Reproductive interference between Nehalennia damselfly species Author(s) :Hans VAN GOSSUM, Kirsten BEIRINCKX, Mark R. FORBES, and Thomas N. SHERRATT Source: Ecoscience, 14(1):1-7. 2007. Published By: Centre d'etudes nordique, Universite Laval DOI: URL: http://www.bioone.org/doi/full/10.2980/1195-6860%282007%2914%5B1%3ARIBNDS %5D2.0.CO%3B2
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14 (1): -7 (2007)
Reproductive interference between Nehalennia damselfly species1 Hans VAN GOSSUM2, Department of Biology, Carleton University, 1125 Colonel By Drive, Ottawa, Ontario K1S 5B6, Canada, and Evolutionary Biology Group, University of Antwerp, Groenenborgerlaan 171, B-2020 Antwerp, Belgium, e-mail:
[email protected] Kirsten BEIRINCKX, Mark R. FORBES & Thomas N. SHERRATT, Department of Biology, Carleton University, 1125 Colonel By Drive, Ottawa, Ontario K1S 5B6, Canada.
Abstract: We tested the hypotheses that reproductive interference between 2 congeneric damselfly species influences their local population densities and the female morph ratios in one of the species. Nehalennia irene has 2 female types (andromorph and gynomorph), whereas N. gracilis exhibits only one female type. Andromorphic N. irene females not only resemble conspecific males in body coloration, but also resemble heterospecific females of N. gracilis. We predicted male N. irene to be most attracted to gynomorphs of N. irene and male N. gracilis to be least attracted to them. Further, if N. gracilis males harass andromorphic N. irene females excessively, then they may reduce andromorph frequencies of N. irene locally. Our results indicate hybridization to be prevented by a “lock-and-key” mechanism, but male N. irene often attempt mating with female N. gracilis. Contrary to prediction, andromorph frequency in N. irene did not depend on whether N. irene populations were in sympatry or allopatry with N. gracilis. As predicted, N. irene males attempted tandem formation most frequently with conspecific gynomorphs, while N. gracilis males made most heterospecific tandem attempts on N. irene andromorphs. Collectively, our results suggest that N. gracilis females may be frequently harassed by N. irene males, and that this may help explain the relative rarity of N. gracilis. Keywords: competition, harassment, insect community, mating interference, social environment. Résumé : Nous avons testé les hypothèses voulant que l’interférence au niveau de la reproduction de 2 espèces de demoiselles du même genre influence leur densité locale de population et les ratios de morphes femelles dans l’une des 2 espèces. Nehalennia irene a 2 types de femelles (andromorphe et gynomorphe) alors que N. gracilis présente un seul type de femelle. Les femelles andromorphes de N. irene ressemblent non seulement aux mâles de son espèce par la coloration du corps mais ressemblent aussi aux femelles de N. gracilis. Nous avons prédit que les mâles N. irene seront le plus attirés par le type gynomorphe des femelles N. irene et que les mâles N. gracilis seront attirés le moins par celles-ci. De plus, si des mâles N. gracilis harcèlent de façon excessive les femelles andromorphes N. irene, cela pourrait réduire localement la fréquence de ce type de femelles. Nos résultats suggèrent que l’hybridation est prévenue par un mécanisme de « relation clé à serrure » mais que les mâles N. irene essaient fréquemment de s’accoupler avec des femelles N. gracilis. Contrairement à notre prédiction, la fréquence du type andromorphe chez les femelles N. irene n'était pas affectée par le fait que si les populations de N. irene étaient en sympatrie ou en allopatrie avec N. gracilis. Tel que prédit, les mâles N. irene ont tenté de former des tandems plus fréquemment avec des femelles gynomorphes de leur espèce alors que les mâles N. gracilis ont fait le plus de tentatives inter-espèces sur des femelles N. irene de type andromorphe. L’ensemble de nos résultats suggère que les femelles de N. gracilis peuvent être harcelées fréquemment par des mâles N. irene et que ceci pourrait contribuer à expliquer la rareté relative de N. gracilis. Mots-clés : communauté d’insectes, compétition, environnement social, harcèlement, interférence d’accouplement. Nomenclature: Walker, 1953.
Introduction
Interactions among closely related, sympatric species can result in reproductive character displacement, that is, divergence in the signals, receiver selectivity, or other aspects of reproductive biology of the species (Waage, 1979; Howard, 1993). Selection favouring reproductive character displacement is thought to be particularly strong, at least locally, when low-quality hybrids are produced (Parris, 1999; 2001) and/or when the time and energy budgets of at least one species are adversely affected as a result of their interaction (Singer, 1990). In this way, reproductive interference may explain specific patterns of behaviour and 1Rec.
2005-12-20; acc. 2006-06-29. Associate Editor: Timothy T. Work. 2Author for correspondence.
morphological character variation and/or variation in population size and relative abundance of species (Kuno, 1992; Takafuji, Kuno & Fujimoto, 1997). We explored whether reproductive interference could affect female morph frequency and/or the relative abundance of 2 closely related species: Nehalennia gracilis and N. irene (Odonata, suborder Zygoptera). Nehalennia irene is distributed across Canada, whereas N. gracilis is restricted in Canada to Ontario, Québec, New Brunswick, and Nova Scotia (Walker, 1953). Both species frequent marshy areas with relatively dense vegetation; however, N. gracilis is confined to sphagnum bogs (Walker, 1953). The Nehalennia system is of particular interest from the perspective of reproductive interference because in one species, N. gracilis, females are monomorphic (see Walker,
Van Gossum et al.: Reproductive interference competition
1953), while the related species, N. irene, exhibits femalelimited polymorphism. Thus, in N. irene as with many other coenagrionid species (Cordero & Andrés, 1996; Fincke, 2004), one female morph (andromorph) is coloured and/or patterned similar to the conspecific male, while the other female morph (gynomorph) is dissimilar from the conspecific male. Nehalennia irene andromorphic females appear to resemble not only conspecific males, but also heterospecific females of N. gracilis, so there is potential for males of both species to attempt to mate with heterospecifics (see Methods for detailed species descriptions). Female-limited polymorphism in damselflies is genetically determined, at least for the five species that thus far have been studied (Andrés & Cordero, 1999; Sánchez-Guillén, Van Gossum & Cordero Rivera, 2005). Furthermore, recent studies comparing morphological (Monetti, Sánchez-Guillén & Cordero Rivera, 2002) and genetic variation (Andrés, Sánchez-Guillén & Cordero, 2000; 2002; Wong, Smith & Forbes, 2003) across sites or among populations support the view that the polymorphism is under selection. Current adaptive explanations assume that male harassment can reduce female lifetime reproductive success (Robertson, 1985; Sherratt, 2001; Fincke, 2004). If andromorphs are confused with males, then escaping from harassment by males may provide a selective advantage to andromorphs when they are initially rare in populations compared to males (Sherratt, 2001). Alternatively, or in addition, males may approach female morphs at a rate based on their prior experience with these morphs, which again could be beneficial for andromorphs when they are rare compared to gynomorphs (Miller & Fincke, 1999; Van Gossum, Stoks & De Bruyn, 2001a). Heterospecific interactions are relatively common among damselflies (Bick & Bick, 1981; Corbet, 1999), including amongst members of the same genus (Paulson, 1974; Robertson & Paterson, 1982; De Marchi, 1990; Forbes, 1991). Interactions between damselfly species may occasionally produce hybrids, but even in cases where they do not, such attention may lead to female injury and upset female time budgets. Thus, the selective benefits of a particular female morph may well depend on the local combination of conspecific and heterospecific interactions. Given that andromorphic N. irene females resemble not only conspecific males, but also heterospecific females, then one might expect that male N. irene would be preferentially attracted to N. irene gynomorphs over both andromorphs and N. gracilis females. We had opposite expectations for male N. gracilis: given the phenotypic similarity between its own females and andromorphic N. irene, male N. gracilis might be expected to show attraction towards andromorphs but little or no interest in gynomorphs of N. irene. Our general objective was to address the extent to which interspecific interactions between closely related Nehalennia species may be important in determining either species abundance and/or morph frequency. Our specific objectives were five-fold. First, we documented N. irene female morph frequencies at sites where N. gracilis was also present versus sites where N. gracilis was absent. We expected that if N. gracilis males were more attracted to N. irene andromorphs (which look similar to N. gracilis
females) than to gynomorphs, andromorph frequency in sympatric populations could be lower compared to populations in allopatry (because of interspecific harassment falling mainly on the andromorph). However, this prediction rests on the premise that harassment from male N. gracilis can be costly to andromorphs of N. irene. Secondly, we thus estimated the relative abundance of each species in sympatric populations as a proxy to estimating frequency of interspecific interactions. Third, we performed sequential presentations of N. gracilis females and N. irene females to both conspecific and heterospecific males to determine the nature of various types of interactions with females initiated by conspecific or heterospecific males. We did these presentations at one site where both species were sufficiently abundant. Thus, we could determine, experimentally, the intensity of sexual motivation of males of both species and their likelihood of engaging in misdirected sexual activity. Fourth, we noted whether males could successfully clasp con- and heterospecific females. Sometimes, heterospecific tandem formation is prevented because the male is unable to secure a firm grip on the pronotum of females (Paulson, 1974), a phenomenon analogous to a “lock and key”. Finally, we combined information on relative species abundance and male mate preferences to develop a simple model to estimate magnitudes of different con- and heterospecific interactions.
Methods Species descriptions We start by first describing males and females of both species in more detail, as their morphologies relate to our expectations of interspecific interactions. For males of N. irene (Figure 1a), abdominal segments nine and ten are blue with paired dark spots, whereas these segments are entirely blue in N. gracilis (Figure 1b). Andromorphic females of N. irene (Figure 1a and b) resemble the conspecific male’s coloration, i.e., blue with black dots on distal abdominal segments and blue on the same ventral body parts as the male. Gynomorphic N. irene (Figure 1a) are very differently coloured, with most body parts that are blue in conspecific males being yellow in these females. By contrast, N. gracilis (Figure 1b) females are monomorphic and appear very similar in colour to the andromorphs and males of N. irene. Notwithstanding this similarity in appearance, females of the 2 species can be distinguished by an experienced researcher with a 20× lens, based on the shapes of the hind margins of their pronota (Walker, 1953; Lam, 2004). Also, there is a very slight colour difference ventrally (Figure 1b): N. gracilis females are blue and whitish, compared to blue and yellowish in andromorphs of N. irene (Lam, 2004; see also Forbes, Richardson & Baker, 1995 for a detailed description of both female morphs of N. irene). Survey of species abundance and morph frequency Sites were located in Ontario and Québec, where both damselfly species are found. We sampled sites for numbers of males and females of both species. As mentioned, we first compared female morph frequencies of N. irene at sites with and without N. gracilis. In total, 17 allopatric and 4 sympatric sites were sampled for andromorph frequencies of N. irene. For the 4 sites in sympatry (Upper Fry Lake, Blackwater
ÉCOSCIENCE, vol. 14 (1), 2007
F igure 1. Picture of male and female Nehalennia damselflies: a) N. irene: male (1) on top, gynomorph female (2) in the middle, and andromorph (3) below; b) N. gracilis male (4) on top, N. gracilis female (5) in the middle, and N. irene andromorph female (3) below. Note the similarity in phenotype between the latter two female types.
Road, Lac St-Charles, Hebert’s Bog), we determined relative abundances of the 2 species. Our sampling occurred during June–July 2004 and was standardized. We walked slowly along the pond-margin while sweeping a butterfly net in a constant rhythm through the vegetation and making “∞-shaped” figures. Each netted individual was identified to species and sex. Female N. irene were further identified to morph. Each damselfly received a small black dot on one of its wings using a waterproof marker prior to release, in order to preclude recounting the same individual in subsequent sweeps. Because sweeping was done blind with respect to species we could use these data, excluding the few recaptures, as an indication of relative abundance of N. irene and N. gracilis. Presentation experiments Following this survey, one site (Hebert’s Bog) was selected where numbers of both N. irene and N. gracilis were sufficiently high to allow subsequent presentations of females of both species to males of both species. We did this using one-female presentation experiments. Females were
captured and, prior to their use, measured from the tip of their head to the end of their abdomen using digital calipers (accurate to 0.1 mm). Consulting Walker (1953), we did not expect to find large differences in size between females of the 2 species. Notwithstanding, we could assess whether the size of the female model influenced the likelihood of male reaction. Females were glued by their legs and head capsule to the bottom of a grass stem at a 30° angle. Such restrained females could not resist mating attempts, thereby allowing us to specifically evaluate male interest for the different female types. For each presentation, a perching male was located in the vegetation at Hebert’s Bog. We introduced the female model just lateral to a perched male (i.e.,
