contention. Fisherian processes models stress the im- Until relatively recently, there was dis- portance of linkage disequilibrium be- agreement over the importance of female tween the female preference and the sex- mate choice. In the past 15 years, however, ually selected trait; the preference evolves many studies have shown that females ex- as a correlated response to male trait evo- hibit mating preferences and that these lution. Correlated effects models suggest mating preferences can have an important that female preferences evolve as a corre- effect on male mating success. Many mod- lated result of male preference evolution. els have been proposed to explain the evo- That is, males have a preference for a trait lution of female preferences; these models in females, the genetic basis of the prefer- can be assigned to one of five primary cat- ence in males is shared with females or is egories: direct benefits (Trivers, 1972; Hal- correlated for some other reason, there is liday, 1978; Thornhill and Alcock, 1983; no significant cost to the expression of this Kirkpatrick and Ryan, 1991), good genes preference in females, and thus a female (Williams, 1966; Zahavi, 1977; Hamilton preference for the trait in males evolves as and Zuk, 1982; Andersson, 1986; Pomian- a correlated effect of evolution of the male kowski, 1988), Fisherian processes (Fisher, preference for the trait in females. 1930; Lande, 1981; Kirkpatrick, 1982), cor- Models stressing the importance of good related effects (Darwin, 1871; Lande and genes, correlated effects, Fisherian process- Arnold, 1985; Halliday and Arnold, 1987; es, and some cases of direct benefits re- Arnold and Halliday, 1992), and preexist- quire genetic variation in the preference ing biases (Barlow, 1977; West-Eberhard, and some component of male fitness, and 1984; Kirkpatrick, 1987a; West-Eberhard et they predict coevolution of the preference al., 1987; Endler and McLellan, 1988; Ba- and trait. Little experimental data have solo, 1990b, 1995b; Kirkpatrick and Ryan, been produced that support one of these 1991). Direct benefits models suggest that revolutionary models to the exclusion of females receive a benefit from mating with the others. None of these models predict a certain male. For example, they may re- the evolution of a preference prior to a trait ceive a resource directly or they may gain (although any of them could result in pref- access to a resource for either themselves erences for traits not yet present). The fifth or their offspring. Good genes models sug- model, the preexisting bias model, sug- gest that female preferences evolve under gests that there are female biases resulting selection for females to mate with males from evolutionary processes independent 290 1996 BASOLO—PHYLOGENY OF A PREFERENCE 291 of sexual selection on the specific trait un- to describe how their interaction might af- der study and present prior to the appear- fect the direction of selection. Ryan (1990) ance of that male trait. (By convention, suggested that male traits may arise that mating preferences are presented in terms capitalize on biases in the female sensory of females and preferred traits are pre- system, using the term "sensory exploita- sented in terms of males, but the ideas are tion." Basolo (1990b) proposed a critical interchangeable regardless of sex.) test using phylogenetic information and a A unique prediction of a preexisting bias stepwise approach for testing preexisting model is that the preference appeared pri- biases models and suggested a broadening or to the origin of the trait. This prediction of the category of biases to include higher can only be tested using the comparative levels of integration and information pro- method, and to implement the compara- cessing. tive method good phylogenetic informa- Preexisting biases can evolve for a num- tion is essential. In this paper, the impor- ber of reasons (Basolo, 1990b, 1995a, tance of robust phylogenetic information 1995b), but regardless of the origin of the to the study of the evolution of female bias, preexisting bias models postulate that preferences and preferred male traits is a male trait can arise and be favored by a demonstrated. First, I discuss the preexist- previously established bias. However, fur- ing bias model of sexual selection in terms ther evolution of the bias may occur fol- of both female preference and male trait lowing its origin, and after the male trait evolution. Second, I discuss the use of phy- arises and is selected by the preexisting logenetic information to test a hypothesis bias, other sources of sexual selection, e.g., of sexual selection, using my own work on good genes, direct benefits, correlated ef- swordtail fish as an example. Third, I dis- fects, Fisherian processes, and other pre- cuss how phylogenetic information can be existing biases, may act in conjunction utilized to generate new hypotheses once with the existing bias to further elaborate we know the phylogenetic distribution of or modify the preference. In addition, the a preference and trait; specifically, how initial bias can be changed as a result of new hypotheses can be formulated about natural selection or other sources of evo- how a preexisting bias should differ be- lutionary change. tween lineages in which the male trait has A clear demonstration that a preexisting and has not arisen. bias has played a role in the evolution of a male trait requires that three criteria be PREEXISTING BIASES met: (1) females prefer a conspecific male trait, (2) the absence of the male trait is the Sexual Selection ancestral state within a group, and (3) in a The idea of preexisting biases affecting species possessing the ancestral state for the direction of selection is not new, but it the male trait, females prefer the male trait has recently been formalized. Barlow even though it was not generally present (1977) suggested that signals should in the evolutionary history of the species. evolve to forms that are best perceived by To adequately test a preexisting bias mod- the receiver. West-Eberhard (1984) sug- el, a robust phylogenetic hypothesis is es- gested that sensory traps can be used by a sential. signaler to capitalize on receiver response that has been selected in another context. Adaptive Male Trait Evolution Kirkpatrick (1987a, 1987b) suggested that Mate choice models address the evolu- intrinsic biases affect female perception tion of mating preferences, but they also and can affect the direction of male trait make predictions concerning the evolution evolution. Endler and McLellan (1988) con- of male traits. In the case of preexisting sidered how the environment and sensory biases, male traits that arise and increase properties of the receiver affect signal re- in frequency because of a preexisting bias ception and used the term "sensory drive" are always by definition adaptive in the 292 SYSTEMATIC BIOLOGY VOL. 45 context of mating. Using phylogenetic in- erence has been investigated theoretically formation, it is possible to determine when with a model of visual recognition (Arak a female bias arose. At any time after the and Enquist, 1993; Enquist and Arak, appearance of a bias, an "adaptive field" 1993); simulations of a neural network for a male trait exists; that is, mate choice model demonstrate that in some cases a re- will favor the male trait if it arises. Muta- sponse to certain patterns not previously tions that occur at low frequencies and re- encountered can be stronger than a re- sult in new male traits may be lost before sponse to patterns that were initially se- selection can ever act on them or before lected to elicit a response. These unexpect- selection can have a maintaining effect. ed biases may evolve concealed and However, when an adaptive field in the nonfunctioning until a trait arises that is form of a preexisting bias exists for this recognized and selected by them.
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