Varying herbivore population structure correlates with lack of local adaptation in a geographic variable plant-herbivore interaction

Local adaptation of parasites to their hosts due to coevolution is a central prediction of many theories in evolutionary biology. However, empirical studies looking for parasite local adaptation show great variation in outcomes, and the reasons for such variation are largely unknown. In a previous study, we showed adaptive differentiation in the arctiid moth Utetheisa ornatrix to its host plant, the pyrrolizidine alkaloid-bearing legume Crotalaria pallida, at the continental scale, but found no differentiation at the regional scale. In the present study, we sampled the same sites to investigate factors that may contribute to the lack of differentiation at the regional scale. We performed field observations that show that specialist and non-specialist polyphagous herbivore incidence varies among populations at both scales. With a series of common-garden experiments we show that some plant traits that may affect herbivory (pyrrolizidine alkaloids and extrafloral nectaries) vary at the regional scale, while other traits (trichomes and nitrogen content) just vary at the continental scale. These results, combined with our previous evidence for plant population differentiation based on larval performance on fresh fruits, suggest that U. ornatrix is subjected to divergent selection even at the regional scale. Finally, with a microsatellite study we investigated population structure of U. ornatrix. We found that population structure is not stable over time: we found population differentiation at the regional scale in the first year of sampling, but not in the second year. Unstable population structure of the herbivore is the most likely cause of the lack of regional adaptation.     

Do canal‐cutting behaviours facilitate host‐range expansion by insect herbivores?

According to the escalation–radiation model of co-evolution, insect herbivores that acquire the ability to circumvent a plant defence enter a new adaptive zone and increase in species. How herbivore counter-adaptations to plant defences might lead to speciation is poorly understood. Studies of nymphalid butterflies suggest that the evolution of a broadened host range may be a critical step. This paper examines if leaf-feeding insects capable of deactivating defensive plant canals with canal cutting often have broad host ranges. A total of 94 species of canal-cutting insects were identified from the literature, including eight new canal cutters described in this paper. Only 27% of canal cutters with known host ranges are generalists that feed on plants in multiple families. The proportion of generalist canal cutters is similar or lower than estimates of generalists among phytophagous insects overall. Only five species, at most, of the canal-cutting generalists feed exclusively on plants with secretory canals. The paucity of generalists can be attributed in part to the considerable taxonomic distance separating canal-bearing plant families and to their corresponding chemical distinctiveness. The dependence of many canal-cutting species on host chemicals for defence would also favour specialization.  © 2009 The Linnean Society of London, Biological Journal of the Linnean Society , 2009, 96 , 715–731.     

Genetic and morphological divergence reveals local subdivision of perch (Perca fluviatilis L.)

The level of gene flow is an important factor influencing genetic differentiation between populations. Typically, geographic distance is considered to be the major factor limiting dispersal and should thus only influence the degree of genetic divergence at larger spatial scales. However, recent studies have revealed the possibility for small-scale genetic differentiation, suggesting that the spatial scale considered is pivotal for finding patterns of isolation by distance. To address this question, genetic and morphological differentiation were studied at two spatial scales (range 2–13 km and range 300 m to 2 km) in the perch ( Perca fluviatilis L.) from the east coast archipelago of Sweden, using seven microsatellite loci and geometric morphometrics. We found highly significant genetic differentiation between sampled locations at both scales. At the larger spatial scale, the distance per se was not affecting the level of divergence. At the small scale, however, we found subtle patterns of isolation by distance. In addition, we also found morphological divergence between locations, congruent with a spatial separation at a microgeographic scale, most likely due to phenotypic plasticity. The present study highlights the importance of geographical scale and indicates that there might be a disparity between the dispersal capacity of a species and the actual movement of genes. Thus, how we view the environment and possible barriers to dispersal might have great implications for our ability to fully understand the evolution of genetic differentiation, local adaptation, and, in the end, speciation.  © 2009 The Linnean Society of London, Biological Journal of the Linnean Society , 2009, 96 , 746–758.     

Discordance in body size, colour pattern, and advertisement call across genetically distinct populations in a Neotropical anuran (Dendropsophus ebraccatus)

Patterns of intraspecific geographic variation in morphology and behaviour, when examined in a phylogenetic context, can provide insight into the microevolutionary processes driving population divergence and ultimately speciation. In the present study, we quantified behavioural and phenotypic variation among populations from genetically divergent regions in the Central American treefrog, Dendropsophus ebraccatus . Our fine-scale population comparisons demonstrated regional divergence in body size, colour pattern frequencies, and male advertisement call. None of the characters covaried with phylogenetic history or geographic proximity among sampled populations, indicating the importance of highly localized selection pressures and genetic drift in shaping character divergence among isolated regions. The study underscores how multiple phenotypic characters can evolve independently across relatively small spatial scales.  © 2009 The Linnean Society of London, Biological Journal of the Linnean Society , 2009, 97 , 298–313.     

Describing a multitrophic plant-herbivore-parasitoid system at four spatial scales

Herbivore-parasitoid interactions must be studied using a multitrophic and multispecies approach. The strength and direction of multiple effects through trophic levels may change across spatial scales. In this work, we use the herbaceous plant Ruellia nudiflora, its moth herbivore Tripudia quadrifera, and several parasitoid morphospecies that feed on the herbivore to answer the following questions: Do herbivore and parasitoid attack levels vary depending on the spatial scale considered? With which plant characteristics are the parasitoid and the herbivore associated? Do parasitoid morphospecies vary in the magnitude of their positive indirect effect on plant reproduction? We evaluated three approximations of herbivore and parasitoid abundance (raw numbers, ratios, and attack rates) at four spatial scales: regional (three different regions which differ in terms of abiotic and biotic characteristics); population (i.e. four populations within each region); patch (four 1 m² plots in each population); and plant level (using a number of plant characteristics). Finally, we determined whether parasitoids have a positive indirect effect on plant reproductive success (seed number). Herbivore and parasitoid numbers differed at three of the spatial scales considered. However, herbivore/fruit ratio and attack rates did not differ at the population level. Parasitoid/host ratio and attack rates did not differ at any scale, although there was a tendency of a higher attack in one region. At the plant level, herbivore and parasitoid abundances were related to different plant traits, varying the importance and the direction (positive or negative) of those traits. In addition, only one parasitoid species (Bracon sp.) had a positive effect on plant fitness saving up to 20% of the seeds in a fruit. These results underline the importance of knowing the scales that are relevant to organisms at different trophic levels and distinguish between the specific effects of species.     

Did Polyommatus icarus (Lepidoptera: Lycaenidae) have distinct glacial refugia in southern Europe? Evidence from population genetics

Pleistocene climatic oscillations strongly influenced the genetic composition of many species which are often divided into several genetic lineages. In this context, we studied the allozymes of a common and widely distributed butterfly, the common blue Polyommatus icarus, over a large part of Europe. The species had a rather high genetic diversity within populations with a strikingly high mean number of alleles per locus (2.98). In contrast, differentiation between populations was very low ( F _ST: 0.0187). Only a marginal trend of decline in genetic diversity from the south to the north was observed. Isolation-by-distance existed on a European scale ( r =  0.826), but not at a regional level. Regional differentiation between populations in western Germany was extremely low ( F _ST: 0.0041). It is probable that P. icarus was widely distributed in the Mediterranean region during the last ice age and expanded into central Europe in the postglacial period without major genetic erosion. Moderate present and past gene flow in an intact metapopulation structure may have occurred on local, regional and perhaps even continental scales.  © 2003 The Linnean Society of London, Biological Journal of the Linnean Society , 2003, 80 , 529–538.     

Increased moth herbivory associated with environmental stress of pinyon pine at local and regional levels

 Using 6 years of observational and experimental data, we examined the hypothesis that water and nutrient stress increase the susceptibility of pinyon pine (Pinus edulis) to the stem- and cone-boring moth (Dioryctria albovittella). At two geographic levels, a local scale of 550 km² and a regional scale of 10,000 km², moth herbivory was strongly correlated with an edaphic stress gradient. At a local scale, from the cinder soils of Sunset Crater to nearby sandy-loam soils, nine of ten soil macro- and micronutrients, and soil water content were lowest in cinder-dominated soils. Herbivore damage was six times greater on trees growing in the most water and nutrient deficient site at Sunset Crater compared to sites with well-developed soils. Percentage silt-clay content of soil, which was highly positively correlated with soil nutrient and soil moisture at a local scale, accounted for 56% of the variation in herbivory at a regional scale among 22 sites. Within and across sites, increased stem resin flow was positively associated with reduced moth attack. On the basis of moth distribution across a stress gradient, we predicted that pinyons growing in highly stressful environments would show increased resistance to herbivores if supplemented with water and/or nutrients. We conducted a 6-year experiment at a high-stress site where individual trees received water only, fertilizer only, and water + fertilizer. Relative to control trees, stem growth and resin flow increased in all three treatments, but only significantly in the water + fertilizer treatment. Although there was no significant difference in herbivore damage among these three treatments, there was an overall reduction in herbivore damage on all treatment trees combined, compared to control trees. This experiment suggests that release from stress leads to increased resistance to insect attack and is consistent with our observational data. While other studies have predicted that short-term stress will result in herbivore outbreaks, our studies extend this prediction to chronically stressed host populations. Finally, while flush-feeders are not predicted to respond positively to stressed host plants, we found a positive association between herbivore attack and stressed pinyon populations. Received: 25 December 1995 / Accepted: 15 August 1996     

Scale-independent criteria and scale-dependent agents determining the structure of a ground cricket mosaic hybrid zone (Allonemobius socius – Allonemobius fasciatus)

The structure of the hybrid zone between the ground crickets, Allonemobius socius and Allonemobius fasciatus , approximates an environmental mosaic based on temperature/moisture at regional spatial scales. In the present study, we show that the micro-geographic spatial structure (i.e. single fields) of this hybrid zone is governed by the same criteria. Thus, the criteria that structure this hybrid zone are scale independent, even though the agents that implement these criteria may differ at various scales (climate, latitude, and elevation at regional scales; grass height, slope aspect, and field use at micro-geographic scales). Additionally, the study demonstrates a previously unknown barrier to genetic exchange in this system that acts before conspecific sperm precedence.  © 2008 The Linnean Society of London, Biological Journal of the Linnean Society , 2008, 94 , 777–796.     

Herbivore host-associated genetic differentiation depends on the scale of plant genetic variation examined

Herbivore adaptation to plant genetic variation can lead to reproductive isolation and the formation of host-associated lineages (host-associated differentiation, or HAD). Plant genetic variation exists along a scale, ranging from variation among individual plant genotypes to variation among plant species. Along this scale, herbivores may adapt and diverge at any level, yet few studies have examined whether herbivore differentiation exhibits scaling with respect to host variation (e.g., from genotypes to species). Determining at which level(s) herbivore differentiation occurs can provide insight into the importance of plant genetic variation on herbivore evolution. Previous studies have found strong genetic differentiation in the eriophyid mite, Aceria parapopuli, between hybrid Populus hosts and parental Populus species, but minimal neutral-locus differentiation among individual trees of the same species. We tested whether genetic differentiation in A. parapopuli scales with genetic variation in its Populus hosts. Using mite ITS1 sequence data collected among host species and among host populations, two key patterns emerged. (1) We found strong differentiation of A. parapopuli among Populus species, supporting the hypothesis that plant species differences drive reproductive isolation and HAD. (2) We did not find evidence of host-driven genetic differentiation in mites at the level of plant populations, suggesting that this level of plant variation is insufficiently strong to drive differentiation at a neutral locus. In combination with previous studies, we found that HAD occurs at the higher levels of plant genetic variation, but not at lower levels, and conclude that HAD depends on the scale of plant genetic variation examined.     

Complex trait differentiation between host-populations of the pea aphid Acyrthosiphon pisum (Harris): implications for the evolution of ecological specialisation

Variation in traits affecting preference for, and performance on, new habitats is a key factor in the initiation of ecological specialisation and adaptive speciation. However, habitat and resource use also involves other traits whose influence on ecological and genetic divergence remains poorly understood. In the present study, we investigated the extent of variation of life-history traits among sympatric populations of the pea aphid Acyrthosiphon pisum , which shows several host races that are specialised on various plants of the family Fabaceae plants and is an established model for ecological speciation. First, we assessed the community structure of microbial partners within host populations of the pea aphid. The effect of these microbes on host fitness is uncertain, although there is growing evidence that they may modulate various important adaptive traits of their host such as plant utilisation and resistance against natural enemies. Second, we performed a multivariate analysis on several ecologically relevant features of host populations recorded in the present and previous studies (including microbial composition, colour morph, reproductive mode, and male dispersal phenotype), enabling the identification of correlations between phenotypic traits. We discuss the ecological significance of these associations of traits in relation to the habitat characteristics of pea aphid populations, and their consequences for the evolution of ecological specialisation and sympatric speciation.  © 2009 The Linnean Society of London, Biological Journal of the Linnean Society , 2009, 97 , 718–727.     

Life history evolution in a globally invading tephritid: patterns of survival and reproduction in medflies from six world regions

Comparisons among populations from different localities represent an important tool in the study of evolution. Medflies have colonized many temperate and tropical areas all over the world during the last few centuries. In a common garden environment, we examined whether medfly populations obtained from six global regions [Africa (Kenya), Pacific (Hawaii), Central America (Guatemala), South America (Brazil), Extra-Mediterranean (Portugal) and Mediterranean (Greece)] have evolved different survival and reproductive schedules. Whereas females were either short-lived [life expectancy at eclosion (e₀) 48–58 days; Kenya, Hawaii and Guatemala] or long-lived (e₀ 72–76 days; Greece, Portugal and Brazil], males with one exception (Guatemala) were generally long-lived (e₀ 106–122 days). Although males universally outlived females in all populations, the longevity gender gap was highly variable (20–58 days). Lifetime fecundity rates were similar among populations. However, large differences were observed in their age-specific reproductive patterns. Short-lived populations mature at earlier ages and allocate more of their resources to reproduction early in life compared with long-lived ones. In all populations, females experienced a post-reproductive lifespan, with this segment being significantly longer in Kenyan flies. Therefore, it seems plausible that medfly populations, inhabiting ecologically diverse habitats, have evolved different life history strategies to cope with local environmental conditions.  © 2009 The Linnean Society of London, Biological Journal of the Linnean Society , 2009, 97 , 106–117.     

Species' diversity in the New Caledonian endemic genera Cephalidiosus and Nobarnus (Insecta: Heteroptera: Tingidae), an approach using phylogeny and species' distribution modelling

The patterns of local endemism in New Caledonia were analysed in two endemic genera of Tingidae (Insecta, Heteroptera), Cephalidiosus and Nobarnus , through a phylogenetic analysis and species' distribution modelling. The aim was to determine the possible causes of diversification and endemism in New Caledonia. Our results show that environmental conditions are probably important for the distribution of the genus Cephalidiosus , in conjunction with other factors such as resource (host plant) distribution, but suggest that the same environmental conditions have not influenced the speciation processes and diversification in the genus.  © 2009 The Linnean Society of London, Biological Journal of the Linnean Society , 2009, 97 , 177–184.     

Meadow pipit (Anthus pratensis) egg appearance in cuckoo (Cuculus canorus) sympatric and allopatric populations

Host populations tend to show less ability to discriminate against parasites when living in their absence. However, comparison of rejection rates among sympatric and allopatric host populations does not allow determination of whether the greater tolerance in allopatric populations reflects a genetic change or phenotypic plasticity. Here we test the existence of changes in a host's adaptation to brood parasitism in the absence of parasitism by studying intraclutch variation in egg appearance, which is a genetically determined component of host defence favouring discrimination of parasitic eggs. We investigated egg phenotypes of a common host of the European cuckoo, Cuculus canorus , in the presence and in the absence of cuckoos. By using objective spectroradiometry techniques of colour assessment we compared intraclutch variation between populations of meadow pipit, Anthus pratensis , sympatric (England) and allopatric (Iceland and Faeroe Islands) with C. canorus . Allopatric populations of A. pratensis showed greater intraclutch variation in egg appearance in the ultraviolet part of the spectrum than did a population sympatric with C. canorus . Two possible alternative mechanisms explaining these findings are discussed.  © 2003 The Linnean Society of London, Biological Journal of the Linnean Society , 2003, 79 , 543–549.     

Spatial scale of local adaptation in a plant-pathogen metapopulation

The rate and scale of gene flow can strongly affect patterns of local adaptation in host-parasite interactions. I used data on regional pathogen occurrence to infer the scale of pathogen dispersal and to identify pathogen metapopulations in the interaction between Plantago lanceolata and its specialist phytopathogen, Podosphaera plantaginis. Frequent extinctions and colonizations were recorded in the metapopulations, suggesting substantial gene flow at this spatial scale. The level of pathogen local adaptation was assessed in a laboratory inoculation experiment at three different scales: in sympatric host populations, in sympatric host metapopulations and in allopatric host metapopulations. I found evidence for adaptation to sympatric host populations, as well as evidence indicating that local adaptation may extend to the scale of the sympatric host metapopulation. There was also variation among the metapopulations in the degree of pathogen local adaptation. This may be explained by regional differences in the rate of migration.     

Genetic structure of fragmented November moth (Lepidoptera: Geometridae) populations in farmland

Habitats are now becoming increasingly fragmented throughout the world due to intense cultivation. As a consequence, populations of some animals with low mobility have become isolated, thus increasing the risk of inbreeding and local extinction. In Britain, weakly flying geometric moths of the genus Epirrita are a good model species with which to test the genetic effects of habitat fragmentation on insect populations. Genetic variation within and between populations of two Epirrita species captured using a network of light traps at two spatial scales (local and national) was assessed using allozyme electrophoresis, with particular reference to the local scale (the 330-ha arable farm estate at Rothamsted, Hertfordshire, in southern Britain). Populations sampled widely in England and Wales displayed low (but statistically significant) levels of genetic differentiation for both species ( F _st  = 0.0051–0.0114 and 0.0226 for E. dilutata and E. christyi , respectively). However, analysis of large samples of E. dilutata from four small woods at Rothamsted revealed low ( F _st  = 0.0046) but significant differentiation, indicating that gene flow was restricted, even at this very small scale. It was concluded that small intervening patches of farmland (often a few fields width) were enough to prevent genetic homogeneity. The close similarity between more distant Epirrita populations was considered to be a result of historical, rather than recurrent gene flow, as genetic equilibrium between drift and gene flow is unlikely over such scales.  © 2003 The Linnean Society of London . Biological Journal of the Linnean Society , 2003, 78 , 467–477.     

Genetic variation and structure in native populations of the fire ant Solenopsis invicta: evolutionary and demographic implications

We studied population genetic variation and structure in the fire ant Solenopsis invicta using nuclear genotypic and mitochondrial DNA (mtDNA) sequence data obtained from samples collected throughout its native range. Geographic populations are strongly differentiated at both genomes, with such structure more pronounced in Brazil than in Argentina. Higher-level regional structure is evident from the occurrence of isolation-by-distance patterns among populations, the recognition of clusters of genetically similar, geographically adjacent populations by ordination analysis, and the detection of an mtDNA discontinuity between Argentina and Brazil coinciding with a previously identified landform of biogeographical relevance. Multiple lines of evidence from both genomes suggest that the ancestors of the ants we studied resembled extant northern Argentine S. invicta , and that existing Brazilian populations were established more recently by serial long-distance colonizations and/or range expansions. The most compelling evidence for this is the corresponding increase in F _K (a measure of divergence from a hypothetical ancestor) and decrease in genetic diversity with distance from the Corrientes population in northern Argentina. Relatively deep sequence divergence among several mtDNA clades, coupled with geographical partitioning of many of them, suggests prolonged occupation of South America by S. invicta in more-or-less isolated regional populations. Such populations appear, in some cases, to have come into secondary contact without regaining the capacity to freely interbreed. We conclude that nominal S. invicta in its native range comprises multiple entities that are sufficiently genetically isolated and diverged to have embarked on independent evolutionary paths.  © 2007 The Linnean Society of London, Biological Journal of the Linnean Society , 2007, 92 , 541–560.     

Cuticular hydrocarbon profiles of codling moth larvae,Cydia pomonella (Lepidoptera: Tortricidae), reflect those of their host plant species

The cuticular hydrocarbons (CHCs) of codling moth larvae collected in the field from their host plant species, apple and walnut, were analyzed and compared with the CHCs of fruits from these two phylogenetically distant hosts. The CHC profiles of the larvae consisted solely of n‐alkanes (C₂₃–C₃₁) and differed quantitatively between host populations. Amounts of the CHCs from the walnut‐collected larvae were shifted towards longer‐chain alkanes compared to those from apple‐collected larvae. A similar shift was observed for the CHC profiles of walnut and apple fruits. Analysis of the CHCs of larvae reared on artificial diet, in comparison with hydrocarbons from the diet, confirmed that larval CHCs scarcely reflect hydrocarbons from the food source. This finding indicates that the larval hydrocarbons must be biosynthesized to a large degree by the insect, rather than being gained directly from its diet. Hence, codling moth populations from apple and walnut each synthesize their own CHC profiles, which largely resemble those of their respective host plant, yielding a potential tool of chemical camouflage from certain natural antagonists of the larvae. The findings of the present study, together with recent molecular population analyses, provides evidence for a process that might ultimately lead to sympatric speciation of this herbivore species. © 2010 The Linnean Society of London, Biological Journal of the Linnean Society, 2010, 101 , 376–384.     

Genetic differentiation on multiple spatial scales in an ecotype-forming marine snail with limited dispersal: Littorina saxatilis

The population genetic structure of marine species lacking free-swimming larvae is expected to be strongly affected by random genetic drift among populations, resulting in genetic isolation by geographical distance. At the same time, ecological separation over microhabitats followed by direct selection on those parts of the genome that affect adaptation might also be strong. Here, we address the question of how the relative importance of stochastic vs. selective structuring forces varies at different geographical scales. We use microsatellite DNA and allozyme data from samples of the marine rocky shore snail Littorina saxatilis over distance scales ranging from metres to 1000 km, and we show that genetic drift is the most important structuring evolutionary force at distances > 1 km. On smaller geographical scales (< 1 km), divergent selection between contrasting habitats affects population genetic structure by impeding gene flow over microhabitat borders (microsatellite structure), or by directly favouring specific alleles of selected loci (allozyme structure). The results suggest that evolutionary drivers of population genetic structure cannot a priori be assumed to be equally important at different geographical scales. © 2008 The Linnean Society of London, Biological Journal of the Linnean Society , 2008, 94 , 31–40.     

Contrasting temporal dynamics and spatial patterns of population genetic structure correlate with differences in demography and habitat between two closely-related African freshwater snails

The relationship between habitat stability, demography, and population genetic structure was explored by comparing temporal microsatellite variability spanning a decade in two closely-related hermaphroditic freshwater snails from Cameroon, Bulinus forskalii and Bulinus camerunensis . Although both species show similar levels of preferential selfing, microsatellite analysis revealed significantly greater allelic richness and gene diversity in populations of the highly endemic B. camerunensis compared to those of the geographically-widespread B. forskalii . Additionally, B. camerunensis populations showed significantly lower spatial genetic differentiation, higher dispersal rates, and greater temporal stability compared to B. forskalii populations over a similar spatial scale. This suggests that a more stable demography and greater gene flow account for the elevated genetic diversity observed in this geographically-restricted snail. This contrasts sharply with a metapopulation model (which includes extinction/contraction, recolonization/expansion, and passive dispersal) invoked to account for population structuring in B. forskalii . As intermediate hosts for medically important schistosome parasites, these findings have ramifications for determining the scale at which local adaptation may occur in the coevolution of these snails and their parasites.  © 2007 The Linnean Society of London, Biological Journal of the Linnean Society , 2007, 90 , 747–760.     

Variability in diapause propensity within populations of a temperate insect species: interactions between insecticide resistance genes and photoperiodism

Temperate insects generally use day length as a reliable cue for long-term seasonal changes in their environment. Significant variation in photoperiodism between and within populations is thought to be associated with genetic variation resulting from local adaptation. In this study, we investigated whether genetic variation associated with selection for insecticide resistance may be a source of divergence in the photoperiodic timing of diapause through pleiotropic interactions. Critical photoperiods for diapause induction were estimated in one susceptible and two insecticide-resistant homozygous strains of the codling moth Cydia pomonella , as well as in their reciprocal F₁ progeny. Diapause responses to naturally decreasing day length were subsequently followed in the laboratory strains and in two field populations of C. pomonella in south-eastern France. We found higher critical photoperiods for diapause induction in homozygous resistant individuals than in both homozygous susceptible and heterozygous ones. This partly explained the significantly earlier timings of diapause found in homozygous resistant individuals of both laboratory and field populations of C. pomonella under natural photoperiods, relative to those found in both homozygous susceptible and heterozygous ones. We assume that adaptive genetic changes associated with selection for insecticide resistance may generate substantial variation in the seasonal timing of diapause, an essential ecological feature of the fitness of insecticide resistance genes in this species.  © 2004 The Linnean Society of London, Biological Journal of the Linnean Society , 2004, 83 , 341–351.