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1 Wing color and mating preferences of Heliconius sara Emily Loew Department of Zoology, University of Wisconsin Madison ABSTRACT Convergence in aposematic coloration of chemically protected butterflies, or Mllerian Mimicry, improves advertisement of unpalatability to predators. Heliconius sara (Heliconiinae) has two races in Costa Rica, each matching a different Mllerian model, one with and the other without a yellow stripe on the bottom edge of the hindwing. Color switching in Heliconius spp. is c ommon but may involve a conflict between natural selection for convergence to models and sexual selection for maintenance of the original color pattern. Here, I manipulate the color pattern of H sara to determine the degree to which sexual selection cons trains color pattern switching. This study was conducted in the Monteverde Butterfly Garden in Monteverde, Costa Rica and looked at mating behaviors of 75 Atlantic race H sara which have uniformly black hindwings. Newly emerged individuals were painted with a stripe of yellow or black on the bottom edge of the hindwing. Mating behavior was observed over 11 days. Males did not show a preference for female wing color for approach, chasing, courtship or rejection (Chi squared test, df = 3, p < 0.05). H owever, females seemed to prefer black painted males for approach, chasing and courtship (Chi squared test, df = 3, p < 0.05). If black is the ancestral condition, these results suggest that color pattern switching in H sara is constrained by female mate choice. RESUMEN La convergencia en la coloracin aposematic de mariposas quimicamente protegidas, y el mimetismo de Mllerian, mejora n la adverlencia de la pete alidad a los depredadores. Heliconius sara (Heliconiinae) tiene dos razas en Costa Rica, cada uno c pula con un diferente modelo de Mllerian, una con y la otra sin una raya amarilla en el borde inferior del a la oculta La conmutacin del color en Heliconius spp es comn pero puede implicar un conflicto entre la seleccin natural para la converge ncia a los modelos y la seleccin sexual para el mantenimiento del patrn original del color. Aqu, manipulo el patrn del color del H. sara para determinar el grado a el cual la seleccin sexual obliga el cambio del patrn del color. Este estudio fue con ducido en el jardn en Monteverde, Costa Rica de la mariposa de Monteverde observ los comportamientos de c pula del sara de la raza H. sara de 75 Atlntico, que tienen a la oculta uniformemente negros. Se pintaron a los individuos emergentes con una raya de amarillo o de negro en el borde inferior del a la oculta El comportamiento de acoplamiento fue observado sobre 11 das. Los machos no demostraron una preferencia por el color femenino del ala para los
2 comportamientos de acercamiento, perseguir, cortej o o rechazamiento ( Chi squared test, df = 3, p < 0.05) Sin embargo, las hembras pretieron preferir a machos pintados de negro para el acercamiento, perseguir y cortejo (Chi squared test, df = 3, p < 0.05) Si el negro es la condicin ancestral, estos resu ltados sugieren que el cambio del pa trn del color en sara del H. s a ra obligada por escogencia femenina de la cpu la INTRODUCTION Wing color and pattern in butterflies may serve in predator avoidance, male male interactions and social signals used during courtship (Silberglied 1989). Aposematic coloration warns predators of toxins or distastefulness (Gilbert 1983, Alcock 1984, Brower 1989). A type of mimicry produced when unpalatable species share the same aposematic coloring to protect themselves from predators is Mllerian mimicry (Gilbert 1982, Mallet et al. 1988, Turner 1989). Heliconius spp. (Leptidoptera: Nymphalidae) are well known for their differentiation of wing color patterns and multiple mimicry complexes including exceptional Mllerian mi micry within their species (Mallet et al. 1989, Jiggins et al. 2001, Jiggins et al. 2004, Kronforst et al. 2006). Heliconius melpomene and H. erato are two well recognized examples found in light gaps and secondary forests of the Neotropics that exhibit t his complex (DeVries 1987, Davidson et al. 1999, Flanagan 2004). Within populations in Central and South America color switching has led to 11 variations in wing patterns and in the same geographical locations the wing patterns are almost perfect mimics ( Turner 1981). Convergence of color pattern between H melpomene and H erato may not have been made without a cost. Butterfly fitness via mimicry is increased due to natural selection because they receive greater protection from predators, however it can decrease fecundity via sexual selection (Mallet et al. 1989). Sexual selection may constrain color convergence by favoring the original color pattern, even though natural selection through Mllerian mimicry causes convergence between models. Only rarely does mate choice evolve with mimicry, and when this is not the case, butterflies need to find a balance between natural and sexual selection (Jiggins et al. 2001). For these reasons sexual selection prevents new races from evolving, whereas natural selecti on allows the species to diverge into new color patterns. Heliconius sara is distinguished from similar species by its small size and a basal forewing bar that crosses the wing well inside the cell. According to DeVries (1987), Heliconius sara is separate d by the continental divide into two subspecies: H sara fulgidus on the Atlantic slope and H sara theudela on the Pacific slope. Heliconius sara theudela enters into a mimicry complex with H doris, H pachinus and H hewisoni while H sara fulgidus mim ics H cydno Therefore, Heliconius sara on the Atlantic side has a hindwing that is uniformly black, while the Pacific race has a yellow stripe on the bottom edge of the hindwing (see Figure 1). The question I am looking at is "What if the Altantic form were to evolve to the Pacific form?" Here, I examine the possible evolutionary conflict between natural selection for color convergence via Mllerian mimicry and mating disruption via sexual selection in H sara
3 Heliconuis sara fulgidus Heliconius sara theudela Figure 1. The two Heliconius subspecies observed in my study are Heliconius sara fulgidus found on the Atlantic slope and Heliconius sara theudela found on the Pacific slope of Costa Rica. MATERIA LS AND METHODS Study site This study was conducted between April 24 th and May 8th, 2007 in the Monteverde Butterfly Garden in Monteverde, Costa Rica. The garden area where observations were made was a 5 x 15 m area that contained the following Heliconius butterflies: H. sara, H. erato, and Dryas julia. The garden had a tin roof with two plastic panels along with thick plastic paneled walls to allow the filtration of ambient light. Screen panels are located on east and west side to allow air to circulate through the greenhouse. Dominant vegetation in the garden was Lantana camara (Verbenaceae), Stachytarpheta jamaicensis (Verbenaceae), Asclepias curvassivica (Asclepiadaceae) and Gurania spp. (Cucurbitaceae). There were also four hanging cups of L. camara cut stems with inflorescences infused with sugar water for food. The west end of the garden received full sun while the east end was mostly shaded. Procedure One hundred Atlantic H. sara fulgidus pupae were obtained by the Monteverde Butterfly Garden. The pupae were pinned in an enclos ed chamber until eclosure, where they were then placed in two separate butterfly enclosures containing a hanging cup of L camara inflorescences filled with sugar water as food. Doing so allowed their wings to dry and ke pt them from mating before I was able to paint their wings. Butterfly wings took approximately one day to dry, whereupon, I painted a yellow or black stripe on the bottom of the hindwing, corresponding to the wing color of H. sara theudela or H. sara fulg idus respectively using Sharpie Paint Pens (see Figure 2). In an effort to keep male and female wing colors even, wing color was determined upon how many of each color and sex had already been released
4 Figure 2. The two Heliconius sara races whom I painted the lower hindwing black or yellow in my experiment. Heliconius sara fulgidus (left) has a black stripe and H. sara theudela (right) has a yellow stripe. Though H. sara fulgidus has uniformly black hindwings, half of the indivi duals were given a black stripe to rule out behavioral changes caused by painting the butterflies. All butterflies were painted to rule out paint as a variable. Immediately after painting, wings were held open for approximately eight to ten minutes to all ow the paint to dry and avoid butterfly wings from sticking together, which would have killed them. Fifteen H. sara already living in the garden were left unaltered and interactions with them were noted but did not contribute to the study. Over the cours e of four days 75 butterflies were released into the garden; 19 females and 20 males were painted black while 18 females and 18 males were painted yellow. Behavioral interactions between H. sara were observed and noted for approximately three hours for 11 sunny days during midday, when H. sara are most active (including the four days the butterflies were released). Behavior was divided into five categories: approach, chasing, courtship, mating and rejection. Approach was considered a direct flight path of a male towards a female while chasing was defined as a male giving chase to a female. Courtship consisted of a string of interactions; the first being a male either giving chase to a female and forcing her to land on a leaf by the downbeat of his wings or by the male approaching a female already resting on a leaf; her wings may be open or closed. The second phase of courtship consisted of a male rapidly flapping his wings, creating a breeze towards the female (Crane 1955). A responsive female woul d also rapidly flap her wings in reply. Mating was defined to be when both sexes had wings closed in a typical daytime rest position facing opposite directions while in copula (Crane 1955). A mating pair was easy to observe since Heliconius stay in copul a for one to three hours (Thompson 2006). When a male approached or attempted to court with a female who raised her abdomen or flew directly away it was defined as rejection. RESULTS General Observations Females tended to prefer black males in all five categories. Male choice was determined by male initiated behaviors like approach, chasing and courtship where female choice appeared to be end in mating and rejection. In the approach category, 96
5 yellow male and 201 black male approaches towards both co lors of females, showed there is a significant trend of female preference towards black painted males, as shown in figure 3a (Chi squared one sample goodness of fit test, 2 = 33.5, df = 3, n = 237, p < 0.05). Figure 3b indicates that black painted males most often chase black painted females (Chi squared one sample goodness of fit test, 2 = 11.1, df = 3, n = 64, p < 0.05). In 375 observed courtships, 295 were black males courting either color female and 159 were solely black females with black males. T his result suggest in courtship, females prefer black males but males are not biased in their color preference of female wing color (Chi squared one sample goodness of fit test, 2 = 119.3, df = 3, n = 375, p < 0.05, Figure 3c). Black painted males are rejected more than yellow painted males by all females in this study. Yellow painted females rejected significantly more black painted males (23) than did black painted females (8) as seen in 3d (Chi squared one sample goodness of fit test, 2 = 23.1, df = 3, n = 39, p < 0.05). There was only one recorded mating therefore there was insufficient data for analysis. Overall interactions between both colored females and yellow males were substantially lower than those observed between black males (yellow = 20 6, black = 570). The only consistent overall trend is a female preference for black painted males which implies there is no male choice. Figure 3 Behavioral observations and comparison of hindwing color preference in Heliconius sara including ap proach (a), chasing (b), courtship (c) and rejection (d) taken over 11 days at the Monteverde Butterfly Garden, Monteverde, Costa Rica. H eliconius. sara sex and hindwing color are indicated by the x axis by male:female order and yellow (Y) or black (B).
6 Additional Observations Unpainted H. sara (those already in the garden before painted individuals were added) interacted with the painted H. sara throughout the observation period. Overall 19 approaches, four chases, 64 courtships, six matings and two re jections were recorded. Besides matings, there were no major trends between the interactions. It is interesting to note that all of the matings occurred between unpainted males and painted females (yellow = 4, black = 2). On one occasion several painted males consistently attempted to pull a mating female of mating position with another male. On several instances female H. sara resting in the same area would be approached and courted by one or more males of different hindwing colors. DISCUSSION Thes e results indicate that black is the preferred mating color for female H. sara while no mating color preference exists for male H. sara Mating behavior in butterflies is generally initiated by the male while the final decision for mate choice is determin ed by the female (Gage et al. 2002). My study supports this by observations that all approaches, chases and courtships were initiated by males, while rejections were determined by females. Perhaps females are soliciting the males by tactics that are und etectable by the untrained eye, which could attribute to disproportionate interactions with females between yellow and black painted males. According to Crane (1955) during courtship pheromones released by female butterflies can have a faint musky odor on ly detectable at very close range and difficult for an untrained person to detect. When at maximum excitement, the female can extrude two bulbous excrescences known as "stink clubs" near the junction of the penultimate and distal segments to solicit males Chemical and behavioral selection would enhance fitness by allowing a new wing pattern to succeed while sexual selection changes to favor the new color. A possibility is H. sara theudela with a black hindwing, is the primitive color morph. Implying H. sara fulgidus has lost the yellow hindwing via evolution to mimic H. cydno who is the equivalent to H. sara theudela on the Pacific coast. It is possible the yellow females prefer yellow males, although this is unknown. A future study involving the sa me experiment but with the Pacific form instead where they are paint black and yellow over the yellow hindwing strip, could give insight. If females still prefer the black males it would support my hypothesis that the Pacific form evolved later in spite o f sexual selection while females preferring yellow males would indicate sexual selection evolved to favor the new color because it is adaptive in light of Mllerian mimicry. Another suggestion is that the dark hindwing pattern of H. sara fulgidus in a m imicry complex with H cydno is the primitive wing color pattern and H. sara theudela has evolved by mimicking H. doris, H. pachinus and H. hewisoni (DeVries 1987) (see Figure 4). Previous studies suggest it is possible for sexual selection in Heliconius spp. to impede the evolution of new wing color patterns (Jiggins et al. 2001). Female mate choice of black hindwing would constrain the wing color and prevent sexual selection from diverging from the Atlantic wing pattern to the Pacific wing pattern. Th is in turn
7 may lead to the constraint of sex limited mimicry in males. Sex linked mimicry occurs when only one of the sexes in a species is mimetic (Gage et al. 2002, Thompson 2006), H. sara fulgidus H. cydno H. s ara theudela H. pachinus H. hewisoni H. doris Figure 4. The phylogeny of two Heliconius sara races with H. sara fulgiudus (left) and H. sara theudela (right) with their comimics (DeVries 1987). which is an example of extreme sexual select ion such as Papilio polyxenes asterius who models Battus philenor in a North American mimicry complex or Spereyia diana where female limited mimicry is seen (Krebs 1988, Codella 1989). Genetically between H melpomene and H erato there is a presence or absence of a mark on one of about eight single loci (Futuyma 1986). Due to the male contribution of wing color to their daughters, if the color allele is not on the sex chromosome then female selection of black males will result in black female offspr ing.
8 Although females preferred to be courted by black males, observations showed they were willing to be courted by yellow males as well. This indicates there is a chance for the Atlantic form to converge to the Pacific form in which case natural selectio n would have to be stronger and more beneficial than female selection in mate choice. In future generations the most adaptive response to convergence of natural selection would be for sexual selection to evolve and "catch up" for maximum fitness and fecun dity. Jiggins (2001) proposed that races do not just arise from geographical isolation, but rather the butterflies mimic the most abundant or unpalatable species in the area due to reproductive selective pressures. A classic example is the mimicry compl ex H. melpomene and H. erato where evolution has actually caused mimetic shifts leaving the butterflies in reproductive isolation W ing patterns have evolved a mimicry complex according to geographical range exhibiting sometimes the benefits of mimicry ou tweigh pressures from sexual and natural selection. It appears the evolution of mimetic patterns is a delicate balance between natural and sexual selection where the benefits of mimicry sometimes out weigh pressures from selection. ACKNOWLEDGEMENTS I would like to thank Jim Wolfe, Zach Gezon for taking the time to help sex the butterflies and answer my questions the Monteverde Butterfly Garden and its staff for assisting me and allowing me to conduct my study in their garden. Thank you to Cam Penning ton for countless hours help ing me to sex, paint and release the butterflies. I would also like to thank Alan Masters for advising me and assisting me in everything from ordering butterflies (which we f inally got) to finding resources to explaining everyt hing that I asked LITERATURE CITED Alcock, J. 1984. The Ecology of Antipredator Behavior Animal Behavior 10 :295 334. Brower, L.P. 1989. Chemical Defenses in Butterflies In: The Biology of Butterflies R.I. Vane Wright and P.R. Ackery, ed. Princeton University Press, Princeton, NJ, pp. 114 118. Codella, S.G. and Lederhouse, R.C. 1989. Intersexual Comparison of Mimetic Protection in the Black Swallowtail Butterfly, Papilio polyxenes: Experiments with Captive Blue Jay Predators Evolution 43(2):410 42 0. Crane, J. 1955. Imaginal Behavior of a Trinidad Butterfly, Heliconius erato hydara Hewitson, with special reference to the social use of color. Zoologica, pp. 177 180. Davidson, A., O.W. McMillan, A.S. Griffin, C.D. Jiggins, and J.L.B. Mallet. 1999. Behavioral and Physiological Differences between Two Parapatric Heliconius Species. Biotropica 31(4):661 668.
9 DeVries, P.J. 1987. In: The Butterflies of Costa Rica and Their Natural History. Volume I: Papilionidae, Pieridae, Nymphalidae Princeton Univers ity Press, Chichester, West Sussex, pp. 197. Flanagan, N.S., A. Tobler, A. Davison, O.G. Pybus, D.D. Kapan, S. PLanas, M. Linares, D. Heckel and W.O. McMillan. 2004. Historical demography of Mullerian mimicry in the neotropical Heliconius butterflies. Evo lution 26:9704 9709. Futuyma, D.J. 1986. The Evolution of Interactions Among Species. In: Evolutionary Biology D.J. Futuyma, Sinauer Associates, Inc., Sunderland, MA, pp. 482 504. Gage, M.J.G., Geoffrey, A.P., Nylin, S., and C. Wiklund. 2002. Sexual Sel ection and Speciation in Mammals, Butterflies and Spiders. Proceedings: Biological Sciences 269 (1507):2309 2316. Gilbert, L.E. 1982. Coevolution and Mimicry In: Coevolution D.J. Futuyma, ed. Sinauer Associates Inc, Sunderland, MA, pp. 263 272. Huheey, J.E. 1988. Mathematical Models of Mimicry. The American Naturalist, Vol. 131, Supplement: Mimicry and the Evolution Process (Jun., 1988), pp. S22 S41. (University of Maryland, College Park, MD) Jiggins, C.D., C. Estrada and A. Rodrigues. 2004. Mimicry an d the evolution of premating isolation in Heliconius melpomene Linnaeus. Evol. Bio. 17:680 691. Jiggins, C.D., R.E. Naisbit, R.L. Coe and J. Mallet. 2001. Reproductive isolation caused by colour pattern mimicry. Nature 411:302 305. Krebs, R.A. and West, D.A. 1988. Female Mate Preference and the Evolution of Female Limited Batesian Mimicry Evolution 42 (5):1101 1104. Kronforst, M.R., L.G. Young, D.D. Kapan, C. McNeely, R.J. O'Neill, and L.E. Gilbert. Linkage of butterfly mate preference and wing color p reference cue at the genomic location of wingless. Evolution 103:6575 6580. Mallet, J.L.B., and Turner, J.R.G. 1998. Biotic drift or the shifting balance did the forest islands drive the diversity of warningly coulored butterflies? In: Evolution on Isla nds P.R. Grant, ed., Oxford University Press, NY, pp. 390 403. Mallet, J., and N.H. Barton. 1989. Strong Natural Selection in a Warning color hybrid zone. Evolution 43(2):421 431. Rutowski, R.J. 1991. The Evolution of Male Mate Locating Behavior in But terflies. The American Naturalist 138 (5): 1121 1139.
10 Silerglied, R.E. 1989. Visual Communication and Sexual Selection Among Butterflies In: The Biology of Butterflies R. I. Van Wright and P. R. Ackery, ed., Princeton University Press, Princeton, NJ, pp. 207 223. Thompson, E. 2006. The effect of wing color on Heliconius melpomene mating behavior and its implications on the evolution of mimicry. CIEE Fall Semster 2006 Turner, J.R.G. 1981. Adaptation a nd Evolution in Heliconius: A Defense of NewDarwinism. Annual Review of Ecology and Systematics 12:99 121. Turner, J.R.G. 1989. Mimicry: The Palatability Spectrum and its Consequences In: The Biology of Butterflies R. I. Van Wright and P. R. Ackery, ed ., Princeton University Press, Princeton, NJ, pp. 207 223.
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El color del ala y las preferencias de apareamiento de Heliconius sara
Wing color and mating preferences of Heliconius sara
Convergence in aposematic coloration of chemically-protected butterflies, or Mllerian Mimicry, improves advertisement of unpalatability to predators. Heliconius sara (Heliconiinae) has two races in Costa Rica, each matching a different Mllerian model,
one with and the other without a yellow stripe on the bottom edge of the hindwing. Color switching in Heliconius spp. is common but may involve a conflict between natural
selection for convergence to models and sexual selection for maintenance of the original color pattern. Here, I manipulate the color pattern of H. sara to determine the degree to which sexual selection constrains color pattern switching. This study was conducted in the Monteverde Butterfly Garden in Monteverde, Costa Rica and looked at mating behaviors of 75 Atlantic race H. sara, which have uniformly black hindwings. Newly- emerged individuals were painted with a stripe of yellow or black on the bottom edge of
the hindwing. Mating behavior was observed over 11 days. Males did not show a preference for female wing color for approach, chasing, courtship or rejection (Chi- squared test, df = 3, p < 0.05). However, females seemed to prefer black painted males for approach, chasing and courtship (Chi-squared test, df = 3, p < 0.05). If black is the ancestral condition, these results suggest that color pattern switching in H. sara is constrained by female mate choice.
La convergencia en la coloracin aposemtica de las mariposas qumicamente protegidas, y el mimetismo de Mller, mejoran la advertencia de la inapetencia a los depredadores. Heliconius sara (Heliconiinae) tiene dos razas en Costa Rica, cada uno hace pareja con un modelo diferente de Mller, una con y la otra sin una raya amarilla en el borde inferior de las alas posteriores. La conmutacin del color en Heliconius spp. es comn, pero puede implicar un conflicto entre la seleccin natural para la convergencia con los modelos y la seleccin sexual para el mantenimiento del patrn del color original. Aqu, manipul el patrn del color del H. sara para determinar el grado en que la seleccin sexual limita el cambio del patrn de color. Este estudio se llev a cabo en el Jardn de Mariposas en Monteverde, Costa Rica y mire los comportamientos de apareamiento de 75 razas Atlnticas de H.sara, que tienen las alas posteriores de manera uniforme negro.
Text in English.
Warning coloration (Biology)
Color de advertencia (Biologa)
Tropical Ecology Spring 2007
Ecologa Tropical Primavera 2007
Mimetismo de Mller
t Monteverde Institute : Tropical Ecology