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Growth and Patterning Are Evolutionarily Dissociated in the Vestigial Wing Discs of Workers of the Red Imported Fire Ant, Solenopsis Invicta 1 1 2Ã JULIA H

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Growth and Patterning Are Evolutionarily Dissociated in the Vestigial Wing Discs of Workers of the Red Imported Fire Ant, Solenopsis Invicta 1 1 2Ã JULIA H JOURNAL OF EXPERIMENTAL ZOOLOGY (MOL DEV EVOL) 308B:769–776 (2007) Growth and Patterning are Evolutionarily Dissociated in the Vestigial Wing Discs of Workers of the Red Imported Fire Ant, Solenopsis Invicta 1 1 2Ã JULIA H. BOWSHER , GREGORY A. WRAY , AND EHAB ABOUHEIF 1Department of Biology, Duke University, Durham, North Carolina 2Department of Biology, McGill University, Montreal, Quebec, Canada ABSTRACT Over the last decade, it has become clear that organismal form is largely determined by developmental and evolutionary changes in the growth and pattern formation of tissues. Yet, there is little known about how these two integrated processes respond to environmental cues or how they evolve relative to one another. Here, we present the discovery of vestigial wing imaginal discs in worker larvae of the red imported fire ant, Solenopsis invicta. These vestigial wing discs are present in all worker larvae, which is uncommon for a species with a large worker size distribution. Furthermore, the growth trajectory of these vestigial discs is distinct from all of the ant species examined to date because they grow at a rate slower than the leg discs. We predicted that the growth trajectory of the vestigial wing discs would be mirrored by evolutionary changes in their patterning. We tested this prediction by examining the expression of three patterning genes, extradenticle, ultrabithorax, and engrailed, known to underlie the wing polyphenism in ants. Surprisingly, the expression patterns of these three genes in the vestigial wing discs was the same as those found in ant species with different worker size distributions and wing disc growth than fire ants. We conclude that growth and patterning are evolutionarily dissociated in the vestigial wing discs of S. invicta because patterning in these discs is conserved, whereas their growth trajectories are not. The evolutionary dissociation of growth and patterning may be an important feature of gene networks that underlie polyphenic traits. J. Exp. Zool. (Mol. Dev. Evol.) 308B:769– 776, 2007. r 2007 Wiley-Liss, Inc. How to cite this article: Bowsher JH, Wray GA, Abouheif E. 2007. Growth and patterning are evolutionarily dissociated in the vestigial wing discs of workers of the red imported fire ant, Solenopsis invicta. J. Exp. Zool. (Mol. Dev. Evol.) 308B:769–776. Pattern formation and growth are highly inte- (West-Eberhard, 2003). Analyzing the relationship grated and iterative processes that play key roles between pattern formation and growth in organ- during the development and evolution of organis- isms that have evolved to be polyphenic can help us mal form. There has been significant progress in to understand the ecological and evolutionary understanding how these two processes are devel- dynamics governing these two highly integrated opmentally coordinated (Milan, ’98; Nijhout, 2003; processes. Caste development in ants is polyphenic: Emlen and Allen, 2004; Crickmore and Mann, 2006; depending on environmental cues, a fertilized egg Emlen et al., 2006), and how changes in each can produce either a winged queen or a wingless individual process has contributed to evolutionary sterile worker. These cues are translated into change (Gould, ’77; Raff, ’96; Carroll et al., ’94, a physiological response through the activity 2001). We understand little, however, about how thesetwoprocesseschangerelativetooneanother Grant sponsor: FQRNT (Quebec Government); Grant sponsor: over evolutionary time or how they individually NSF; Grant number: DEB-0073278. respond during development to environmental cues. ÃCorrespondence to: Ehab Abouheif, Department of Biology, McGill University, Montreal, Quebec, H3A 1B1, Canada. Polyphenism, the ability of a single genome to E-mail: [email protected] give rise to alternative morphologies in response Received 7 May 2007; Revised 29 August 2007; Accepted 30 August 2007 to an environmental cue, is an ecologically Published online 25 September 2007 in Wiley InterScience (www. important and phylogenetically widespread trait interscience.wiley.com). DOI: 10.1002/jez.b.21200 r 2007 WILEY-LISS, INC. 770 J.H. BOWSHER ET AL. of juvenile hormone, which controls both queen the wingless castes. An ‘‘interruption point’’ is determination (Robeau and Vinson, ’76; Passera defined by the absence of gene expression in and Suzzoni, ’79) and worker caste in ants (Wheeler vestigial wing primordia. For example, a striking and Nijhout, ’81b; Ono, ’82; Wheeler, ’90). difference was found between the wingless castes A striking characteristic of ant caste polyphenism of different ant species in the expression of is the absence of wings in worker ants and their engrailed, a gene that defines the posterior presence in reproductives. The evolution of wing- compartment in the wing imaginal disc (Cohen, lessness in the worker caste is one of the main ’93). Engrailed is normally expressed in the factors contributing to the ecological and evolu- vestigial wing discs of the ant Pheidole morrisi, tionary success of ants in that it allowed a eusocial but is absent from the vestigial wing discs of insect to colonize the soil and rotting vegetation the ant Crematogaster lineolata and Formica in the ground (Holldobler and Wilson, ’90). In nitidiventris (Abouheif and Wray, 2002). Discover- contrast, the winged reproductive caste’s main role ing that the interruption points differ in the is mating and dispersal. In the case of Solenopsis wingless worker castes of different ant species invicta, females can fly up to 1,000 ft in the air and was unexpected because the wing polyphenism in as far as 12 miles before founding a nest (Vinson ants evolved just once (Wilson, ’87; Holldobler and and Sorensen, ’86; Taber, 2000). Such long flights Wilson, ’90). have undoubtedly contributed to their efficiency as One possible explanation for this unexpected an invasive pest (Taber, 2000). Although these divergence of interruption points between worker flights play a crucial role in the dispersal of castes of different ant species is that interruption S. invicta, virtually nothing is known about the points evolve when the worker caste demography development of wings in this pest species. evolves. Growth and patterning are considered As in other holometabolous insects, wings in related processes because a change in the size of a adult queen and male ants develop from imaginal worker ant and its wing discs will likely result in discs present in the larvae. Although workers are changes in the patterning of those discs. In the ant wingless as adults, the larvae of all species species C. lineolata, the size distribution of work- examined to date grow vestigial wing imaginal ers is monomorphic with a narrow size range, discs that disappear before pupation (Dewitz, meaning that all the workers within the colony are 1878; Wheeler and Nijhout, ’81a; Sameshima all of the same proportion and differ only slightly et al., 2004). The shape and size of these vestigial in size. In contrast, in the ant P. morrisi, the size wing imaginal discs are diverse. For example, distribution is completely dimorphic with two vestigial wing discs in the genus Crematogaster distinct castes, ‘‘soldiers’’ and ‘‘minor workers.’’ appear as two pairs of small and elongated These two distinct castes show a striking pattern epidermal invaginations (Wheeler and Nijhout, of allometry, meaning that the soldiers are ’81a), whereas in the genus Pheidole, they appear disproportionately larger than the minor workers as two large forewing discs in soldiers, and are (Wheeler and Nijhout, ’81a). Interestingly, Abou- small or completely absent in the minor workers heif and Wray (2002) found that the two mono- (Wheeler and Nijhout, ’81a; Abouheif and Wray, morphic species (C. lineolata and F. nitidiventris) 2002; Sameshima et al., 2004). Interestingly, with a narrow size distribution shared the same previous studies had failed to find worker vestigial interruption point, whereas the dimorphic species wing discs in S. invicta (Petralia and Vinson, ’80). (P. morrisi) was interrupted further downstream Variation in the size and shape of vestigial wing in the wing-patterning network. If the distribution discs in the workers of different ant species is of the worker caste plays an important role in the matched by the variation in the expression of the evolution of the shape and size of vestigial wing gene network underlying the wing polyphenism in discs and interruption points, then examining ants. Abouheif and Wray (2002) characterized the a species with a worker caste distribution that expression of six ant homologs of Drosophila genes is intermediate between the monomorphic and involved in wing-patterning, Ultrabithorax, extra- completely dimorphic species examined in Abou- denticle, engrailed, wingless, scalloped, and spalt, heif and Wray (2002), could reveal a novel during imaginal disc development in the winged relationship between the growth and patterning and wingless castes of four ant species. They of vestigial wing discs. discovered that this wing-patterning network is S. invicta workers have a very broad size conserved in the winged queens and males of these distribution with only the slightest sign of species, but is interrupted at different points in allometry between the largest and smallest workers J. Exp. Zool. (Mol. Dev. Evol.) DOI 10.1002/jez.b GROWTH AND PATTERNING OF WINGS IN FIRE ANTS 771 (Wilson, ’78; Wood and Tschinkel, ’81). This broad represented in the sample. By the third instar, rangeofworkersizeinS. invicta represents an reproductives are easily differentiated from work- intermediate type of worker caste demography. Thus, ers by their discs. The reproductive larvae have we predicted that growth and patterning of the much smaller discs for their overall body size than vestigial wing discs in this species should be different workers. from the growth and patterning of vestigial wing discs Statistical analyses were carried out using SY- in monomorphic and completely dimorphic species. STAT (Systat Software Inc., San Jose, CA). We In this study, we present the discovery and performed a ‘‘homogeneity of slopes’’ or ‘‘paralle- characterization of vestigial wing discs in worker lism’’ test to determine whether growth rates of S.
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