Sören Nylin

Adaptive plasticity and plasticity as an adaptation : a selective review of plasticity in animal morphology and life history

During the last decade there has been a rapidly growing interest in the study of phenotypic plasticity in animals. Confused terminology in this field of research may be one reason why the focus of many studies is not as clear as it could be. The field of plasticity highlights the general problem of demonstrating adaptation. We discuss the terminology and methodology of plasticity studies, with particular reference to the question of which patterns should be considered evidence for plasticity as an adaptation to the environment, and how to find such evidence. We suggest a terminology where plasticity can be adaptive (i.e. beneficial, and maintained by selection) with respect to a function without strictly being an adaptation for it (evolutionary origin linked to this function), and vice versa. Modifications of the original reaction norm, seen today as differences in plasticity between populations and species, can be adaptations for a function even when the plasticity itself is not (it may follow from constraints or from selection for another function). We selectively review cases reported as evidence of adaptive plasticity in animal morphology and life history, choosing examples from a wide range of taxa to illustrate our criteria for what should be called adaptive and adaptation when applied to plasticity.

The Effect of Flexible Growth Rates on Optimal Sizes and Development Times in a Seasonal Environment

The interrelationships among development time, growth rate, and adult size are investigated using simple optimization models of a seasonal life history in which larger adults have greater reproductive output. Unlike most previous studies, our models assume that growth rate is an adaptively flexible character that can be increased at the expense of a greater juvenile mortality rate. Three components of fitness are considered: the cost of developing at a suboptimal time of the year, the reproductive advantage of larger adult size, and the increased mortality from rapid juvenile growth. The study focuses on the optimal responses of size, development time, and growth rate to changes in the amount of time available for completion of the life cycle. The models show that the optimal growth rate and size at maturity may respond in several different ways. Perhaps the most likely effect is that growth becomes faster and size smaller with less time available. It is also possible, however, for either growth rate or size (but not both) to stay constant; in other cases, less time available leads to slower growth or larger size. The effects of increased mortality on the juvenile stage are also explored; here, the optimal size is likely to decrease, but growth rate and development time may increase or decrease.

Adaptive variation in growth rate: life history costs and consequences in the speckled wood butterfly,Pararge aegeria

An important assumption made in most lifehistory theory is that there is a trade-off between age and size at reproduction. This trade-off may, however, disappear if growth rate varies adaptively. The fact that individuals do not always grow at the maximum rate can only be understood if high growth rates carry a cost. This study investigates the presence and nature of such costs inPararge aegeria. Five females from two populations with known differences in life history (south Sweden and Maderia) were allowed to oviposit in the laboratory and their offspring were reared in environmental chambers under conditions leading to direct development. We measured several aspects of life history, including development times, pupal and adult weights, growth rate, female fecundity, longevity and larval starvation endurance. In both populations there seemed to be genetic variation in growth rate. There was no evidence for a trade-off between age and size at pupation. As predicted, larvae with high growth rates also lost weight at a relatively higher rate during starvation. High weight-loss rates were furthermore associated with a lower probability of surviving when food became available again. This is apparently the first physiological trade-off with growth rate that has been experimentally demonstrated. In both populations there were significant differences in growth rate between the sexes, but the populations differed in which sex was growing at the highest rate. In Sweden males had higher growth rates than females, whereas the reverse was true for Madeira. These patterns most likely reflect differences in selection for protandry, in turn caused by differences in seasonality between Sweden and Madeira. Together with the finding that males had shorter average longevity than females in the Swedish, but not in the Maderiran, population, this indicates that a lower adult quality also may be a cost of high growth rate. We argue that for the understanding of life history variation it is necessary to consider not only the two dimensions of age and size, but also to take into full account the triangular nature of the relationship between size, time and growth rate.

Nymphalid butterflies diversify following near demise at the cretaceous/tertiary boundary

The butterfly family Nymphalidae contains some of the most important non-drosophilid insect model systems for evolutionary and ecological studies, yet the evolutionary history of the group has remained shrouded in mystery. We have inferred a robust phylogenetic hypothesis based on sequences of 10 genes and 235 morphological characters for exemplars of 400 of the 540 valid nymphalid genera representing all major lineages of the family. By dating the branching events, we infer that Nymphalidae originated in the Cretaceous at 90 Ma, but that the ancestors of 10–12 lineages survived the end-Cretaceous catastrophe in the Neotropical and Oriental regions. Patterns of diversification suggest extinction of lineages at the Cretaceous/Tertiary boundary (65 Ma) and subsequent elevated speciation rates in the Tertiary.

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.

Synergistic effects of combining morphological and molecular data in resolving the phylogeny of butterflies and skippers

Phylogenetic relationships among major clades of butterflies and skippers have long been controversial, with no general consensus even today. Such lack of resolution is a substantial impediment to using the otherwise well studied butterflies as a model group in biology. Here we report the results of a combined analysis of DNA sequences from three genes and a morphological data matrix for 57 taxa (3258 characters, 1290 parsimony informative) representing all major lineages from the three putative butterfly super-families (Hedyloidea, Hesperioidea and Papilionoidea), plus out-groups representing other ditrysian Lepidoptera families. Recently, the utility of morphological data as a source of phylogenetic evidence has been debated. We present the first well supported phylogenetic hypothesis for the butterflies and skippers based on a total-evidence analysis of both traditional morphological characters and new molecular characters from three gene regions (COI, EF-1α and wingless). All four data partitions show substantial hidden support for the deeper nodes, which emerges only in a combined analysis in which the addition of morphological data plays a crucial role. With the exception of Nymphalidae, the traditionally recognized families are found to be strongly supported monophyletic clades with the following relationships: (Hesperiidae+(Papilionidae+(Pieridae+(Nymphalidae+(Lycaenidae+Riodinidae))))). Nymphalidae is recovered as a monophyletic clade but this clade does not have strong support. Lycaenidae and Riodinidae are sister groups with strong support and we suggest that the latter be given family rank. The position of Pieridae as the sister taxon to nymphalids, lycaenids and riodinids is supported by morphology and the EF-1α data but conflicted by the COI and wingless data. Hedylidae are more likely to be related to butterflies and skippers than geometrid moths and appear to be the sister group to Papilionoidea+Hesperioidea.

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.

Proximate Causes of Rensch’s Rule: Does Sexual Size Dimorphism in Arthropods Result from Sex Differences in Development Time?

A prominent interspecific pattern of sexual size dimorphism (SSD) is Rensch’s rule, according to which male body size is more variable or evolutionarily divergent than female body size. Assuming equal growth rates of males and females, SSD would be entirely mediated, and Rensch’s rule proximately caused, by sexual differences in development times, or sexual bimaturism (SBM), with the larger sex developing for a proportionately longer time. Only a subset of the seven arthropod groups investigated in this study exhibits Rensch’s rule. Furthermore, we found only a weak positive relationship between SSD and SBM overall, suggesting that growth rate differences between the sexes are more important than development time differences in proximately mediating SSD in a wide but by no means comprehensive range of arthropod taxa. Except when protandry is of selective advantage (as in many butterflies, Hymenoptera, and spiders), male development time was equal to (in water striders and beetles) or even longer than (in drosophilid and sepsid flies) that of females. Because all taxa show female‐biased SSD, this implies faster growth of females in general, a pattern markedly different from that of primates and birds (analyzed here for comparison). We discuss three potential explanations for this pattern based on life‐history trade‐offs and sexual selection.