Estimating the relative fitness of local adaptive peaks: the aerodynamic costs of flight in mimetic passion–vine butterfliesHeliconius

Abstract

In a related paper, we demonstrated that mimetic Heliconius butter£ies have converged in wing-beat frequency and degree of asymmetry in the wing motion, whereas sister species are dissimilar in these same traits. Warning signals of sympatric, distasteful species converge in evolutionary models in order to educate their predators more e¤ciently that the signal is associated with unpro¢table prey. Barring other constraints, the behaviours of the di¡erent co-mimetic pairs should ultimately converge on that behaviour which minimizes the energetic cost of £ight. We estimated the energetic cost of each mimic's £ight behaviour in order to predict the di¡erence in height of each ¢tness peak and the direction of convergent selection qualitatively. Following adjustments for body mass, mimetic Heliconius melpomene and Heliconius erato required more aerodynamic power than Heliconius cydno and Heliconius sapho. This di¡erence was attributed to the slower £ight speeds and higher wing-beat frequencies of H. melpomene and H. erato. Consequently, H. melpomene and H. erato expended more energy per unit distance per unit body mass than H. cydno and H. sapho. However, di¡erences in body mass may equalize energy budgets and stabilize the sympatric coexistence of the two pairs of co-mimics.

Discrimination of flying mimetic, passion–vine butterfliesHeliconius

“…However, morphological convergence in mimics may also result in wingbeat frequency convergence for reasons of aerodynamic force production (Srygley 1999). The higher wing-beat frequencies of the melpomene^erato group require greater aerodynamic power and thus they are energetically more costly than the relatively low wing-beat frequencies in the cydno^sapho group (Srygley & Ellington 1999).…”

Costs of dispersal

“… References: 1, Dixon & Kindlmann (1999); 2, Denno et al (1985); 3, Kisimoto (1956); 4, Dixon et al (1993); 5: Ahlroth et al (1999); 6, Fjerdingstad et al (2007); 7, Yano & Takafuji (2002); 8, Xiao et al (2007); 9, Ostergard et al (2007); 10, Greig (1993); 11, Traveset (1991); 12, Zagt (1997); 13, Fedriani & Manzaneda (2005); 14, Grimm (1995); 15, Silva & Taberelli (2001); 16, Young & Lockley (1988); 17, Bell et al (2005); 18, Cummings et al 1993); 19, Deblok & Tanmaas (1977); 20, Lundquist et al (2004); 21, Oliver & Retiere (2006); 22, Craig (1997); 23, Vahl & Clausen (1980); 24, Cheung et al (2006); 25, Vander Wall & Longland (2004); 26, Allen & McAlister (2007); 27, Hiddink et al (2002); 28, Hiddink & Wolff (2002); 29, Pechenik (1999); 30, Aukema & Raffa (2004); 31, Korb & Linsenmair (2002); 32, Srygley (2004); 33, Galeotti & Inglisa (2001); 34, Amo et al (2007); 35, Bonnet et al (1999); 36, Hamann et al (2007); 37, Jessop et al (2004); 38, Pietrek et al (2009); 39, Winne & Hopkins (2006); 40, Smallwood et al (2009); 41, Real & Manosa (2001); 42, Massemin et al (1998); 43, Kenward et al (1999); 44, Solomon (2003); 45, Soulsbury et al (2008); 46, Adamo et al (2008); 47, Srygley et al (2009); 48, Adamo & Parsons (2006); 49, Calleri et al (2006); 50, Bennet & Marshall (2005); 51, Crawford (1992); 52, Epp & Lewis (1984); 53, McHenry & Patek (2004); 54, Wendt (2000); 55, Combes & Dudley (2009); 56, Berrigan (1991); 57, Hedenstrom et al (2001); 58, Srygley & Ellington (1999); 59, Kram (1996); 60, Kramer & McLaughlin (2001); 61, Berrigan & Lighton (1994); 62, Full & Tullis (1990); 63, Duncan & Crewe (1993)…”

Wing Shape Variation Associated With Mimicry in Butterflies

“…Studies of Heliconius and other butterflies have previously demonstrated that locomotor mimicry may be achieved by kinematic (Srygley ; Srygley and Ellington ), aerodynamic (Srygley and Ellington ), and morphological effects (Srygley ). However, Srygley () found no evidence of convergence of wing shape between comimics, and suggested that this may be due to (i) conflicting selective forces operating on the wing; (ii) the evolution of dark apical margins contrasting against the bright colors of the wing, which can create false outlines to the wing that closely resemble those of the model species; (iii) a lack of sufficient selection pressure; or (iv) relatively imprecise measurements of wing shape.…”

“…Batesian mimics, which are not chemically defended, are also known to fly slowly and deliberately, so accurately resemble their model species in both their display patterns and locomotory behavior, but retain the wide thoraces and powerful flight muscles from their ancestry, allowing them to adopt more rapid and erratic flight behaviors when pursued by a predator (Chai and Srygley 1990;Srygley 1994Srygley , 2004. Srygley and Ellington (1999a) described a more subtle aspect of mimetic flight behavior in Müllerian mimic species: both wing-beat frequency and wing motion symmetry could be used to discriminate the comimics H. cydno and H. sapho from a second comimicry group, H. melpomene and H. erato. Although convergence on similar wing-beat frequencies may be related to requirements of aerodynamic force, variation from nearly sinusoidal to more asymmetrical wing motions is expected to have little effect on lift production.…”

“…Indeed, Bates (1862) suggested that mimicry in insects should extend to their physical motions, so a consequence of such selection may be a convergence of locomotory behavior as well as color patterning. In a study of wing motion in butterflies, Srygley (2007;Srygley and Ellington 1999a) found that this appears to be true for species of the genus Heliconius: two comimetic species, Heliconius cydno and Heliconius sapho, beat their wings more slowly and with a more symmetrical motion than their respective sister species, the comimics Heliconius melpomene and Heliconius erato. Because these features are more strongly determined by mimicry group than the lineage from which they derived, wing motion appears to be an important component of the overall mimetic signal and may serve to identify mimics before the predator can see details of the wing pattern (Srygley 2007).…”