Planthopper case studies

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Species concepts and speciation in insect herbivores: Planthopper case studies Michael F. Claridge

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School of Pure & Applied Biology , University of Wales , Cardiff, CF1 3TL, Wales (UK) Published online: 28 Jan 2009.

To cite this article: Michael F. Claridge (1995) Species concepts and speciation in insect herbivores: Planthopper case studies, Bolletino di zoologia, 62:1, 53-58, DOI: 10.1080/11250009509356051 To link to this article: http://dx.doi.org/10.1080/11250009509356051

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Boll. Zool. 62: 53-58 (1995)

Species concepts and speciation in insect herbivores: planthopper case studies MICHAEL F. CLARIDGE

Downloaded by [185.10.253.34] at 07:36 24 March 2014

School of Pure & Applied Biology, University of Wales, Cardiff CF1 3TL Wales (UK)

ABSTRACT General biological and phylogenetic species concepts are compared and contrasted. They are applied to studies on insect herbivores and particularly to variation in populations of the planthoppers Nilaparvata lugens and N. bakeri in Asia and Australia. Speciation processes for these herbivores are discussed in the light of contrasting species concepts. Emphasis is placed on the evolution of reproductive isolation. KEY WORDS: Biological species - Phylogenetic species Speciation - Geographical variation - Acoustic signals - Specific mate recognition systems - Planthoppers.

ACKNOWLEDGEMENTS The planthopper work summarised here has been funded in part by the Overseas Development Agency of the UK Government and Commission of the European Union. John Morgan kindly helped to produce the figures presented here. Invited paper at the Symposium «Speciazione: tempi e modi», 55th Congress of the Unione Zoológica Italiana, Torino, September 27 October 2, 1993.

INTRODUCTION

Species concepts In recent years the urgent need to document and understand biological diversity has stimulated renewed interest in the processes of evolutionary diversification and speciation. However, it is impossible to consider the processes of speciation without some agreement on the nature of species themselves. For sexually reproducing biparental organisms there has been more or less general agreement among biologists since the 1930's and '40's that a species concept based on reproductive isolation was the most useful (e.g. Dobzhansky, 1937; Huxley, 1940; Mayr, 1942). In particular Ernst Mayr (1942, 1963) elaborated what has become generally known as the biological species, which is probably still best defined as «groups of actually or potentially interbreeding natural populations which are reproductively isolated from other such groups» (1942: 120). In this, reproductive isolation maintained by isolating mechanisms between populations in the field is the critical criterion for determining species status. Given this emphasis then speciation is the evolution of reproductive isolation. The biological species has been used with great success over the past 50 years or so for many groups of organisms, but perhaps most particularly for animals. The recognition of sibling or cryptic species which are reproductively isolated, but lack obvious morphological markers, was an important advance resulting directly from the application of this concept. In recent years Paterson (e.g. 1985) has advocated a somewhat different approach to the biological species. In this, species are characterized by distinct specific mate recognition systems (SMRS), which for animals usually consist of a sequence of signals and responses exchanged between males and females. These systems of signals ensure that only like gametes meet and lead to successful fertilization. Thus, Paterson emphasises the importance of recognition rather than isolation. Indeed he terms his species concept the recognition concept in contrast to the isolation concept (= biological species) of other authors. The emphasis by Paterson on specific mate recognition systems is important and his criticisms of the mixed assemblages of phenomena previously termed isolating mechanisms are useful (Claridge, 1988). However, his SMRSs correspond broadly to what were previously termed behavioural and ecological isolating mechanisms and, like them, most importantly result in reproductive isolation. Thus in practice the two species concepts have much in common and together usefully may still be regarded as the biological species (Claridge, 1991; Claridge & Boddy 1994). Two major and well known problems exist for the application of the biological species concept in practice. 1. It is obviously impossible to apply the concept to organisms which either do not undergo sexual reproduction or similar exchange of genetic materials, or are par-

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thenogenetic with not even partial reversion to true sexual reproduction. Clearly species concepts for such organisms must be different since no exchange of gametes occurs and reproductive isolation has no meaning. 2. Even for sexually reproducing organisms it is only possible to determine if two populations are reproductively isolated if they meet naturally in the field at an appropriate time for the interbreeding criterion to be tested - that is if the populations are truly sympatric (Cain, 1953; Claridge, 1988). Of course it may also be possible to obtain some useful data from laboratory crosses and mate choice experiments between such populations. Because of these problems many taxonomists have consistently rejected the biological species often in favour of a morphological species (e.g. Sokal & Crovello, 1970). More recently these criticisms have resulted in various alternative species concepts, generally under the term phylogenetic or evolutionary species (e.g. Wiley, 1976; Cracraft, 1983, 1989). Similar ideas have also been advocated by van Valen (1976) as the ecological species. Perhaps typical of these concepts is that of Cracraft (1983), in which he defines species as «the smallest diagnosable cluster of individual organisms within which there is a parental pattern of ancestry and descent». Thus the species here is equated with a diagnosable clade, but a major problem is that there is no objective way of deciding how big a difference must be to be diagnosable. Thus determination of species status must be wholly subjective. These two broad species concepts with their various nuances are certainly the most widely advocated today. The differences between them are important for understanding speciation and indeed for our general conception of biological diversity. For biological species concepts, speciation is the evolution of different specific mate recognition systems and of reproductive isolation and thus concerns genetic status. For phylogenetic and ecological species concepts speciation consists of the development of diagnosably distinct clades without reference to their genetic status and thus to their evolutionary potential. Speciation of insect herbivores Insect herbivores are among the most species rich categories of living organisms and much attention and thought has been given to the speciation processes that have resulted in such high levels of diversity. These insects are characterized by precise and usually very restricted host plant preferences. Many feed only on one species of plant and very few are generalist feeders. It is perhaps therefore not surprising that discussions on speciation have often concentrated on host shifts and changes in host range. Usually little attention has been given to specific mate recognition systems, that is except for the role of specific host plants in determining them (Claridge, 1993). Most insect herbivores are biparental and reproduce

sexually so that biological species concepts may be applied. Little is usually known about SMRSs in most groups, but it is probable that for most, chemical signals and senses predominate. This is well known in many Coleóptera and Lepidoptera (e.g. Phelan, 1992). Unfortunately chemical interactions during mate finding and courtship are generally not easy to study under field conditions. Unlike chemical signals acoustic ones are much easier to record and analyse. The Homoptera Auchenorrhyncha - the cicadas, leafhoppers, treehoppers, planthoppers etc. - all use acoustic signals dominantly in courtship and mate location (Claridge, 1985a). In the species rich families of Cicadellidae (leafhoppers) and Delphacidae (planthoppers) low intensity specific acoustic signals are exchanged during courtship and transmitted through the plant substrate on which the insects live.

PLANTHOPPER CASE STUDIES The genus Nilaparvata The genus Nilaparvata is found primarily in tropical and subtropical regions of the world and includes 16 named species (Claridge & Morgan, 1987). It is well known to include the very important pest of rice in Asia, the brown planthopper, TV. lugens (Stâl) (see Wilson & Claridge, 1991). Nilaparvata lugens Nilaparvata lugens is restricted for food plants to rice, Oryza species and their cultivars, on which it feeds and in which it lays its eggs. It is widely distributed from India and Pakistan in the west to Australia and Fiji in the east, and to Japan and Korea in the north (Fig. 1). TV. lugens is a morphologically distinct species and is most easily recognized by details of the structure of the male external genitalia in which it differs from a close relative, TV. bakeri Muir (Fig. 2). Like all known Delphacidae, males and females of TV. lugens exchange characteristic amplitude modulated acoustic signals during mate finding (Fig. 3) (Claridge, 1985b; Claridge & de Vrijer, 1993). Geographically definable populations of TV. lugens from rice show some variation in features of both male and female signals (Claridge et al., 1985a), in particular the pulse repetition rates or frequencies (PRF) of critical song sections. The differentiation between some populations, for example ones from the Solomon Islands and N. Australia, was so great when tested in the laboratory as to lead to nonrandom mating and thus to some degree of reproductive isolation and incipient speciation (Claridge et al., 1984). It was therefore concluded that precise PRFs of both male and female calls in this species are critical to the specific mate recognition system. Nilaparvata lugens is specific to rices. However, over the past twenty years or so morphologically in-


SPECIES CONCEPTS AND SPECIATION IN PLANTHOPPERS

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N. lugens (rice)

O N.lugens (leersia) -K N.bakeri (leersia)

Fig. 1 - Sketch map of Asia and Australia to show localities from which species of Nilaparvata have been collected by Claridge and co-workers.

(b)

Fig. 2 - Male genitalia of Nilaparvata lugens (a - d) and N. bakeri (e - h) showing complete genital capsule in ventral view (a, e), pygofer in lateral view (b, f), aedeagus (c, g) and parameres (d, h) (After Wilson & Claridge 1991).

CLARIDGE M. F.

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c

1 See.


D Fig. 3 - Oscillograms of parts of male (A, B) and female (C, D) calls of Nilaparvata lugens from rice (A, C) and Leersia (B, D) collected in the Philippines (After Claridge et al, 1985b).

1 See. distinguishable populations have been found feeding and reproducing on the grass Leersia hexandra, a common semiaquatic weed of flooded rice fields, irrigation and drainage channels and water reservoirs (Claridge et al., 1985b, 1988). Populations from Leersia living in close proximity to those on rice have now been found widely in Asia and Australia (Fig. 1). Although the insects from the two hosts cannot be separated by morphology, they do not feed on each others hosts and if confined on them do very badly and usually die (Claridge et al., 1985b). In the laboratory the two forms will hybridize but given a choice usually mate with their own host type. Thus Saxena et al. (1983) concluded that the Leersia associated insects represented a different biotype or host race of N. lugens, but they did not investigate specific mate recognition systems. Like ./V. lugens from rice, males and females from Leersia exchange acoustic signals during mate location (Fig. 3). These differ significantly from sympatric rice feeding populations through their ranges of distribution (Claridge et al, 1985b, 1988). Mate choice and call playback experiments show clearly that the two host associated populations are reproductively isolated in the various regions where they occur. Indeed natural hybrids in the field would be recognisable from their intermediate calls. No such hybrid calls have been detected in field populations. Thus these insects must represent at least two reproductively isolated sibling species. The status of allopatric populations is difficult to determine, but recent preliminary molecular studies suggest that Australian populations of both host associated species should probably be regarded as different species to those in Asia 0ones et al., 1993). Whatever the final conclusion on the

status of allopatric populations, it is clear that relatively small differences in calls are sufficient to isolate sympatric populations of these insects. Interestingly it is just those sorts of differences which also vary between allopatric populations. Thus the two host associated sympatric sibling species currently both known as N. lugens differ in their host preferences and in their acoustic recognition signals. They also both show geographical variation in the features of those specific mate recognition signals which are known to confer reproductive isolation in sympatry. A possible allopatric scenario for speciation in this complex is therefore at least likely. Nilaparvata bakeri Nilaparvata bakeri is widely sympatric with N. lugens throughout much of Asia (Fig. 1) where it feeds and reproduces on Leersia hexandra (Claridge & Morgan, 1993). It is often found together with the Leersia associated N. lugens. Like the sibling species oiN. lugens, males and females of Af. bakeri exchange distinctive acoustic signals during mate finding and courtship. Despite numerous attempts we have been unable to obtain hybrids between N. bakeri and either of the N. lugens species from any geographical region. It is clear that the distinctly different calls play a role in maintaining reproductive isolation between them. Also, like the N. lugens species, N. bakeri shows very obvious geographical variation in calls particularly of the males (Fig. 4). However, despite the clear differences for example between populations from the Philippines and Indonesia, mate choice experiments show no apparent barriers

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SPECIES CONCEPTS AND SPECIATION IN PLANTHOPPERS

Philippines

India

Indonesia Fig. 4 - Oscillograms of parts of male calls of Nilaparvata bakeri from the Philippines, India and Indonesia (After Claridge & Morgan, 1993).


1 Sec.

to mating. Thus there is no indication that these distinctive features are critical parts of the SMRS of N. bakeri.

DISCUSSION

Species concepts

The two morphologically distinguishable species of Nilaparvata, N. lugens and TV. bakeri, discussed here are clearly different by application of either the biological or phylogenetic species concepts. Equally the two sympatric sibling species, both presently known as AT. lugens, could also be recognized by both. They are clearly reproductively isolated and diagnosably distinct, albeit using relatively small nonmorphological characters. It is difficult for the biological concept to determine the status of allopatric populations, but some degree of reproductive isolation can be demonstrated between some populations of these insects. Similar problems would arise for the application of the phylogenetic species. In particular what degree of difference would be required to establish the status of allopatric populations as different species? This can only be a subjective judgement. Nilaparvata bakeri populations in different regions of Asia show very clear differences in male courtship calls, certainly qualitatively greater than those between the sympatric sibling species of N. lugens. Presumably application of the phylogenetic species would then lead to recognition of them as separate allopatric species. However, we know from mate choice experiments that the different male calls have little obvious effect of providing reproductive isolation between the most obviously distinct populations (Claridge & Morgan, 1993). Thus there is no reason, using the biological species concept, to recognize distinct species within TV. bakeri. In this critical case a true understanding of the nature of the variation within, and of the genetic and evolutionary

status of, allopatric populations is best provided by the biological species. Speciation Classical speciation theory requires the isolation in space (allopatry) of subsets of an ancestral population (e.g. Dobzhansky, 1937; Mayr, 1942). The isolates may then diverge in isolation and lead subsequently to complete speciation by the evolution of specific mate recognition systems and therefore of reproductive isolation. The evolutionary literature has always included suggestions that specialist, species rich groups of organisms may speciate without any necessary period of allopatry, that is by sympatric speciation. Parasites generally and particularly insect herbivores have always been organisms at the forefront of such debates. In recent years Guy Bush (e.g. 1975, 1993) has been the major advocate of such speciation by sympatric host race formation and divergence by host adaptation. This view has been taken up by many ecologists (e.g. Price, 1980, Strong et al., 1984), but with little strong evidence (Claridge, 1988). The evidence for the adaptation of insect herbivores to particular host plants is overwhelming, but that does not preclude allopatric modes of speciation for their origin. As emphasized above, studies on specific mate recognition systems and the nature of reproductive isolation in insect herbivores are rare and often difficult to do, particularly where pheromone systems are involved. However the largely acoustic systems in planthoppers and their relatives make such studies much easier. The case studies on Nilaparvata species summarized above show how acoustic signals are critical to maintaining reproductive isolation. Also allopatric populations frequently show varying degrees of call differentiation which could lead to speciation. Exciting recent studies on populations of the cave-dwelling planthopper, Oliarus polyphemus, isolated in Hawaiian lava tube

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systems show rapid divergence of acoustic mate recognition signals (Hoch & Howarth, 1993). The divergence is such as to produce reproductive isolation between some of the populations studied, providing strong support for an allopatric mode of speciation. Perhaps most remarkable in this context are the experimental studies of de Winter (1992). He was able to select from a laboratory culture population of the planthopper, Ribautodelphax pungens, for courtship calls of high and low pulse repetition rates respectively over only ten generations. After such a short period of selection the resulting populations differed so greatly that high levels of reproductive isolation existed between them. Thus, effectively the process of speciation was simulated by selection for different specific mate recognition systems in the two separate populations. These studies at least demonstrate the possibilities for allopatric speciation among planthoppers and by inference among other herbivores. This of course does not preclude other possible modes of speciation. However, it does suggest that simple generalizations about speciation in major species rich groups of organisms are at least premature.

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