Diversity of Anisoptera (Odonata): Infering speciation processes from patterns of morphological diversity1

Zoology 105 (2002): 355–365 © by Urban & Fischer Verlag http://www.urbanfischer.de/journals/zoology

REVIEW

Diversity of Anisoptera (Odonata): Infering speciation processes from patterns of morphological diversity** Bernhard Misof* Department of Entomology, Zoological Research Institute and Museum Alexander Koenig, Bonn, Germany

Summary With roughly 2500 described species Anisoptera are among the species-poor suborders within insects. However, morphological and ecological variability are truly impressive. Anisoptera are classified into about 15 families of variable species richness. In this analysis phylogenetic research is integrated with comparative approaches to investigate possible explanations of differential speciation rates within this suborder. A short review of phylogenetic work based on morphological characters is compared to published molecular phylogenies. Sistergroup comparisons are used to elucidate whether a) sexual selection, b) duration of life cycles, or c) differentiation in body size, have had a detectable effect on speciation rate. In all three analyses effects of distributional range and latitudinal distribution were controlled. These analyses suggest sexual selection promotes speciation and an increase in body size is positively correlated with speciation rate. The evolutionary significance of these results is discussed and experimental approaches that should advance our understanding of anisopteran diversity are suggested. Key words: molecular phylogeny, diversity, speciation rates, sistergroup comparisons

Introduction Anisoptera represent a comparatively species poor group of winged insects with slightly more than 2500 described species. Dragonflies are generally perceived as swift aerial predators, and the remarkable variety of common names in different societies confirms this observation. In Germany alone, 150 old common names are known, among them Teufelsnadel (Devil’s needle), Wasserhexe (water witch), and Höllenross (Goddess’ horse). Many equally exotic names are known in French, Swedish, and other European languages (the web is full of information on this topic, check also Corbet, 1999). The perception of dragonflies and in particular Anisoptera, differs tremendously between societies

of Asia and Europe. In Asian societies dragonflies enjoy a positive connotation associated with swiftness, strength, courage etc., in contrast to European societies where dragonflies are traditionally associated with evil properties, pain and danger (Corbet, 1999). Apparently these distinct perceptions are quite old and can be traced back at least to Roman times in Europe. The public perception of dragonflies demonstrates that dragonflies, and in particular Anisoptera, are easily identified without much biological knowledge. Scientifically, extinct and extant Anisoptera are clearly a monophyletic group supported by venational characters and structures of the secondary sexual apparatus (Tillyard, 1935; Fraser, 1957). Anisoptera show a morphological differentiation of fore- and hindwings and

*Corresponding author: Bernhard Misof, Department of Entomology, Zoological Research Institute and Museum Alexander Koenig, Adenauerallee 160, 53113 Bonn, Germany; phone: +49-228 91 22 296; fax: +49-228 21 69 76; e-mail: [email protected] **Presented at the 95th Annual Meeting of the Deutsche Zoologische Gesellschaft in Halle, May 20-24, 2002 0944-2006/02/105/04-355 $ 15.00/0

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have largely confluent eyes in many groups. These two easily recognizable features (among others) separates them morphologically from all zygopterous dragonflies. Larvae are without external abdominal gills and rely exclusively upon respiration via internal rectal gill filaments (Tillyard, 1935; Fraser, 1957; Corbet, 1999). The origin of Anisoptera was much debated since the early 20th century (for a review see Tillyard, 1935; Carle, 1982). Anisoptera are not directly related to the giant Carboniferous dragonflies. Carboniferous giants, like species of the genus Meganeura displaying a wing span of roughly 70 cm, represent an early offshoot of the Odonate lineage (Zessin, 1983; Brauckmann and Zessin, 1989). Compared to those ancient forms extant dragonflies are truly dwarfs. Species of the Protanisoptera have been considered stem group representatives of Anisoptera (see Carle, 1982), but morphological evidence clearly rules out this hypothesis. Wing constructions of Protanisoptera only superficially resemble extant anisopteran wings. The construction of the nodus and the absence of the discal brace clearly separates them from all extant dragonflies which are most likely monophyletic (see for example Carle, 1982; Bechly, 1996). In extant Odonata, species are classified into three suborders, the sometimes called damselflies, Zygoptera, the Anisozygoptera and the Anisoptera. Nel et al. (1993) proposed that the Anisozygoptera are paraphyletic in relation to the Anisoptera based mostly on venational characters. Except for the Epiophlebiidae, an extant genus with one species in Japan and one in the Himalayan region, the Anisozygoptera are all extinct. Consequently, the last remnant of the Anisozygoptera, the family Epiophlebiidae is the closest extant sister taxon to the Anisoptera.

Anisopteran diversity

the difference in species richness represents an artifact of taxonomy and not a real biological phenomenon. But this is in contrast to the number of newly described species in most families, which is comparable and in general remains low in odonates compared to other insect groups. Of course, new species will be described in the future, particularly from remote tropical areas, but I think that we have a good general representation of species numbers within Anisoptera. Thus, in Anisoptera, heterogeneous species richness is most probably a real biological phenomenon and deserves closer attention in evolutionary studies. Morphological variability is astonishing (Fig. 2). Larvae are adapted to semi-terrestrial life styles, active foraging in the water body, sit-and-wait hunters, sediment burrowers and some specialized forms to deep sediment burrowers (compare Corbet, 1999). Labial mask constructions as well as body shape show extensive specializations to these different ecological demands (see Tillyard, 1935). Larval development can take up to 6 years in some Petaluridae and Cordulegastridae and can be as short as 2–3 months in several libellulid genera. Larvae can be found in any fresh water system including temporary water bodies like tree holes in some rain forest species (Corbet, 1999). Morphological differentiation of imagines are most obvious in wing structures. Besides variation in venational characters, the functional significance of which remains poorly understood (Wootton, 1991), wing coloration varies from completely hyaline wings to beautifully colored appearances most prominently expressed in Chlorogomphidae and Libellulidae. Similarly, body coloration varies from a simple black and yellow pattern, as is also found in the Epiophlebiidae, to complex elaboration of all kinds of colors and metallic appearances. Sexual dimorphism can be extensive in body and wing coloration or be totally absent. Body size varies from 3 cm

Within Anisopera, species are classified into thirteen families of variable species richness depending on author (compare Carle, 1995; Bechly, 1996; Lohmann, 1996) (Fig. 1). Just three families, the Aeshnidae, Gomphidae and Libellulidae together constitute about 3/4 of the total number of anisopterous species. This heterogeneity is certainly not simply related to geological age. Gomphidae appear at 190 MYA (Bechly, 2002) and Petaluridae around 160 MYA (Nel et al., 1998). Aeshnidae (Wighton and Wilson, 1986) and Chlorogomphidae are known from 120 MYA old fossil beds (Bechly, unpubl.). Since 96 MYA Libellulidae appear in the fossil record (Nel and Paicheler, 1994). Despite similarly old fossil records, Gomphidae are species rich (roughly 813 species), and Petaluridae are species poor (9 species), likewise Aeshnidae are species rich (377 species) and Chlorogomphidae are species poor (27 species). Perhaps,

Fig. 1. Relative species richness among families of Anisoptera.

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wing span in some gomphid and libellulid taxa up to 18 cm wing span in giants of the families Petaluridae, Gomphidae, Aeshnidae, Cordulegastridae and Chlorogomphidae. Anisoptera inhabit all biogeographic areas even north of the polar circle and show their highest species density in the tropics. In all biotas, they are top insect predators, often in high abundance (Corbet, 1999). I have tried to give a short sketch of anisopteran diversity and its origin. Both phenomena, the astounding diversity and the doubtful root within extant dragonflies have baffled scientists for over a century and have triggered important taxonomic and biological investigations (for reviews see Tillyard, 1935; Fraser, 1957; Carle, 1982; Corbet, 1999). In 1935, Tillyard was able to state that odonates “.. stand as one of the best understood of all Orders of Insects, ...” (Tillyard, 1935, p. 2). However, our knowledge of phylogenetic relationships and evolutionary processes responsible for the genesis of this diversity is still in its infancy. We have no clear picture of phylogenetic relationships within families and an analysis of speciation processes has not been attempted at all. To account for the patterns of anisopteran biodiversity, explanations must include aspects of ecological and morphological variation as well as differential speciation rates. Of necessity explanations of biodiversity must have an evolutionary background without which our comprehension of diversity would be largely limited. Consequently, I will first briefly review the status quo of phylogenetic hypotheses and relate them to our own molecular work. This part will set the stage for a discussion of morphological novelties and variability. Finally, I will attempt explanations for increased speciation rates within Anisoptera. Because these analyses are only correlative, significant associations between species numbers and morphological characters can only

hint at underlying mechanisms. A causal analysis of mechanisms of speciation is not within the scope of this approach (compare Panhuis et al., 2001).

Phylogenies Within Anisoptera, phylogenies have been published based on morphological (Pfau, 1991; Carle, 1995; Lohmann, 1996; Trueman, 1996; Bechly, 1996; Bechly et al., 1998) and molecular characters (Artiss et al., 2001; Misof et al., 2001). Those phylogenies are, of course only partly congruent (Fig. 3). Rather than discuss the pros and cons of all published ideas I shall instead present a short overview of the most recently published phylogeny based on morphological characters (Bechly et al., 1998) and compare it to a recent molecular approach (Misof et al., 2001). I will not discuss possible homoplasies and homologies on which both phylogenetic analyses rely upon but instead will only present the topological congruencies and incongruencies among them. This overview is intended to give an idea of the unsolved questions in systematic research on Anisoptera. It is also intended to show that there is already enough phylogenetic information available to attempt analyses of character evolution and speciation processes.

Phylogenies based on morphological characters Bechly et al. (1998) based their morphological analysis on 40 wing characters, one larval mask and one head character. Seventeen wing characters had been treated as ordered. The reconstructed phylogeny shows all Anisoptera with spoon-shaped mask as a monophyletic

Fig. 2. Larval and imaginal anisopteran Diversity. The figure illustrates types of larval masks adapted to completely different modes of predation and illustrates differentiation in imaginal appearences. Zoology 105 (2002) 4

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group. This clade was already recognized by Carle as Libelluloidea (1995) and Bechly (1996) as Cavilabiata. It is, however, incongruent with Pfau’s analysis (1991). Pfau based his phylogenetic analysis on a detailed morphological investigation of secondary sexual organs and concluded that Petaluridae, Gomphidae and Cordulegastridae constitute a monophyletic sistergroup to the remaining Libelluloidea. Thus, he assumed the character spoon-shaped labial mask at least as plesiomorphic between Cordulegastridae and the remaining Cavilabiata. One particular species, Neopetalia punctata, will be of decisive importance in evaluating the monophyly of Cavilabiata. In his classification of Odonata (1957), Fraser combined all species of the genera Austropetalia, Archipetalia, Hypopetalia, Phyllopetalia and Neopetalia into one family, the Neopetaliidae, and recognized a closer association between the Neopetaliidae and Aeshnidae based on imaginal and larval characters. The larva of Neopetalia punctata was not known at this time. Carle and Louton (1994) first described it and had to conclude that this species has to be removed from the Neopetaliidae due to its libelluloid larva. The larva has a clear spoon-shaped labial mask and large toothlike proventricular lobes. The remaining species were combined in a new family Austroptealiidae (Carle and Louton, 1994; Carle, 1996). The analysis of an independent molecular data set will be a decisive approach to solve this question. In Bechly’s et al. (1998) analysis, Austropetaliidae and Aeshnidae form a clear monophyletic group and the Petaluridae and Gomphidae are at the stem of the Anisoptera-clade. Resolution at the stem is poor as only one extra step is enough to erase resolution between Petaluridae, Gomphidae and the remaining monophyletic groups. The position of the Petaluridae, Gom-

phidae and Austropetaliidae + Aeshnidae is one of the most debated problems in systematic research on Anisoptera. Pfau’s (1991) and Carle’s (1995) work include larval and imaginal characters, but their phylogenetic results are still inconclusive in relation to basal branching events. None of these analyses addresses phylogenetic history below the family level.

Phylogenies based on molecular characters Our molecular approach was designed to investigate the suitability of mitochondrial rRNA fragments for phylogenetic problems below and above the family level. We used a roughly 2000 bp long fragment and 42 representative species to reconstruct a phylogeny of the Anisoptera (Misof et al., 2001; Fig. 4). The monophyly of species classified into single families was confirmed and additionally, we were able to propose first phylogenetic hypotheses below the family level in several groups. The molecular data set was compatible with a monophyly of the Cavilabiata. The species Neopetalia punctata is clearly within the libelluloid clade and does not show any closer relationship to Austropetaliidae and Aeshnidae. Resolution of basal branching events was again poor. We have now sequenced a more exhaustive species selection and are able to adduce preliminary phylogenetic hypotheses within all major clades (Misof et al., in prep). Details of this analysis will be published elsewhere. Phylogenetic knowledge in all major branches is still far from being complete and in particular for basal branching events still dissatisfying. However, despite areas of low resolution, a pattern of branching events gradually emerges which calls for an interpretation.

Fig. 3. Comparison of previously published phylogenies. The figure sketches four selected hypotheses in a simplified version. Several of the newly erected families, for example Neopetaliidae, Chlorogomphidae, and Austropetaliidae are not shown in these diagrams. It becomes clear that only the sistergroup relationship of Corduliidae and Libellulidae has not been debated.

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Character complexes: Color patterns, sexual dimorphism and body size A comprehensive discussion of morphological variability and related evolutionary explanations is certainly beyond the scope of this paper. For a detailed analysis of morphological variability of imaginal characters see Carle (1995) and Fraser (1957). I will concentrate on selected character complexes that display evolutionary modifications within several monophyletic groups. Three character systems deserve special attention: the evolution of elaborate color patterns, the evolution of sexual dimorphism, and the differentiation of body size. Starting from a basic color pattern of yellow markings on black, which is present in Epiophlebiidae, eyecatching derivatives have evolved in many families, predominantly in Aeshnidae, Gomphidae, Corduliidae s.l., and Libellulidae. In aeshnids complex patterns of blue, green and yellow markings seem to have evolved several times independently. Dull brownish body colors are present in Gynacanthinae, tropical rain forest species, and some Telephlebiinae and Brachytroninae. In Gomphids the basic yellow on black markings is modified to yellow, green and brownish patterns with variable extensions. Many Corduliids show a very con-

spicuous metallic body coloration and complex wing color patterns in some genera. In many cases the evolution of derived color patterns coincides with the evolution of sexual dimorphism. All Anisoptera show sexual dimorphism in body weight (Corbet, 1999). Females are heavier and more stout than males as it is often the case in insects. Many Anisoptera display sexual dimorphism in hind wing structures which is apparently lost in some Aeshnidae and Cavilabiata groups. Males typically display a so-called anal angle on hind wings which correlates with the expression of orelliets on second abdominal segments. Together both characters are thought to have functional importance in copulation. In Zygoptera and Anisozygoptera this character is absent. Sexual dimorphism in body coloration can be found in Aeshnids, Gomphids and Libellulids. This is particularly obvious in Aeshnids, Gomphids and Libellulids. The most astounding instances of sexual dimorphism are found in the extremely heterogeneous Libellulidae. It is unclear whether sexual differentiation in Libellulids has evolved several times independently or whether it is a basic character complex for this family. Clear sexual dimorphism of wing coloration occurs in Chlorogomphidae, some Libellulidae and to a lesser extent in Corduliidae s.l. (Tillyard, 1935). However, many species do not show sexual differentiation. Mapping sexual dimorphism in wing and body coloration on a consensus tree of morphological and molecular results implies that both features are independently derived within several families of Anisoptera. Wing span as a measure of body size varies tremendously within families, especially in Gomphids and Libellulids. There is no clear recognizable phylogenetic pattern in this variation. Variance in body size is most likely related to ecological differentiation and/or interspecific interactions, which are frequently observed in Anisoptera. Derived character states in color patterns, sexual dimorphism, and body size, are remarkably often found in species rich clades which suggests a positive correlation of these features with speciation rates.

Gaining statistical power: Sistergroup Comparisons

Fig. 4. Molecular phylogeny based on mitochondrial rRNA genes. Phylogeny is based on a roughly 2000 bp long fragment of the mitochondrial rRNA genes (for details see Misof et al., 2001). Zoology 105 (2002) 4

It is fairly straightforward to count species numbers, but it is not at all trivial to tell whether a strong heterogeneity of species richness among groups is due to stochastic effects or is in need of an evolutionary explanation. Several authors have already stressed the fact that a constant speciation rate with stochastic variation will equally likely generate every possible relative species richness between sistergroups (for example Farris, 1976; Slowinski and Guyer, 1989, 1993; Maddison and Slatkin, 1991; Sanderson and Donoghue, 359

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1994). This still holds if constant extinction rates are included in the model (Slowinski and Guyer, 1993). This level of model complexity is important since we can only record net speciation rates in extant taxa. Relating an evolutionary novelty to an increased net speciation rate within one single taxon does not tell us anything at first hand. To infer possible mechanisms responsible for what we see in extant species multiple sistergroup comparisons are required to achieve statistical power. Phylogenetic contrast or sistergroup comparisons introduced by Felsenstein (1985) (reviewed in Martins and Hansen, 1996) can provide such a frame work within which meaningful analyses of net speciation rates become feasible. For example, Slowinski and Guyer (1993), Baracclough et al. (1995, 1999), Owens et al. (1999) and Arnqvist et al. (2000), have successfully used sistergroup comparisons to show that sexual dimorphism can be correlated with an increased net speciation rate in vertebrates and invertebrates. Furthermore, Arnqvist et al. (2000) showed that sistergroup comparisons that encompass comparisons between taxonomic groups of higher order are less reliable, because signals for potential correlates between characters and speciation rates become blurred with phylogenetic distance. Therefore, our comparisons are restricted to the genus or subfamily level. I searched for sistergroups of heterogeneous species counts regardless of character states. This approach guarantees that the selection of sistergroups will not be biased towards the evolutionary hypothesis under consideration. I relied on Bechly’s updated phylogenetic system (Bechly, unpubl.) and additional molecular data where morphological data were inconclusive. In several cases I had to use exclusively morphological or molecular information depending on the resolution of the data sets. The choice of possible sistergroups is certainly still a major weakness of the analysis. In several occasions I had to rely exclusively on taxonomic judgement, for example, I compared the genera Chlorogomphus and Chloropetalia, which are morphologically clearly distinct, or the genera Parazyxomma and Zyxomma as the most likely sistergroups within the Zyxommatinae. However, the uncertainties of phylogenetic relationships will most likely not bias the results of the comparative analysis since errors will be equally well distributed. If the sistergroup assignments are not totally wrong, the high error rate will at most blur the significance of the results.

Correlative analysis Several potential character complexes have been proposed to correlate with increased speciation rates. Ecological potential or speciation via ecological differenti360

ation has been proposed as a driving force in speciation (Mitter et al., 1988; Farrell, 1998; Baracclough et al., 1999; Schluter, 2001). Other well known hypotheses include the sexual selection hypothesis which assumes that sexual selection promotes speciation in allopatry and sympatry (for example Owens et al., 1999; Arnqvist et al., 2000; Panhuis et al., 2001; Barraclough and Nee, 2001). Another famous hypothesis predicts that a decrease in generation time promotes speciation (see Owens et al., 1999) and a related hypothesis assumes that a decrease in body size is correlated with an increase in speciation rates (for example Hutchinson and MacArthur, 1959; Brown, 1997; Owens et al., 1999). In this study, I tested for a positive correlation for the last three character complexes with speciation rates. Results were controlled for distributional range since an increase in areal distribution will always be potentially associated with a higher species count. Ranges of taxa were scored by using distributional information from Steinmann (1997) for each species and only biogeographic areas like Nearctis, Neotropis or Ethiopis were considered. The number of occupied biogeographic areas was used to estimate the distributional range of taxa. Likewise, the results were controlled for latitudinal distribution, which can have a strong effect on sistergroup comparisons. Dragonfly species richness appears much higher in the tropics compared to temperate areas, as it is the case for many other taxonomic groups (see Cardillo, 1999). Taxa were scored as either temperate zone (1) or tropically centered (2), or of mixed distribution (3). Cosmopolitan taxa were excluded from the analysis. Wilcoxon signed rank tests were performed and two tailed probabilities tested throughout. In each test, species count was the dependent variable and characters (dimorphism, voltinism, body size) the independent variables. In the first tests (sexual dimorphism) the a priori prediction was that an increase in the independent variable will be correlated with an increase in species richness. In the following two tests (size, voltinism) the a priori prediction was a negative association between independent and dependent variable.

Does sexual selection promote speciation in Anisoptera? Sexual dimorphism is usually associated with intraand/or intersexual selection. Therefore, I used sexual dimorphism as a sign for the presence of sexual selection processes in sistergroup comparisons. Sexual dimorphism in Anisoptera is apparent in body weight, secondary sexual organs, body coloration, and wing coloration. Differential body weight (females are larger Zoology 105 (2002) 4

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and heavier than males) and differential expression of secondary sexual organs are found in all Anisoptera. Thus, these character complexes are unlikely to have an influence on heterogeneous species counts among taxa and were excluded from the comparative analysis. For this investigation body coloration and wing coloration were the two most promising character complexes. Dimorphism in body and wing coloration varies continuously among taxa. Differential wing coloration varies from slightly brownish winged females and hyaline winged males, for example in many Corduliids, to clearly different wing colors and patterns between sexes, for example in several Libellulids and Chlorogomphids. However, differential wing coloration between sexes is less pronounced than dimorphism in body coloration. Sexual differences in body coloration vary from gradual to clearly contrasting patterns and colors in Aeshnids, Gomphids, and Libellulids. I scored sexual dimorphism as no sexual dimorphism in coloration (0), gradual dimorphism (1) or strong dimorphism in either wing or body coloration (2). If there was variance in character expression within a genus or taxon I scored an average. This is certainly a simplification of the actual situation, but will not bias the analysis due to its stochastic effect. I compared all sistergroups in which I found differences in sexual dimorphism. I identified eight contrasts in which sexually dimorphic species were sister taxa to sexual monomorphic species (Table 1). Species numbers in these contrasts confirmed the expectation of a positive correlation of sexual dimorphism and species numbers except in two cases. Sexual dimorphism was significantly correlated with relative species richness (Wilcoxon signed rank test, p = 0.05, n = 8). Relative distributional range in those contrasts was not correlated with relative species richness (Spearman rank correlation, p > 0.2, n = 8), demonstrating that relative distributional range does not enhance the effect of sexual selection on relative

species richness. The average number of occupied biogeographic areas of sexually dimorphic species was 4.5 (± 3.15 SD), the average number of monomorphic species was 1.2 (± 0.52 SD). Although, there is a clear difference between the distributional range of dimorphic and monomorphic species (Table 1), this difference was not significant (Wilcoxon signed rank test, p > 0.05, n = 8). Relative distributional range cannot explain relative species richness in these comparisons. Likewise, latitudinal effects were irrelevant in these contrasts. Except for two contrasts, the relative latitudinal distribution was 1 (Table 1). Consequently, latitudinal distribution can not enhance the relationship between sexual dimorphism and species numbers. Size was not a confounding variable in these contrasts. The average size of sexually dimorphic species was 2.19 (± 0.76 SD), the average size of monomorphic species was 2.19 (± 0.76 SD). The difference between both was not significant. However, relative size and relative species richness were highly correlated in these contrasts (Spearman rank correlation, p < 0.02, n = 8). Increasing relative body size enhanced the effect of sexual dimorphism on species numbers. There were not enough data available to test whether voltinism might be a confounding variable. In summary, sexual dimorphism was positively correlated with relative species richness independent of size, distributional range and latitudinal effects. Relative size and relative species richness correlate suggesting that an increase in body size has an additional effect on net speciation rate. There was no obvious evidence that extinction rates are different between dimorphic and monomorphic groups. Thus, sexual selection seems to promote speciation in Anisoptera. Discussion on sexual selection as a key engine of speciation is usually focused on the evolution of female mating preferences, which can, at least theoretically, promote speciation in allo – and sympatry (see Panhuis et al., 2001). Experi-

Table 1. Relative sexual differentiation and species numbers in pairs of sistertaxa. Dimorph

#

DR

LD

BS

Monomorph

#

DR

LD

BS

Zyxomma Zygonyx Zenithoptera Brachidiplacini Chlorogomphus Gomphini Anacini Caliaeschna

6 20 3 115 26 384 31 2

5 4 1 2 2 5 10 5

3 2 3 2 2 2 2 2

2 3 1 1.5 3 2 3 2

Parazyxomma Olpogastra Diastatops Tetrathemistini Chloropetalia Octogomphini Polycanthagynini Boyeria

1 4 7 82 1 59 2 5

1 1 1 2 1 5 2 2

3 3 3 2 2 2 2 1

2 3 1 1.5 2 2 3 3

# species numbers DR distributional range LD latitudinal distribution BS body size Zoology 105 (2002) 4

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mental evidence in calopterygid damselflies (CórdobaAguilar, 2002) has revealed that female choice plays a significant role in mating systems. However, experimental evidence for female mating preferences in Anisoptera is lacking. It is even not clear whether sexual ornamentation in males displays significant variability from which female choice might profit. Investigations of ornament variability within clearly sexually dimorphic species would be a fruitful enterprise. The analysis of pre- and postzygotic reproductive isolation will be an important step towards disentangling the influence of sexual selection on speciation processes. If sexual selection is a driving force in speciation, prezygotic isolation should develop before any signs of postzygotic isolation are detected in closely related species groups. Otherwise prezygotic isolation could be a secondary phenomenon of reinforcement. Combat is a commonly observed phenomenon in Anisoptera, even interspecific combat, and mostly directed towards territorial gain (Corbet, 1999). The consequences of combat can be severe and lead to the death of fighters (Corbet, 1999). It can not be excluded that intrasexual selection is the driving force in the divergence of sexual differentiation and speciation instead of intersexual selection. Experimental approaches are definitely warranted. Siva-Jothy and colleges (Simmons and Siva-Jothy, 1998; Siva-Jothy and Hadrys, 1998) investigated sperm competition and mating behavior in libellulid and aeshnid dragonflies. They demonstrated that the investigated libellulid dragonflies are highly promiscuous and have developed elaborate mechanism of sperm removal. This will likely hold for other dragonfly species as well, but has not been directly studied. Polyandrous mating systems can lead to sexual conflict, a special form of sexual selection, and in consequence promote speciation (Arnqvist et al., 2000), even in cases of missing sexual differentiation. It will be worthwhile to address this problem within Anisoptera. Unfortunately, no data are available on mating behavior for species rich groups like Gomphids and Corduliids.

Do short life cycles promote speciation in Anisoptera? A classic hypothesis predicts that short life cycles promote speciation (Hutchinson and MacArthur, 1959; Brown, 1997). The number of generations per year varies tremendously among dragonfly taxa. A naive glimpse at anisopteran variability suggests that short life cycles are indeed associated with species richness. Remarkably short life cycles can be found in Aeshnidae and Libellulidae which are among the most species-rich clades. I compared species counts of sistergroups which 362

differ in this life cycle parameter. Short life cycles were predicted to be associated with higher species counts. Data were scored as years per generation. We relied upon data on life cycle duration collected by Corbet and Suhling (unpubl. data). If there was variance within a taxon, the average year per generation time was recorded. I identified 13 contrasts in which generation time varies between sister groups (Table 2). However, of those 13 contrasts, only 7 show the expected correlation. There was no significant relationship between voltinism and species numbers (Wilcoxon signed rank test, p > 0.05, n = 11). Thus, contrary to the expectation, short life cycle duration is not related to rates of speciation in Anisoptera.

Does small body size promote speciation in Anisoptera? I expected species richness to be positively correlated with small body size as seen in studies on birds (see Brown, 1997). I relied on wing span as a measure of body size. Size was categorically scored as small (wing span up to 4 cm) (1), medium (species from 4 to 7 cm) (2) and large (wing span beyond 7 cm) (3). Again, if there was variance within taxa the average value for that taxon was recorded. Data was extracted from revisions or local checklists. In some cases I had to rely on secondary information mostly drawn from Fraser’s classification of Odonata (1957). In 11 cases sistergroups showed a clear difference in size classes (Table 3). In those contrasts size was positively correlated with species richness (Wilcoxon signed rank test, p < 0.001, n = 11). Distributional range (p > 0.05, n = 6), latitude (p > 0.05, n = 4) and sexual dimorphism (p > 0.05, n = 4) were not confounding variables (Table 3). The effect of increasing size on species number was therefore not enhanced by distributional ranges (Spearman rank correlation, p > 0.05, n = 11). However, relative species richness and relative latitudinal distribution were highly correlated (Spearman rank correlation, p < 0.01, n = 11). The correlation of size and species richness therefore appears stronger in tropical areas. In summary, contrary to the expectation, increasing body size appears to enhance net speciation rate in Anisoptera. A plausible interpretation of this phenomenon is not easy. Perhaps size differentiation, as a form of ecological differentiation, is common and extinction rates are higher in small, less vagile forms. Larger species possibly suffer lower extinction rates by better accommodations to climatological shifts. Higher extinction rates in small forms could also be due to differences in larval habitat selections. It certainly makes a Zoology 105 (2002) 4

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difference whether temporary pools or permanent water systems are selected for larval development. A direct experimental approach would be the analysis of metapopulation dynamics in closely related size differentiated species.

Problems Phylogenies are only hypotheses based on current knowledge. Reconstructions of character evolution depend on robust phylogenies and do not represent independent hypotheses. Therefore, they are only as good as the underlying phylogeny. In Anisoptera reconstruction of character evolution still suffers from an insufficient resolution in basal branching events. Current families appear to represent valid monophyletic groups, maybe with the exception of the Corduliidae s.l., based on morphological and molecular evidence. However, the reconstruction of major morphological transitions, like the evolution of secondary sexual organs and the evolution of larval body plans will have to await additional data and analysis. A combination of molecular and morphological data will greatly enhance our knowledge in this field. Speciation is a consequence of evolutionary processes. It leads to the establishment of genetically isolated populations maintained by adaptive or nonadaptive character complexes. Speciation rates do vary between clades, however, the significance of this phenomenon is not easily understood. I tried to address this problem by searching for characters covariing with speciation rates and found that sexual selection and large body size could promote speciation. Several potential problems

Table 2. Voltinism and species numbers in pairs of sistertaxa. Taxon

Y/G

#

Taxon

Y/G

#

Palpopleura Celithemis Orhemis Hemistigma Hemicordulia Somatochlora Sieboldius Onychogomphus Stylogomphus Austroaeschna Gynacantha Nasiaeschna Tanypteryx

0.33 0.75 0.33 0.33 1.5 3.5 2 2.25 2 2 0.75 1 4.5

6 9 15 2 34 41 5 67 8 17 86 1 2

Perithemis Leucorrhinia Libellula Uracis Procordulia Cordulia Hagenius Ophiogomphus Lanthus Planaeschna Limnetron Brachytron Uropetala

0.75 2 1.5 1 4 4.5 5 2.5 2.5 4 2 2 5.5

13 16 30 7 13 2 3 23 4 5 1 1 2

# species numbers Y/G years per generation

have to be kept in mind. The analyses rely on number of described species. However, taxonomists might tend to overlook species in sexually monomorphic forms. Differentiation in sexual characters is often preserved even in collected material, whereas ecological differentiation is usually not. Correlations are not causal relationships. If significant covariation of certain character complexes and speciation rates are present we can certainly conclude that there is evidence for a possible causal relationship. Our conclusions will be further strengthened by controlling for additional confounding variables. The observed diversity differences among extant taxa are a product of both speciation and extinction. Without

Table 3. Body size and species numbers in pairs of sistertaxa. Taxon

#

BS

SD

DR

LD

Taxon

#

BS

SD

DR

LD

Zygonichina Diastatops Cordulephya Chlorogomphus Cordulegastridae* Heliogomphus Boyeria Aeschnophlebia Oligoaeschna Austropetaliidae* Lindenia

26 7 4 26 29 19 5 5 21 5 1

3 1.5 2 3 3 2 3 3 2.5 3 3

2 0.5 0 2 0 0.5 0.5 1 0 0 0

4 1 1 2 2 2 2 1 3 1 1

2 2 2 2 1 2 1 1 3 1 1

Onychothemistina Zenithoptera Neophya Chloropetalia Zoraenidae* Microgomphus Caliaeschna Brachytron, Nasiaeschna Gomphaeschna Archipetaliidae* Melanocacus

5 3 1 1 3 13 2 2 2 1 2

2 1 1 2 2 1 2 2 2 2 2.5

0 2 0 0 0 0.5 2 1 0 0 0

2 1 1 1 1 2 5 2 1 1 1

2 2 2 1 1 2 3 1 1 1 2

* Bechly (2002) treats them as families, other authors not, for example Carle (1995) # species numbers DR distributional range LD latitudinal distribution BS body size SD sexual dimorphism Zoology 105 (2002) 4

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an excellent fossil record we can not say much about net speciation rates, which as a consequence constrains our possibilities of excluding alternative explanations of speciation rates. Approaches that enable us to differentiate between speciation and extinction phenomena will greatly enhance our understanding of extant biodiversity. Nee et al. (1994) have developed a promising approach using molecular sequence data. Since larval and imaginal life style are ecologically well separated, speciation processes can potentially be driven by adaptive radiations in both stages. However, apparent imaginal speciation phenomena can be a consequence of ecological differentiation at larval stages. Analyses of ecological differentiation within anisopterous larvae are extremely scarce and restricted to a couple of taxa (Corbet, 1999). Due to this lack of knowledge, we are still unable to address the problem whether speciation processes are driven by adaptive radiation in larval or adaptive / non-adaptive radiation in imaginal stages.

Acknowledgement I wish to express my thanks to the speakers of the systematics and evolutionary biology groups within the DZG, Heike Waegele and Klaus Reinhold, for inviting me as a plenary lecturer to the DZG-Meeting 2002, Halle. I extremely appreciated constructive critisism from Katharina Misof, University of Bonn and one anonymous reviewer. My thanks also to the staff of the ZFMK Molecular Biology Unit in supporting my work in every respect. I am very much indepted to Philip Corbet and Frank Suhling for sharing unpublished data on life cycle duration of Anisoptera. This work was supported by a grant of the DFG MI 649/1-1.

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