On the origin and evolution of major morphological characters

Although the mathematical principles underpinning population-level evolution are now well studied, the origin and evolution of morphological novelties has received far less attention. Here, a broad but general theory for how this sort of change takes place is outlined, relying on functional continuity, least-constrained components of morphology, redundancy and preadaptation. At least four distinct sorts of redundancy are identified: (i) redundancy arising through duplication (amplification); (ii) redundancy arising through regionalisation (parcellation); (iii) redundancy arising through functional convergence; and (iv) redundancy arising from shared function (functional degeneracy). Although organisms are here recognised to be functionally constrained ("burdened", in Riedl's terminology), these constraints can be overcome through the combination of the four principles given above. Contrary to its common treatment, functional constraint is neither an ever-increasing restriction on the scope of evolution, nor does it require drastic events to overcome or "break" it. Rather, it is an evolutionary quantity, subject to selection at some level. The rules that govern morphological evolution are the primary controls on what is allowed to happen in the evolution of the overall genotype-phenotype system, suggesting strong controls on the sorts of developmental changes that might be associated with macroevolution. This model, then, sees organism functionality as the primary control on evolvability, with exact genetic make-up being of secondary importance. It should prove possible to recast traditional notions of body-plan evolution into the formulations of complex system analysis, which in the future may prove a unifying discipline for fields as disparate as palaeontology and gene regulatory networks. In particular, understanding how morphology can evolve may provide the critical link between the ecological and morphological networks that are currently the intense focus of evolutionary investigations.     

On the evolution of non-specific mutualism

It has been argued that mutualisms are non-specific when mutualistic interactions are weak and transient, and become more specific as interactions increase in strength. However, this runs counter to the observation that there exist tightly linked mutualisms of great antiquity that are highly nonspecific. Here we argue that mutualism generates positive, interspecific, frequency-dependent selection, which acts as a cohesive evolutionary force, discouraging evolution of specificity. A simple mathematical model is constructed to analyse the evolution of a community consisting of two guilds of species with mutualistic between-guild interactions, two competing species in each guild and two genetically distinct phenotypes within each species. With some simplifying assumptions, the trajectories in the neighbourhood of the only interior equilibrium point are determined analytically in terms of interactions between individuals. These show that the equilibrium is locally stable (no evolution) when there is little differentiation between phenotypes in mutualistic and interspecific, competitive interactions. On the other hand, when there is strong differentiation between phenotypes in their mutualistic interactions, the equilibrium is unstable and the community starts to evolve towards non-specificity. There are, however, two forces counteracting this tendency which, if sufficiently potent, cause evolution towards specificity. The first is generated by strong differentiation between phenotypes in interspecific competition; the second is caused by specificity which already exists between species in their mutualistic interactions. Thus, the tendency for non-specificity or specificity to evolve depends on the interplay between antagonistic and mutualistic interactions in the community. We illustrate these results with some numerical examples and, finally, survey some data on specificity of mutualisms in the light of the analysis.     

Natural selection on extrafloral nectar production in Chamaecrista fasciculata: the costs and benefits of a mutualism trait

Cost-benefit models of the evolution of mutualism predict that the current state of mutualism results from trade-offs between fitness costs of mutualist traits and the fitness benefits of association. We test the assumptions of such models by measuring patterns of natural selection on a mutualist trait, extrafloral nectar production in Chamaecrista fasciculata. Selection was measured on plants from which ants had been excluded (removing the mutualist benefit of the trait), from which all insects had been excluded (removing costs of herbivory in addition to mutualist benefits), and unmanipulated plants (where both costs and benefits were present). Selection analysis based on half-sibling-mean regressions of fitness on the trait revealed no evidence of costs of extrafloral nectar production in the absence of all insects or in the absence of ants. However, examination of the selective surfaces for these treatments suggest that costs of nectar production may exist and are exacerbated by the presence of herbivory. In the presence of ants, natural selection favors high extrafloral nectar production, consistent with a fitness benefit to this mutualist trait in the presence of the mutualist partner. In this study, the interaction of costs and benefits did not produce an evolutionary optimum for the trait within the range of variation observed, suggesting that application of a cost-benefit framework to this trait will benefit from considering the influence of temporal and spatial variation on the quality of costs and benefits.     

A general model for the evolution of mutualisms

The evolution of mutualisms presents a puzzle. Why does selection favour cooperation among species rather than cheaters that accept benefits but provide nothing in return? Here we present a general model that predicts three key factors will be important in mutualism evolution: (i) high benefit to cost ratio, (ii) high within‐species relatedness and (iii) high between‐species fidelity. These factors operate by moderating three types of feedback benefit from mutualism: cooperator association, partner‐fidelity feedback and partner choice. In defining the relationship between these processes, our model also allows an assessment of their relative importance. Importantly, the model suggests that phenotypic feedbacks (partner‐fidelity feedback, partner choice) are a more important explanation for between‐species cooperation than the development of genetic correlations among species (cooperator association). We explain the relationship of our model to existing theories and discuss the empirical evidence for our predictions.     

Macroevolutionary patterns in the origin of mutualisms involving ants

Ants are a diverse and abundant insect group that form mutualistic associations with a number of different organisms from fungi to insects and plants. Here, we use a phylogenetic approach to identify ecological factors that explain macroevolutionary trends in the mutualism between ants and honeydew-producing Homoptera. We also consider association between ant-Homoptera, ant-fungi and ant-plant mutualisms. Homoptera-tending ants are more likely to be forest dwelling, polygynous, ecologically dominant and arboreal nesting with large colonies of 10(4)-10(5) individuals. Mutualistic ants (including those that garden fungi and inhabit ant-plants) are found in under half of the formicid subfamilies. At the genus level, however, we find a negative association between ant-Homoptera and ant-fungi mutualisms, whereas there is a positive association between ant-Homoptera and ant-plant mutualisms. We suggest that species can only specialize in multiple mutualisms simultaneously when there is no trade-off in requirements from the different partners and no redundancy of rewards.     

A seed predator drives the evolution of a seed dispersal mutualism

Although antagonists are hypothesized to impede the evolution of mutualisms, they may simultaneously exert selection favouring the evolution of alternative mutualistic interactions. We found that increases in limber pine (Pinus flexilis) seed defences arising from selection exerted by a pre-dispersal seed predator (red squirrel Tamiasciurus hudsonicus) reduced the efficacy of limber pine's primary seed disperser (Clark's nutcracker Nucifraga columbiana) while enhancing seed dispersal by ground-foraging scatter-hoarding rodents (Peromyscus). Thus, there is a shift from relying on primary seed dispersal by birds in areas without red squirrels, to an increasing reliance on secondary seed dispersal by scatter-hoarding rodents in areas with red squirrels. Seed predators can therefore drive the evolution of seed defences, which in turn favour alternative seed dispersal mutualisms that lead to major changes in the mode of seed dispersal. Given that adaptive evolution in response to antagonists frequently impedes one kind of mutualistic interaction, the evolution of alternative mutualistic interactions may be a common by-product.     

An ant—treehopper mutualism: effects of Formica subsericea on the survival of Vanduzea arquata

Abstract. 1. The numbers of Formica subsericea (Say) were positively correlated with those of the treehopper, Vanduzea arquata Say on branches of black locust.
2. The mean numbers of V.arquata on branches were greater in the second than in the first generation. However, the mean number of ants tending them was significantly lower in the second compared to the first generation.
3. Defoliation of branches resulted in a reduction in the number of mem-bracids on branches and ant numbers declined similarly.
4. Survival of V.arquata was significantly greater when tended by F.subsericea than when ants were exciuded.
5. Ant attendance significantly reduced the number of predators on branches with _Karquata compared to branches lacking both ants and treehoppers. This, in part, explains the greater survival of V.arquata nymphs tended by ants.     

Extreme environmental variation sharpens selection that drives the evolution of a mutualism

The importance of infrequent events for both adaptive evolution and the evolution of species interactions is largely unknown. We investigated how the infrequent production of large seed crops (masting) of a bird-dispersed tree (whitebark pine, Pinus albicaulis) influenced phenotypic selection exerted by its primary avian seed predator-disperser, the Clark's nutcracker (Nucifraga columbiana). Selection was not evident during common years of low seed abundance, whereas it was replicated among areas and favoured traits facilitating seed dispersal during infrequent years of high seed abundance. Since nutcrackers act mostly as seed predators during small seed crops but as seed dispersers during the largest seed crops, trees experienced strong selection from nutcrackers only during infrequent years when the interaction was most strongly mutualistic. Infrequent events can thus be essential to both adaptive evolution and the evolutionary dynamics of species interactions.     

Insect life history and the evolution of bacterial mutualism

Bacterial symbiosis has played a fundamental role in the evolution of eukaryotes. However, we still know little about how cooperative relationships with bacteria originate, and why they form in some host species but not others. Facultative symbionts that are beneficial, but not essential, provide unique insights into these processes. We use data from over a hundred aphid species to test if host life history is associated with the presence of facultative symbionts. We find that aphid species that have mutualistic associations with ants that protect them from natural enemies are less likely to carry symbionts that provide similar benefits. We also find one symbiont species occurs more frequently in unrelated aphid species that specialise on certain plant genera. In addition, aphid species that attack multiple plants often carry different symbiont complements. Our findings provide evidence of the ecological conditions that facilitate stable, mutually beneficial relationships between microbes and eukaryotic hosts.     

Molecular phylogenies of fig pollinating and non-pollinating wasps and the implications for the origin and evolution of the fig-fig wasp mutualism

Abstract. Figs host three ecologically distinct groups of wasps: pollinators, non-pollinators (parasitic wasps) and parasitoids. Both pollinators and non-pollinators complete their life cycles using fig tissue, while parasitoids appear to attack some groups of non-pollinators. We used nucleotide sequence data to address a series of questions concerning genealogical associations, host specificities and degree of strict-sense co-evolution exhibited by members of these groups. We used the relatively conserved 12S rRNA gene of the mitochondria to estimate high level relationships among pollinator, parasitic and parasitoid taxa by sampling species collected from host figs representing five sections (three subgenera) from Asia, Africa, Europe and Central America. We found that all pollinators formed a clear monophyletic group. However, we could not resolve whether or not all of the non-parasitoid wasps associated with figs (Agaonidae, sensu Bouček) formed a single monophyletic group. Further, we used the more variable COII mitochondrial gene to attempt to determine relationships among closely related species of pollinators within two New World genera. Using sequences from the same gene we estimated the phylogenetic relationships among the parasites collected from the same New World host fig species and compared them with those of the pollinators. At fine taxonomic scale, we found that for both pollinator and parasites, species were generally specific to a given fig host. Moreover, the phylogenies of the non-pollinators are largely congruent with those of the pollinators, suggesting the predominance of strict-sense co-evolution on shared host fig species. The implications of these findings and opportunities for future research are discussed.     

Testing the out-of-Florida hypothesis on the origin of cheating in the yucca-yucca moth mutualism

Mutualistic interactions can be exploited by cheaters that take the rewards offered by mutualists without providing services in return. The evolution of cheater species from mutualist ancestors is thought to be possible under particular ecological conditions. Here we provide a test of the first explicit model of the transition from mutualism to antagonism. We used the obligate pollination mutualism between yuccas and yucca moths to examine the origins of a nonpollinating cheater moth, Tegeticula intermedia, and its pollinating sister species, T. cassandra. Based on geographic distribution and ecological factors affecting the pollinators, previous research had indicated that the cheaters evolved in Florida as a result of sympatry of T. cassandra and another pollinator species. We used mitochondrial DNA (mtDNA) sequences and amplified fragment length polymorphism (AFLP) data to investigate the phylogeographic history of the pollinator-cheater sister pair and to test whether the cheaters arose in Florida. Contrary to predictions, phylogenetic and population genetic analyses suggested that the cheaters evolved in the western United States and subsequently spread eastward. Western populations of cheaters had the most ancestral haplotypes and the highest genetic diversity, and there was also significant genetic structure associated with a geographic split between eastern and western populations. In comparison, there was evidence for weak genetic structure between northern and southern pollinator populations, suggesting a long history in Florida. The western origin of the cheaters indicated that the pollinators have more recently become restricted to the southeastern United States. This was supported by AFLP analyses that indicated that the pollinators were more closely related to the western cheaters than they were to geographically proximate cheaters in the east. Shared mtDNA between pollinators and eastern cheaters suggested hybridization, possibly in a secondary contact zone. The results negate the out-of-Florida hypothesis and reveal instead a long, complex, and disparate history for the pollinator-cheater sister pair.     

Ecological factors promoting the evolution of colony defense in aphids: computer simulations

Summary Colony defense has been reported in a limited number of species of aphids. This paper examines which life-historical traits have promoted the evolution of colony defense using two kinds of deterministic simulation models. These models postulate that first-instar larvae can counterattack predators and that the duration of this instar stage is a variable, subject to selection. Prolonging the first-instar span increases the proportion of defenders in the colony, while it results in a delay in reproduction. By calculating the optimal first-instar span, the optimal defensive effort of a colony under various ecological conditions could be estimated. Simulations based on the general model, which regards the number of adults maturing in a period as performance, predicted that a lower birthrate leads to a longer first-instar span (larger investment in defense). This condition also allowed the evolution of dimorphism in the first-instar span, which may ultimately result in the appearance of soldiers. Where birthrate declines with time, the first-instar span was predicted to be prolonged in later stages. Colony duration had little influence on the optimal first-instar span if the season is long enough to repeat generations. The galling-aphid model that assumes a fixed number of generations predicted that a longer duration of colonies leads to a longer first-instar span, but that birthrate has little influence on the optimal first-instar span. A tendency in defense reported in pemphigid aphids was consistent with the prediction from the galling-aphid model.     

Variation in mutualisms: the spatiotemporal mosaic of a pollinator assemblage

Variation in time (annual and seasonal) and space (between- and within-population) is examined for the pollinator assemblage of Lavandula latifolia (Labiatae), an insect-pollinated, summer- flowering, evergreen shrub of Mediterranean woodlands in southeastern Spain. Lavandula latifolia is pollinated there by nearly 85 species of comparatively long-tongued Hymenoptera, Diptera and Lepidoptera. The diversity, composition and abundance of pollinators varied markedly between years. Lepidopteran taxa prevailed numerically in one year, hymenopterans in four years, and both groups had similar abundance in the remaining year. The vast majority of pollinators exhibited significant annual differences in average abundance. Only 35.7% of taxa were recorded in all of the six study years. The pollinator assemblage had marked seasonal dynamics. Important changes in species richness, abundance and composition took place over the flowering season of L. latifolia (nearly 3 months). Only 21.7% of insect taxa occurred throughout the flowering season. Lavandula latifolia populations at different distances from water courses differed broadly in the abundance and composition of pollinators. Hymenopterans dominated numerically at the water-distant sites, whereas lepidopterans prevailed in populations growing in the vicinity of streams. Only 40.7% of taxa were recorded at all of the four study populations. Within the same plant population, horizontal distances of the order of 25 m resulted in significant changes in pollinator composition. Variations at the four scales considered combine to produce, from the viewpoint of L. latifolia, a spatio-temporal mosaic of pollinators. As these differ broadly in frequency of pollen transfer, size of pollen loads deposited, and between-flower flight distance patterns, spatio-temporal variation will predictably result in inconsistent or contradictory selective pressures on the plant, thus hindering specialization in relation to particular pollinators.     

Seasonal changes in the response of wood-ants (Formica lugubris) to sucrose baits

Abstract. 1. The acceptability of sucrose solutions to Formica lugubris Zett. in the field was tested by offering droplets of known concentrations to ants tending aphids.
2. A probit model fitted to the data allowed the computation of the Median Effective Concentration (ED₅₀) and its confidence limits.
3. In spring and early summer ED₅₀ was about 0.15 M sucrose, but the ED₅₀ rose in 1 week at the end of June from 0.2 M to 0.9 M. The change was simultaneous on pine and birch trees. The ED₅₀ fell gradually to about 0.4 M in early November.
4. The increase in ED₅₀ is related to the production of the summer apterae in the aphids tended, Cinara pini (L.) on pines and Symydobius oblongus (von Heyden) on birch. This increases the 'quality' of food resource so that low sucrose concentrations can no longer compete for ant attendance.
5. The increase in ED₅₀ may limit the attendance of wood-ants at the nectaries of bracken, Pteridium aquilinum (L.) Kuhn. and at colonies of some other aphid species which are attended only in early summer.     

How to become a yucca moth: minimal trait evolution needed to establish the obligate pollination mutualism

The origins of obligate pollination mutualisms, such as the classic yucca–yucca moth association, appear to require extensive trait evolution and specialization. To understand the extent to which traits truly evolved as part of establishing the mutualistic relationship, rather than being pre‐adaptations, we used an expanded phylogenetic estimate with improved sampling of deeply‐diverged groups to perform the first formal reconstruction of trait evolution in pollinating yucca moths and their nonpollinating relatives. Our analysis demonstrates that key life‐history traits of yucca moths, including larval feeding in the floral ovary and the associated specialized cutting ovipositor, as well as colonization of woody monocots in xeric habitats, may have been established before the obligate mutualism with yuccas. Given these pre‐existing traits, novel traits in the mutualist moths are limited to the active pollination behaviours and the tentacular appendages that facilitate pollen collection and deposition. These results suggest that a highly specialized obligate mutualism was built on the foundation of pre‐existing interactions between early Prodoxidae and their host plants, and arose with minimal trait evolution. © 2010 The Linnean Society of London, Biological Journal of the Linnean Society, 2010, 100 , 847–855.     

Pollination and seed predation by moths on Silene and allied Caryophyllaceae: evaluating a model system to study the evolution of mutualisms

Nursery pollinators, and the plants they use as hosts for offspring development, function as exemplary models of coevolutionary mutualism. The two pre-eminent examples--fig wasps and yucca moths--show little variation in the interaction: the primary pollinator is an obligate mutualist. By contrast, nursery pollination of certain Caryophyllaceae, including Silene spp., by two nocturnal moth genera, Hadena and Perizoma, ranges from antagonistic to potentially mutualistic, offering an opportunity to test hypotheses about the factors that promote or discourage the evolution of mutualism. Here, we review nursery pollination and host-plant interactions in over 30 caryophyllaceous plants, based on published studies and a survey of researchers investigating pollination, seed predation, and moth morphology and behavior. We detected little direct evidence of mutualism in these moth-plant interactions, but found traits and patterns in both that are nonetheless consistent with the evolution of mutualism and merit further attention.     

The influence of diet on growth and secretion behaviour of myrmecophilous Polyommatus icarus caterpillars (Lepidoptera: Lycaenidae)

Abstract.

• 1 Caterpillars of the facultatively myrmecophilous butterfly Polyommatus icarus were reared on inflorescences, or foliage, of four natural hostplant species and on an artificial diet to study dietary effects on larval growth and secretory capacity.
• 2 Caterpillars achieved highest weights and relative growth rates when fed flowers of Medicago sativa, Lotus corniculatus or Melilotus officinalis. Larvae reared on Coroniüa varia (flowers and leaves), foliage of M.sativa and on the artificial diet pupated at lower weights and achieved lower growth rates.
• 3 In standardized experiments with the ant species Lasius flavus, secretion rates from the dorsal nectar organ (DNO) were 2 times higher among flower-fed caterpillars than among foliage-fed siblings or caterpillars on the artificial diet. Larvae reared on C.varia flowers were superior to all other food treatments with respect to secretion rates.
• 4 High water content of larval diet, as in flowers, appears to be important for lycaenid caterpillars to achieve high secretion rates, whereas the correlation between myrmecophily and nutrient availability, as evidenced by growth rates, was less pronounced.
• 5 Using experimental data on larval growth and secretion rates, the lifetime volume of secretions from the DNO is estimated to range from 2 to 5 μl in most food treatments. Only on C.varia flowers (5.5–8.7 μl) and on M.sativa leaves (0.9–1.1 μl) did the caterpillars deviate in their absolute investment in myrmecophily.
• 6 The estimated lifetime investment accounted for 1.6–5.5% of prepupal fresh weight in all food treatments except on C.varia flowers (7.8–12.3%).

     

Assessing current adaptation and phylogenetic inertia as explanations of trait evolution: the need for controlled comparisons

The determination of whether the pattern of trait evolution observed in a comparative analysis of species data is due to adaptation to current environments, to phylogenetic inertia, or to both of these forces requires that one control for the effects of either force when making an assessment of the evolutionary role of the other. Orzack and Sober (2001) developed the method of controlled comparisons to make such assessments; their implementation of the method focussed on a discretely varying trait. Here, we show that the method of controlled comparisons can be viewed as a meta-method, which can be implemented in many ways. We discuss which recent methods for the comparative analysis of continuously distributed traits can generate controlled comparisons and can thereby be used to properly assess whether current adaptation and/or phylogenetic inertia have influenced a trait's evolution. The implementation of controlled comparisons is illustrated by an analysis of sex-ratio data for fig wasps. This analysis suggests that current adaptation and phylogenetic inertia influence this trait.