Abstract
The common buckeye, or Junonia coenia, is a butterfly species that demonstrates phenotypic plasticity in some populations but not in others. In populations in the Eastern United States, the ventral hindwing is tan in the summer and dark red in early spring and fall, but in populations in Southern California, this plasticity is drastically reduced and the ventral hindwing is tan throughout the year. It is currently unknown to what extent this color plasticity may be locally adaptive. Here, I investigate whether J. coenia wing color plasticity may play a role in thermoregulation, and whether this seasonal plasticity is associated with behavioral differences in the field. Using infrared imaging on red and tan North Carolina butterflies I show that autumnal red butterflies reach higher final temperatures than tan warm season butterflies. Furthermore, behavioral field experiments reveal that tan butterflies appear to be more active than red and wild-caught butterflies. Thus, I show that red wing phenotypes could be adaptive in cooler climates because they contribute to higher butterfly body temperatures, and I speculate that lower activity levels of red autumnal butterflies may help save energy when temperatures are lower and environmental conditions are more challenging.
Introduction
Many insects use environmental cues during development to ensure an optimal seasonal phenotype. This ability to express different phenotypes in response to environmental cues is known as phenotypic plasticity. Seasonal plasticity is common in butterflies; many species optimize both wing patterns and behavior in response to environmental conditions such as day length and temperature (Brakefield & Reitsma, 1991; Daniels, Mooney, & Reed, 2012; Nijhout, 2003; Smith, 1991). One such butterfly species is Junonia coenia, the common buckeye, a butterfly found throughout most of North America. Eastern populations of this species display seasonal phenotypic plasticity in wing coloration where ventral hindwings of adult butterflies are pale tan in the summer and dark red in the fall and early spring (Brakefield & Reitsma, 1991; Daniels et al., 2012). In J. coenia populations from North Carolina, ventral hindwing coloration is determined by both temperature and daylength cues during larval and pupal development. The tan phenotype is induced by long daylength and high temperature whereas the red phenotype is induced by short daylength and low temperature. Low temperature and short daylength have been shown to induce the red phenotype both separately and when combined (Smith, 1991). In Southern California populations of J. coenia, however, phenotypic plasticity is drastically reduced and ventral hindwing surfaces tend to be tan year-round, with little seasonal variation (Daniels et al., 2012). Currently, the adaptive significance of wing color plasticity in buckeyes is unknown. Two hypotheses have been proposed to explain wing color plasticity in this species: crypsis and thermoregulation. The crypsis hypothesis predicts that the darker phenotype could help the red butterflies blend in with a background of red autumn leaves to minimize predation (Daniels et al., 2012). The thermoregulation hypothesis suggests that the darker color of the fall phenotype could absorb and retain more heat from the sun when ambient temperatures are lower, while the lighter color of the summer phenotype could help reflect heat when ambient temperatures are higher.
Butterfly wings play various roles in butterfly thermoregulation, most notably through basking-facilitated heat absorbance or exchange. Most butterflies rely on basking in the sun to warm up to temperatures where flight, oviposition, courtship, and other behaviors necessary for survival are possible (Heinrich, 1993). Various basking positions are possible, such as dorsal basking, where the wings are open and the dorsal wing surfaces are exposed to the sun, or lateral basking, where the wings are closed and ventral wing surfaces are oriented towards the sun (Heinrich, 1993). Heat conduction from the most basal portions of butterfly wings leads to increases in body temperature when the butterfly is in the dorsal basking position. Wing position also influences convection of air around the wings and therefore affects body temperature—in the dorsal basking position, for example, warm air trapped under the wings warms the butterfly’s body (Wasserthal, 1975). Wing color itself has also been linked to thermoregulation in some butterfly species (Kingsolver, 1987; Van Dyck & Matthysen, 1998; Watt, 1968). The ventral basking position and increased ventral hindwing melanization are associated with increased final temperatures and faster heating rates in Colias butterflies (Watt, 1968). This link between increased melanization on the basal ventral hindwing and increased body temperature has also been observed in other pierid species (Kingsolver, 1987). Together, this body of research on pierids strongly links differences in wing coloration to thermoregulation. Thermoregulatory differences caused by wing coloration may also be related to differences in flight duration in Colias butterflies, and darker wing color has been linked to faster heating and different behavioral flight patterns in males of the satyrine butterfly species Pararge aegeria (Roland, 1982; Van Dyck & Matthysen, 1998). Seasonal plasticity in behavioral traits has been observed in other butterfly species—there are behavioral differences between dry and wet season-morphs in the tropical butterfly species Bicyclus anynana (Brakefield & Reitsma, 1991).
Here, I work to test the hypothesis that seasonal plasticity in J. coenia is linked to thermoregulation. A thermoregulatory benefit may be provided by the darker ventral hindwings of North Carolina (NC) J. coenia individuals in colder seasons. If J. coenia also spends time in a lateral basking position, the dark red wing surface could help the butterfly body reach warmer temperatures in a colder climate. The added thermoregulatory benefit of a darker wing surface may not be necessary in the summer. In Southern California (CA), however, different environmental conditions may render the evolutionary benefits of this phenotypic plasticity in ventral hindwing color insignificant or even maladaptive. It may be easier for the butterflies to reach temperatures necessary for flight in the warmer autumnal temperatures in CA than during cooler days in NC, so an additional evolutionary adaptation to assist in thermoregulation is perhaps unnecessary or too costly. To test the thermoregulatory effects of wing color plasticity, I examined whether red NC J. coenia individuals warm up faster and reach higher temperatures than tan individuals when warmed under an incandescent light under constant low temperature. I also observed behavior and temperature of red, tan, and wild-caught NC butterflies in North Carolina and red, tan, and wild-caught CA butterflies in Southern California at sunrise to determine whether red wing surfaces become warmer under natural conditions and whether behavioral differences are associated with alternate seasonal morphs.