Niklas Janz

Diversity begets diversity: host expansions and the diversification of plant-feeding insects

BackgroundPlant-feeding insects make up a large part of earths total biodiversity. While it has been shown that herbivory has repeatedly led to increased diversification rates in insects, there has been no compelling explanation for how plant-feeding has promoted speciation rates. There is a growing awareness that ecological factors can lead to rapid diversification and, as one of the most prominent features of most insect-plant interactions, specialization onto a diverse resource has often been assumed to be the main process behind this diversification. However, specialization is mainly a pruning process, and is not able to actually generate diversity by itself. Here we investigate the role of host colonizations in generating insect diversity, by testing if insect speciation rate is correlated with resource diversity.ResultsBy applying a variant of independent contrast analysis, specially tailored for use on questions of species richness (MacroCAIC), we show that species richness is strongly correlated with diversity of host use in the butterfly family Nymphalidae. Furthermore, by comparing the results from reciprocal sister group selection, where sister groups were selected either on the basis of diversity of host use or species richness, we find that it is likely that diversity of host use is driving species richness, rather than vice versa.ConclusionWe conclude that resource diversity is correlated with species richness in the Nymphalidae and suggest a scenario based on recurring oscillations between host expansions – the incorporation of new plants into the repertoire – and specialization, as an important driving force behind the diversification of plant-feeding insects.

Evolutionary dynamics of host-plant specialization: a case study of the tribe Nymphalini.

Abstract Two general patterns that have emerged from the intense studies on insect‐host plant associations are a predominance of specialists over generalists and a taxonomic conservatism in host‐plant use. In most insect‐host plant systems, explanations for these patterns must be based on biases in the processes of host colonizations, host shifts, and specialization, rather than cospeciation. In the present paper, we investigate changes in host range in the nymphalid butterfly tribe Nymphalini, using parsimony optimizations of host‐plant data on the butterfly phylogeny. In addition, we performed larval establishment tests to search for larval capacity to feed and survive on plants that have been lost from the female egg‐laying repertoire. Optimizations suggested an ancestral association with Urticaceae, and most of the tested species showed a capacity to feed on Urtica dioica regardless of actual host‐plant use. In addition, there was a bias among the successful establishments on nonhosts toward plants that are used as hosts by other species in the Nymphalini. An increased likelihood of colonizing ancestral or related plants could also provide an alternative explanation for the observed pattern that some plant families appear to have been colonized independently several times in the tribe. We also show that there is no directionality in host range evolution toward increased specialization, that is, specialization is not a dead end. Instead, changes in host range show a very dynamic pattern.

BUTTERFLIES AND PLANTS: A PHYLOGENETIC STUDY

A database on host plant records from 437 ingroup taxa has been used to test a number of hypotheses on the interaction between butterflies and their host plants using phylogenetic methods (simple character optimization, concentrated changes test, and independent contrasts test). The butterfly phylogeny was assembled from various sources and host plant clades were identified according to Chase et al.s rbcL‐based phylogeny. The ancestral host plant appears to be associated within a highly derived rosid clade, including the family Fabaceae. As fossil data suggest that this clade is older than the butterflies, they must have colonized already diversified plants. Previous studies also suggest that the patterns of association in most insect‐plant interactions are more shaped by host shifts, through colonization and specialization, than by cospeciation. Consequently, we have focused explicitly on the mechanisms behind host shifts. Our results confirm, in the light of new phylogenetic evidence, the pattern reported by Ehrlich and Raven that related butterflies feed on related plants. We show that host shifts have generally been more common between closely related plants than between more distantly related plants. This finding, together with the possibility of a higher tendency of recolonizing ancestral hosts, helps to explain the apparent large‐scale conservation in the patterns of association between insects and their host plants, patterns which at the same time are more flexible on a more detailed level. Plant growth form was an even more conservative aspect of the interaction between butterflies and their host plants than plant phylogeny. However, this is largely explained by a higher probability of colonizations and host shifts while feeding on trees than on other growth forms.

The role of female search behaviour in determining host plant range in plant feeding insects: a test of the information processing hypothesis

Recent theoretical studies have suggested that host range in herbivorous insects may be more restricted by constraints on information processing on the ovipositing females than by trade–offs in larval feeding efficiency. We have investigated if females from polyphagous species have to pay for their ability to localize and evaluate plants from different species with a lower ability to discriminate between conspecific host plants with differences in quality. Females of the monophagous butterflies Polygonia satyrus, Vanessa indica and Inachis io and the polyphagous P. c–album and Cynthia cardui (all in Lepidoptera, Nymphalidae) were given a simultaneous choice of stinging nettles (Urtica dioica) of different quality. In addition, the same choice trial was given to females from two populations of P. c–album with different degrees of specificity. As predicted from the information processing hypothesis, all specialists discriminated significantly against the bad quality nettle, whereas the generalists laid an equal amount of eggs on both types of nettle. There were no corresponding differences between specialist and generalist larvae in their ability to utilize poor quality leaves. Our study therefore suggests that female host–searching behaviour plays an important role in determining host plant range.

How Specialists Can Be Generalists: Resolving the "Parasite Paradox" and Implications for Emerging Infectious Disease

The parasite paradox arises from the dual observations that parasites (broadly construed, including phy- tophagous insects) are resource specialists with restricted host ranges, and yet shifts onto relatively unrelated hosts are common in the phylogenetic diversification of parasite lineages and directly observable in ecological time. We synthe- size the emerging solution to this paradox: phenotypic flexibility and phylogenetic conservatism in traits related to resource use, grouped under the term ecological fitting, provide substantial opportunities for rapid host switching in changing environments, in the absence of the evolution of novel host-utilization capabilities. We discuss mechanisms behind ecological fitting, its implications for defining specialists and generalists, and briefly review empirical examples of host shifts in the context of ecological fitting. We conclude that host shifts via ecological fitting provide the fuel for the expansion phase of the recently proposed oscillation hypothesis of host range and speciation, and, more generally, the generation of novel combinations of interacting species within the geographic mosaic theory of coevolution. Finally, we conclude that taxon pulses, driven by climate change and large-scale ecological perturbation are drivers of biotic mixing and resultant ecological fitting, which leads to increased rates of rapid host switching, including the agents of Emerging Infectious Disease.

Host plant utilization in the comma butterfly: sources of variation and evolutionary implications

A major challenge in the study of insect-host plant interactions is to understand how the different aspects of offspring performance interact to produce a preference hierarchy in the ovipositing females. In this paper we investigate host plant preference of the polyphagous butterfly Polygonia c-album (Lepidoptera: Nymphalidae) and compare it with several aspects of the life history of its offspring (growth rate, development time, adult size, survival and female fecundity). Females and offspring were tested on four naturally used host plants (Urtica dioica, Ulmus glabra, Salix caprea, and Betula pubescens). There was substantial individual variation in host plant preference, including reversals in rank order, but the differences were largely confined to differences in the ranking of Urtica dioica and S. caprea. Different aspects of performance on these two plants gave conflicting and complementary results, implying a trade-off between short development time on U. dioica, and larger size and higher fecundity on S. caprea. As all performance components showed low individual variation the large variation in host plant preference was interpreted as due to alternative oviposition strategies on the basis of similar ‘performance hierarchies’. This indicates that the larval performance component of host-plant utilization may be more conservative to evolutionary change than the preference of ovipositing females. Possible macro-evolutionary implications of this are discussed.

Ovi position preference and larval performance in Polygonia c-album (Lepidoptera: Nymphalidae): the choice between bad and worse

As Thompson ( 1988a) remarks, the relationship between adult oviposition preference and offspring performance is the crux of the problem of understanding the evolution of insect/plant associations. Females often display a hierarchy of preferences for different hosts, so that they use a host lower in the hierarchy when the preferred species is not available (e.g. Wiklund, 1981; Thompson, 1988b). The preference hierarchy may be more or less well correlated with larval performance; here used as a composite term for offspring growth rate, survival and reproduction (Thompson, 1988a). A good correlation suggests that plant characteristics, including plant chemistry and nutritional value, is the most important factor that influences larval performance, limits host plant range and promotes specialization on only a few host plants the general pattern in insects. This is the core of both coevolution theory and sequential evolution theory for the evolution of insect-host plant interactions (Ehrlich & Raven, 1964; Jermy, 1984; Ronquist & Nylin, 1990). Conversely, poor correlations can be used as evidence by those who consider other ecological factors, such as selection for enemy-free space, to be of great importance in the evolution of host plant choice and specialization (e.g. Atsatt, 1981; Bernays & Graham, 1988; see also Strong, 1988). Thompson (1988a) and Thompson & Pellmyr (1991) review some of the evidence on preference-performance relationships, and note that the correlations range all the way from good to poor. Surprisingly often, poor correlations are found (e.g. Chew, 1977; Courtney, 1981; Williams, 1983; Penz & Araujo, 1991; Valladares & Lawton, 1991). There is evidence that a number of factors may cause poor correlations between preference and performance (Thompson, 1988a; Thompson & Pellmyr, 1991). These include: (1) selection for enemy-free space;

Host plant preferences in the comma butterfly (Polygonia c-album): Do parents and offspring agree?

Abstract:We studied the host plant preferences of parents and offspring in the comma butterfly, Polygonia c-album (L.), from the Stockholm area of central Sweden. Females of the spring and summer broods were given a choice of four host plants (Urtica dioica, Ulmus glabra, Salix caprea and Betula pubescens) in flight cages, whereas their newly hatched larval offspring were given a choice of leaf samples from the same plants in petri dishes. Disagreement regarding ranking of host plants among parents and offspring could indicate trade-offs between adult and offspring fitness correlates. In the case of P. c-album, we predicted that if such trade-offs are weak, the choices of parents and offspring should be in agreement, because a good correlation between female host plant preference and offspring laboratory performance has previously been found. Both female and larval plant preferences differed between broods. The preferences of females and offspring were in close agreement, also differing in the same way be...

No effect of larval experience on adult host preferences in Polygonia c-album (Lepidoptera: Nymphalidae): on the persistence of Hopkins' host selection principle

Abstract 1. The possible effect of juvenile imprinting or ‘chemical legacy’ on the subsequent oviposition – often called the ‘Hopkins’ host selection principle’– has been a controversial but recurrent theme in the literature on host‐plant preference. While it appears possible in principle, experimental support for the hypothesis is equivocal. The present study points out that it is also important to consider its theoretical implications, and asks under what circumstances, if any, it should be favoured by natural selection.

Butterfly host plant choice in the face of possible confusion

We tested predictions from the theory that ovipositing females of phytophagous insects are limited by their neural capacity for information processing. Previous studies have found that relatively specialized insects make faster and/or more accurate identifications of host plants compared to generalists. The study species was the polyphagous comma butterfly, Polygonia c-album (Nymphalidae). We compared females originating from two populations (Sweden and England) which differ in degree of specialization on the preferred host Urtica dioica (Urticaceae). Females were given a choice between this plant and a very similar nonhost, white dead nettle, Laminum album (Lamiacease), or a choice between a relatively poor host, Betuala pubescens, and the nonhost Betula pendula (Betulaceae). Oviposition rate was lower in cages with Betula compared to cages with Urtica, demonstrating that P. c-album females will withhold eggs when preferred hosts are not available. As predicted, females originating from the Swedish generalist population oviposited more often on the nonhost Lamium. However, females of both populations discriminated very strongly against oviposition on B. pendula. We found that newly hatched larvae have some ability to move from herbaceous nonhost to hosts. Although alternative interpretations are possible, the results give further support to the hypothesis that there are trade-offs between diet breadth and the ability to discriminate among plants.