Variation of Eye Size in Butterflies: Inter- and Intraspecific Patterns
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J. Zool., Lond. (2000) 252, 187±195 # 2000 The Zoological Society of London Printed in the United Kingdom Variation of eye size in butter¯ies: inter- and intraspeci®c patterns Ronald L. Rutowski Department of Biology, Arizona State University, Tempe, AZ 85287-1501, U.S.A. E-mail: [email protected] (Accepted 6 October 1999) Abstract Differences in behaviour, such as the mate-locating tactic, may favour the evolution of interspeci®c and intersexual differences in the structure of the visual system. This notion was tested by examining the relationships between eye size, body size, sex and mate-locating tactic in 16 species of butter¯ies. The 16 species were grouped in eight phylogenetically close pairs that differed in the mate-locating tactic displayed by the males. Eye size was characterized by eye surface area, which was estimated from a set of linear eye measurements made on 10 individuals of each sex in each species. The major ®ndings were that eye surface area was positively correlated with body size both among and within species, males have larger eyes relative to their body size than females, and after controlling for body size and phylogeny, interspeci®c differences in the mate-locating tactic of males does not explain interspeci®c variation in the size of male eyes or in the magnitude of sexual difference in eye size. The optical and behavioural consequences of variation in eye size with body size and sex will await a better understanding of how eye structure varies with size within and between species. Key words: eye size, butter¯ies, sexual dimorphism, body size, mate-locating tactic INTRODUCTION trolled for phylogeny) revealed that diurnal and visually hunting species have consistently larger eyes with more In arthropods, the shape and size of the compound eye ommatidia, greater binocular overlap and more well- in¯uences many features of the visual ®eld including its de®ned frontolateral acute zones than species that hunt dimensions, acuity and sensitivity. For example, the nocturnally using non-visual cues (Bauer & Kredler, ¯atter the surface of an eye, the ¯atter the array of facet 1993). lenses that gather light for the underlying photorecep- At the intersexual level, the eyes of male insects are tors and the smaller the angle between the optical axes typically larger and morphologically more complex than of adjacent facets. This means that the region of the those of females (e.g. Beersma, Stavenga & Kuiper, 1977; visual ®eld examined by a ¯attened part of the eye is Zeil, 1983). This sexual dimorphism is generally inter- more densely sampled and so is seen with greater acuity preted as the adaptive result of the critical role of the (Land, 1997). As for eye size, the area of the cornea will visual system in males in detecting mates and acquiring set limits on the relationship between the number and matings (Thornhill & Alcock, 1983; Land, 1989, 1990, size of facet lens (i.e. a larger eye can have more facets, 1997). For instance, male blow¯ies chase females at high larger facets, or both than a small eye), which will in speeds during courtship. This behaviour favours males turn determine the size of the visual ®eld, its overall with regions of the eye that are both morphologically acuity and the sensitivity of the eye. and neurally specialized for the in-¯ight tracking of An adaptationist's logic leads to the expectation that rapidly moving objects. Not surprisingly, male blow¯ies interspeci®c and intersexual differences in the character- have larger eyes than females with morphological istics of the compound eye which affect the visual ®eld modi®cations that enhance visual system resolution and should re¯ect differences in behaviour, life style and sensitivity in the frontal region (Land & Eckert, 1985). habitat preferences that make different demands on the In butter¯ies, males search for females visually and, visual system. This prediction has been well supported like blow¯ies, engage in rapid pursuit ¯ights when they (Horridge, 1977; Wehner, 1981; Land, 1989, 1990, 1997; ®nd them (Rutowski, 1991). In contrast, after mating, Warrant & McIntyre, 1992, 1993). As a relevant females ¯y about searching for non-moving oviposition example of interspeci®c differences, a comparative study sites using visual (Rausher, 1978; Prokopy & Owens, of 27 species of predaceous carabid beetles (not con- 1983) and chemical cues (Dempster, 1992). Given these 188 R. L. Rutowski Table 1. The species pairs, their taxonomic af®liations, the mean HFL and EESA (from the 10 individuals of each sex), and their categorization with respect to male mate-locating tactic. Superspeci®c taxonomy is based on Scott (1986). The letter in parentheses following each binomen is used to indicate this species in Fig. 3 HFL (mm) EESA (mm2) Subfamily Family (tribe) Species ,<,<Strategy (source) Hesperidae Hesperiinae Ochlodes venatus (A) 2.27 2.30 2.33 2.83 Perch (Dennis & Williams, 1987) Thymelicus lineola (B) 3.76 3.6 1.8 2.25 Patrol (Pivnick & McNeill, 1985) Papilionidae Papilioninae Papilio machaon (D) 5.64 5.48 5.38 5.92 Perch (Wickman, 1992a) (Papilionini) Papilio rutulus (E) 5.85 5.55 6.02 6.89 Patrol (Scott, 1975; R. L. Rutowski, pers. obs.) Lycaenidae Lycaeninae Polyommatus icarus (F) 1.88 1.92 1.01 1.26 Perch (Lundgren, 1977) (Polyommatini) Celastrina argiolus (G) 1.68 1.72 0.8 1.03 Patrol (Wickman, 1992a; R. L. Rutowski, pers obs.) Nymphalidae Nymphalinae Melitaea cinxia (H) 3.4 3.14 2.01 2.47 Perch (Wickman, 1992a) (Melitaeini) Melitaea diamina (I) 2.93 2.8 1.54 2.0 Patrol (Wickman, 1992a) Nymphalidae Nymphalinae Mellicta athalia (J) 3.1 2.9 1.74 2.22 Patrol (Wickman, 1992a) Eurodryas aurinia (M) 2.93 2.73 1.27 1.67 Perch (Wickman, 1992a) Nymphalidae Nymphalinae Issoria lathonia (N) 3.91 3.7 2.89 3.74 Perch (Wickman, 1992a) (Argynnini) Argynnis paphia (O) 5.17 5.04 4.89 5.78 Patrol (Magnus, 1950) Nymphalidae Satyrinae Pararge aegeria (P) 2.82 2.61 1.7 2.03 Perch (Davies, 1978; Wickman & Wiklund, 1983) Aphantopus hyperantus (Q) 3.0 2.76 1.4 1.87 Patrol (Wickman, 1992a) Satyridae Satyrinae Coenonympha pamphilus (R) 2.78 2.4 0.91 1.26 Perch (Wickman, 1992b) Coenonympha tullia (T) 2.95 2.63 1.04 1.49 Patrol (Wickman, 1992b) sexual differences in behaviour selection should favour have dramatic frontal acute zones (Sherk, 1978). Hence, eyes in male butter¯ies that are larger than those of I predict that male perchers should have larger eyes females. Larger eyes have either more facets, larger than male patrollers. Moreover, perching is unlike any facets or both, any of which will enhance the probability behaviour seen in female butter¯ies, while patrolling is of detection, recognition and tracking of small moving similar in many respects to the search for oviposition objects. Consistent with this expectation, Yagi & sites displayed by females. I predict, then, that the Koyama (1963) reported that male butter¯ies have sexual difference in eye size in perchers will be greater larger eyes than females, but they did not rigorously than that in patrollers. control for the sexual differences in body size that are Here, I extend Yagi & Koyama's (1963) observations common in this group or phylogeny (Rutowski, 1997). and test these predictions by examining species and However, does the speci®c tactic used by males to sexual differences in eye size among a group of 16 species search for mates affect eye structure? Male butter¯ies of butter¯ies that differ in male mate-locating tactics. use two main tactics to locate females: patrolling and Unlike previous comparative studies, an effort was made perching (for review, see Scott, 1974; Rutowski, 1991). here to control explicitly for body size and phylogeny. When males patrol, they ¯y about the environment This test was modelled after Wickman's (1992a) study searching for females mostly at nectar sources and that demonstrates a relationship between male mate- oviposition sites. When males perch, they remain sta- locating behaviour and wing size and shape in butter¯ies. tionary and wait for females to pass nearby. Females Again, the predictions examined were as follows. that pass nearby are seen and rapidly approached and (1) Within species, males should have larger eyes than courted. These two classes of strategies are expected to females regardless of the mate-locating tactic typical for make different sorts of demands on a male's visual the species. system. Perchers, I argue, should bene®t more from a (2) Males that use a perching tactic to locate mates large visual ®eld and one that is relatively high in acuity should have larger eyes than males that use a patrolling throughout to maximize the distance at which passing tactic. females, males and predators can be detected over a (3) The sexual difference in eye size should be larger in large range of arrival directions. A large and acute perchers than patrollers. visual ®eld can be achieved through having many large facets. In contrast, mobile patrollers will often be able to approach conspeci®cs closely at foodplants and MATERIALS AND METHODS oviposition sites and so may have high acuity more restricted to the forward facing part of the eye. In line The species and their behaviour with these expectations, dragon¯ies that perch when hunting have more uniform facet diameters across the Comparative tests of selectionist hypotheses about the eye than those that patrol while hunting, which tend to effects of behaviour on the evolution of morphology are Eye size in butter¯ies 189 Table 2. The eye and leg dimensions that were measured and used to calculate estimated eye surface area (EESA).