The Role of Nuptial Coloration in Female Holbrookia maculata: Evidence for a Dual Signaling System

Abstract

-Although the behavioral significance of bright female coloration has been evaluated for many organisms, its role in squamates is less clear. The conditional signal hypothesis posits that bright female coloration signals are conditional upon the degree of coloration: early in the breeding season low-intensity coloration signals courtship receptivity, whereas later in the season high-intensity pigmentation signals courtship rejection. This system is adaptive if the benefits of color maintenance and expression outweigh the costs associated with conspicuous markings. Results of this work on the lesser earless lizard, Holbrookia maculata, of southern New Mexico, suggest that females (1) maximize the potential for egg fertilization by stimulating courtship with low-intensity coloration when eggs are ready for fertilization, and (2) reject courtship with high-intensity pigmentation when carrying fertilized eggs. This line of evidence establishes a more complete explanation for the adaptive role of bright female coloration in lizards. The role of secondary sexual coloration in animals has been the focus of much research (Darwin, 1871; Andersson, 1994). Results of this research suggest that coloration evolves and is I Present address: Department of Biology, Augustana College, Rock Island, Illinois 61201-2296, USA; E-mail: [e-mail] l secondary sexual coloration in anee the focus of much research (Dar; dersson, 19 4). Results of this remaintained in individuals that are successful at signaling competitive and reproductive abilities. Where secondary sexual coloration exists in an animal system, males are usually the more colorful sex. Male color intensity is correlated with fighting ability and mate choice preferences by females (Bradbury and Andersson, 1987; Andersson, 1994). In some species, females are the more brightly colored sex, and color functions 624 This content downloaded from 157.55.39.27 on Mon, 05 Sep 2016 05:46:39 UTC All use subject to http://about.jstor.org/terms NUPTIAL COLORATION IN FEMALE LIZARDS in sex role reversal or courtship by females and mate choice by males in insects, fish, amphibians, and birds (Baird, 1988; Andersson, 1994). However, bright female lizard coloration seems to operate in additional ways. Intense female pigmentation in lizards occurs in some 36 species (Cooper and Greenberg, 1992). For about half of these, coloration is brightest between ovulation and oviposition and, thus, when females are gravid (carrying fertilized eggs in the oviducts). Generally, the onset of coloration occurs shortly before ovulation, quickly brightens after ovulation (within hours), and then fades following egg laying. In species with multiple clutches of eggs per season, coloration is more complex, and many do not fade completely following oviposition (Zucker and Boecklen, 1990; T. Baird, pers. comm.). There appears to be a hormonal basis to this phenomenon because pigmentation is exogenously induced by progesterone in at least some species and in progesterone and estradiol combinations (Cooper and Clarke, 1982; Cooper and Crews, 1988). From a behavioral point of view, female aggression is sometimes positively related to color intensity (Cooper and Greenberg, 1992). Of those species for which data have been collected, bright females display aggressive behavior toward males that are interpreted by researchers as rejection of male sexual advances. Recent studies have attempted to identify the adaptive significance of such coloration in lizards (Cooper and Greenberg, 1992; Watkins, 1997). Bright coloration in female lizards may serve to advertize gender and sexual maturity (Cooper and Greenberg, 1992). That males of some species whose females lack nuptial coloration identify plainly colored females as being reproductively mature suggests bright coloration functions in other capacities. One possibility is that brightly colored females signal territoriality of nest sites to each other (Yedlin and Ferguson, 1973), although recent evidence for Crotaphytus collaris that tested the behavioral significance of female aggression refuted this hypothesis (Sloan and Baird, 1999). Scattered accounts suggest that females are sexually receptive to males prior to ovulation and while in the process of developing nuptial coloration (the courtship stimulation hypothesis: Fitch, 1956; Cooper and Crews, 1988) and then are nonreceptive following ovulation when pigments are vivid and near peak intensity (the courtship rejection hypothesis: Cooper, 1988; Cooper and Crews, 1988). The conditional signal hypothesis was developed in response to these two latter observations (Cooper and Greenberg, 1992). This hypothesis states that males, while monitoring their territories, detect subtle color changes in females early in the breeding season that signal sexual receptivity. Some time later, intensification of color and aggression by females signal gravidness, and any further copulation is fruitless. That is, the initial onset of coloration signals female receptivity, whereas the full color display signals rejection by the female. Adult females of the lesser earless lizard (Holbrookia maculata) of White Sands, New Mexico, exhibit the phenomenon of bright pigmentation (Dixon, 1967). However, a detailed examination of the role of bright female coloration is lacking for this species. Preliminary observations of this population suggested that gravid females exhibit bright coloration during the breeding season during which time they are aggressive toward males and that coloration fades and aggression subsides later in the breeding season when females are no longer gravid (Hager, 1998). The objectives of this study were to (1) determine whether the onset of female coloration stimulates courtship and attempted copulation in males, (2) establish that bright female coloration at its peak intensity is effective in reducing male sexual advances, and (3) ascertain the detailed relationship of coloration with behavior and reproductive state in females. MATERIALS AND METHODS Holbrookia maculata is short, stout, and dorsally pallid with fairly well-defined ventro-lateral blotches (Smith, 1943). It is the only lizard endemic to the white gypsum dunes of the White Sands National Monument (WSNM), New Mexico (Atstatt, 1939; Dixon, 1967). Norris (1967) reported that, with the exception of Uta stansburiana of the Pisgah Lava Flow, San Bernardino County, California, White Sands H. maculata exhibit the best background color match of any phrynosomatid lizard in the United States. Body coloration of mature males and females is sexually dimorphic (Clarke, 1965; Hager, In press). Two black blotches are found bilaterally on both males and females and are confined to the ventro-lateral portion of the midtorso (Stebbins, 1985). These spots are always present but are smaller and less prominent in females. Males have throat patches that range from light orange to bright crimson. Bright female coloration is a phenomenon displayed only during the breeding season, from approximately mid-May to mid-July (Dixon, 1967; Hager, In press). At this time, the throat and much of the head is bright yellow. Also, reddish-orange pigmentation is deposited laterally on the body, from the shoulders and axillae posterior and including the rear limbs. The ventro-lateral black blotches do not appear to change with the development of breeding colors. Female H. maculata at WSNM 625 This content downloaded from 157.55.39.27 on Mon, 05 Sep 2016 05:46:39 UTC All use subject to http://about.jstor.org/terms