Constraints on adaptation of Escherichia coli to mixed‐resource environments increase over time

Can a population evolved in two resources reach the same fitness in both as specialist populations evolved in each of the individual resources? This question is central to theories of ecological specialization, the maintenance of genetic variation, and sympatric speciation, yet relatively few experiments have examined costs of generalism over long‐term adaptation. We tested whether selection in environments containing two resources limits a population's ability to adapt to the individual resources by comparing the fitness of replicate Escherichia coli populations evolved for 6000 generations in the presence of glucose or lactose alone (specialists), or in varying presentations of glucose and lactose together (generalists). We found that all populations had significant fitness increases in both resources, though the magnitude and rate of these increases differed. For the first 4000 generations, most generalist populations increased in fitness as quickly in the individual resources as the corresponding specialist populations. From 5000 generations, however, a widespread cost of adaptation affected all generalists, indicating a growing constraint on their abilities to adapt to two resources simultaneously. Our results indicate that costs of generalism are prevalent, but may influence evolutionary trajectories only after a period of cost‐free adaptation.     

Nested diets: a novel pattern of individual-level resource use

Many generalist populations may actually be composed of relatively specialist individuals. This 'individual specialization' may have important ecological and evolutionary implications. Although this phenomenon has been documented in more than one hundred taxa, it is still unclear how individuals within a population actually partition resources. Here we applied several methods based on network theory to investigate the intrapopulation patterns of resource use in the gracile mouse opossum Gracilinanus microtarsus . We found evidence of significant individual specialization in this species and that the diets of specialists are nested within the diets of generalists. This novel pattern is consistent with a recently proposed model of optimal foraging and implies strong asymmetry in the interactions among individuals of a population.     

Incomplete division of labor: error-prone multitaskers coexist with specialists

Division of labor (DoL) occurs when individual members of a group specialize by performing particular tasks toward some common goal. Under complete DoL, every individual acts as a specialist and so performs only one kind of task. But under incomplete DoL, some individuals may act as generalists and so have the capacity to perform more than one kind of task. This persistence of generalists in the presence of specialists presents a theoretical challenge, particularly if generalists must pay an extra cost, an inefficiency penalty, for their capacity to perform more than one type of task. Prior work focused on how such costs tend to drive evolution toward complete DoL, with only specialists typically remaining at equilibrium [Wahl, L.M., 2002a. Evolving the division of labor: generalists, specialists and task allocation. J. Theoret. Biol. 219, 371-388; Wahl, L.M., 2002b. The division of labor: genotypic versus phenotypic specialization. Am. Nat. 160, 135-145]. Relaxing this key assumption, we show that generalists, despite paying some extra costs, can coexist with specialists. Relaxing another assumption, we also show that this coexistence can hold even when generalists often perform the wrong task. How can stable multitasking emerge despite this flawed decision-making? From the perspective that cognitive errors matter only when they translate into fitness decrements, we observe that error-prone generalists may persist most commonly in situations in which their mistakes do little to jeopardize group success. Our findings show that incomplete DoL can emerge even when generalists often err and must pay extra costs for their multitasking capacity.     

Habitat loss, resource specialization, and extinction on coral reefs

Coral reefs worldwide are being degraded because of global warming (coral bleaching) and coastal development (sedimentation and eutrophication). Predicting the risk of species extinctions from this type of habitat degradation is one of the most challenging and urgent tasks facing ecologists. Habitat specialists are thought to be more prone to extinction than generalists; however, specialists may be more susceptible to extinction because (1) they are specialists per se, (2) they are less abundant than generalists, or (3) both. Here, I show that declines in coral abundance lead to corresponding declines in the abundance of coral‐dwelling fishes, but with proportionally greater losses to specialists than generalists. In addition, specialists have smaller initial population sizes than generalists. Consequently, specialists face a dual risk of extinction because their already small populations decline more rapidly than those of generalists. Corresponding with this increased extinction risk, I describe the local extinction of one specialist species and the near‐global extinction of another species. I conclude that habitat specialists will be the first species lost from coral reefs because their small populations suffer the most from human‐induced disturbances.     

Increased genetic differentiation in a specialist versus a generalist bee: implications for conservation

Oligolectic bees are specialists that collect pollen from one or a few closely related species of plants, while polylectic bees are generalists that collect pollen from both related and unrelated species of plants. Because of their more restricted range of floral hosts, it is expected that specialists persist in more isolated populations than do generalists. We present data on the population structure of two closely related bee species sampled from a super abundant floral host in the southern Atacama Desert. Pairwise comparisons of population subdivision over identical distances revealed that the specialist bee had significantly more differentiated populations in comparison to the generalist. Further, populations of the specialist had significantly less genetic variation, measured as observed and expected heterozgyosity, than those of the generalist. Our data support the hypothesis of decreased gene flow among populations of the specialist bee even at equivalent geographic distances. The resulting reductions in effective population size for specialists make them particularly prone to extinction due to both demographic and genetic reasons. Our findings have important implications for the conservation of bees and other specialist insects. Deceased     

Does habitat specialization shape the evolutionary potential of wild bird populations?

Because specialist species evolved in more temporally and spatially homogeneous environments than generalist species, they are supposed to experience less fluctuating selection. For this reason, we expect specialists to show lower overall genetic variation as compared to generalists. We also expect populations from specialist species to be smaller and more fragmented, with lower neutral genetic diversity. We tested these hypotheses by investigating patterns of genetic diversity along a habitat specialization gradient in wild birds, based on estimates of heritability, coefficients of variation of additive genetic variance, and heterozygosity available in the literature. We found no significant effect of habitat specialization on any of the quantitative genetic estimators but generalists had higher heterozygosity. This effect was mainly a consequence of the larger population size of generalists. Our results suggest that evolutionary potential does not differ at the population level between generalist and specialist species, but the trend observed in heterozygosity levels and population sizes may explain their difference in susceptibility to extinction.     

Host and habitat specialization of avian malaria in Africa

Studies of both vertebrates and invertebrates have suggested that specialists, as compared to generalists, are likely to suffer more serious declines in response to environmental change. Less is known about the effects of environmental conditions on specialist versus generalist parasites. Here, we study the evolutionary strategies of malaria parasites (Plasmodium spp.) among different bird host communities. We determined the parasite diversity and prevalence of avian malaria in three bird communities in the lowland forests in Cameroon, highland forests in East Africa and fynbos in South Africa. We calculated the host specificity index of parasites to examine the range of hosts parasitized as a function of the habitat and investigated the phylogenetic relationships of parasites. First, using phylogenetic and ancestral reconstruction analyses, we found an evolutionary tendency for generalist malaria parasites to become specialists. The transition rate at which generalists become specialists was nearly four times as great as the rate at which specialists become generalists. We also found more specialist parasites and greater parasite diversity in African lowland rainforests as compared to the more climatically variable habitats of the fynbos and the highland forests. Thus, with environmental changes, we anticipate a change in the distribution of both specialist and generalist parasites with potential impacts on bird communities.     

Evolutionary increases in defense during a biological invasion

Invasive plants generally escape from specialist herbivores of their native ranges but may experience serious damage from generalists. As a result, invasive plants may evolve increased resistance to generalists and tolerance to damage. To test these hypotheses, we carried out a common garden experiment comparing 15 invasive populations with 13 native populations of Chromolaena odorata, including putative source populations identified with molecular methods and binary choice feeding experiments using three generalist herbivores. Plants from invasive populations of C. odorata had both higher resistance to three generalists and higher tolerance to simulated herbivory (shoot removal) than plants from native populations. The higher resistance of plants from invasive populations was associated with higher leaf C content and densities of leaf trichomes and glandular scales, and lower leaf N and water contents. Growth costs were detected for tolerance but not for resistance, and plants from invasive populations of C. odorata showed lower growth costs of tolerance. Our results suggest that invasive plants may evolve to increase both resistance to generalists and tolerance to damage in introduced ranges, especially when the defense traits have low or no fitness costs. Greater defenses in invasive populations may facilitate invasion by C. odorata by reducing generalist impacts and increasing compensatory growth after damage has occurred.     

Is specialization an evolutionary dead end? Testing for differences in speciation,extinction and trait transition rates across diverse phylogenies of specialists and generalists

Specialization has often been claimed to be an evolutionary dead end, with specialist lineages having a reduced capacity to persist or diversify. In a phylogenetic comparative framework, an evolutionary dead end may be detectable from the phylogenetic distribution of specialists, if specialists rarely give rise to large, diverse clades. Previous phylogenetic studies of the influence of specialization on macroevolutionary processes have demonstrated a range of patterns, including examples where specialists have both higher and lower diversification rates than generalists, as well as examples where the rates of evolutionary transitions from generalists to specialists are higher, lower or equal to transitions from specialists to generalists. Here, we wish to ask whether these varied answers are due to the differences in macroevolutionary processes in different clades, or partly due to differences in methodology. We analysed ten phylogenies containing multiple independent origins of specialization and quantified the phylogenetic distribution of specialists by applying a common set of metrics to all datasets. We compared the tip branch lengths of specialists to generalists, the size of specialist clades arising from each evolutionary origin of a specialized trait and whether specialists tend to be clustered or scattered on phylogenies. For each of these measures, we compared the observed values to expectations under null models of trait evolution and expected outcomes under alternative macroevolutionary scenarios. We found that specialization is sometimes an evolutionary dead end: in two of the ten case studies (pollinator‐specific plants and host‐specific flies), specialization is associated with a reduced rate of diversification or trait persistence. However, in the majority of studies, we could not distinguish the observed phylogenetic distribution of specialists from null models in which specialization has no effect on diversification or trait persistence.     

How parasites can promote the expression of social behaviour in their hosts

Recent theory on the role of parasites in the evolution of social behaviour has emphasized the costs of social behaviour to hosts. However, parasites whose primary effect on host fitness is to reduce fecundity can favour the evolutionary origin or maintenance of social behaviour, including eusociality, under certain conditions. If the parasites are not readily transmitted among members of social groups, then other group members will not be selected to reject infected individuals as social partners, nor will adaptive suicide or avoidance of grouping be selectively favoured for infected individuals. Rather, total or partial parasitic castration may promote the expression of helping behaviour by infected individuals. Some parasites may therefore act to increase variance in direct reproductive value within populations or societies, and to promote reproductive division of labour. The necessary conditions of reduced host fecundity and low within-group transmission are met in some insect-parasite systems, and could occur in other host-parasite systems as well.     

Variation in the degree of specialization can maintain local diversity in model communities

We hypothesize that the continuum between generalist and specialist adaptations is an important general trade-off axis in the maintenance of local diversity, and we explore this idea with a simple model in which there are patch types to which species arrive as propagules and compete. Each patch type is defined by a competitive ranking of all species. A highly specialist species is the top competitor in one patch type but has a relatively low average ranking across different patch types, while a generalist species has a high average rank across patch types but is not the top competitor in any patch type. We use random dispersal and vary the fecundity of all species together to vary total propagule density and therefore recruitment limitation and density-dependent mortality. When fecundity is very high, each patch becomes occupied by its specialist species and generalists go extinct, so the number of species at equilibrium is equal to the number of patch types. If fecundity is very low, generalists dominate and specialists go extinct. There is a range of fecundity levels in which specialists, generalists, and intermediates coexist, and the number of species is substantially greater than the number of patch types. While coexistence of specialists and generalists has been considered a problem in evolutionary ecology, our results suggest to the contrary that this trade-off contributes to the maintenance of local diversity.     

Colony size predicts division of labour in attine ants

Division of labour is central to the ecological success of eusocial insects, yet the evolutionary factors driving increases in complexity in division of labour are little known. The size–complexity hypothesis proposes that, as larger colonies evolve, both non-reproductive and reproductive division of labour become more complex as workers and queens act to maximize inclusive fitness. Using a statistically robust phylogenetic comparative analysis of social and environmental traits of species within the ant tribe Attini, we show that colony size is positively related to both non-reproductive (worker size variation) and reproductive (queen–worker dimorphism) division of labour. The results also suggested that colony size acts on non-reproductive and reproductive division of labour in different ways. Environmental factors, including measures of variation in temperature and precipitation, had no significant effects on any division of labour measure or colony size. Overall, these results support the size–complexity hypothesis for the evolution of social complexity and division of labour in eusocial insects. Determining the evolutionary drivers of colony size may help contribute to our understanding of the evolution of social complexity.     

Individual advantages to ecological specialization: insights on cognitive constraints from three conspecific taxa

The information-processing hypothesis (IPH) posits that specialist herbivores should make host-associated decisions more effectively than generalists and thus enjoy associated fitness advantages that may help explain the evolutionary prevalence of host-specific insects. This is because generalists must evaluate a greater diversity of host plants/cues than specialists and thus face a cognitive challenge that is predicted to constrain the efficiency and accuracy of their choices. Here, we present the first individual-level evaluation of this hypothesis. This involved experimentally quantifying the specificity, efficiency, and accuracy of host selection, as both larvae and adults, for many individuals representing each of three 'host forms' of Neochlamisus bebbianae leaf beetles. These experiments provided several significant findings: host forms differed in larval specificity, with the more specialized host forms more efficiently and accurately selecting optimal hosts as both larvae and adults. Positive correlations between larval specificity and both efficiency and accuracy across test individuals provided the most direct evidence to date for a biological association between these variables. Our results thus provide strong and consistent support for the IPH at the level of both populations and individuals. Because individual N. bebbianae make many host-associated decisions in nature, our results suggest that cognitive constraints may play a major role in the evolutionary dynamics of ongoing ecological specialization and diversification in this species.     

Comparative analysis of quantitative trait loci controlling glucosinolates,myrosinase and insect resistance in Arabidopsis thaliana

Evolutionary interactions among insect herbivores and plant chemical defenses have generated systems where plant compounds have opposing fitness consequences for host plants, depending on attack by various insect herbivores. This interplay complicates understanding of fitness costs and benefits of plant chemical defenses. We are studying the role of the glucosinolate-myrosinase chemical defense system in protecting Arabidopsis thaliana from specialist and generalist insect herbivory. We used two Arabidopsis recombinant inbred populations in which we had previously mapped QTL controlling variation in the glucosinolate-myrosinase system. In this study we mapped QTL controlling resistance to specialist (Plutella xylostella) and generalist (Trichoplusia ni) herbivores. We identified a number of QTL that are specific to one herbivore or the other, as well as a single QTL that controls resistance to both insects. Comparison of QTL for herbivory, glucosinolates, and myrosinase showed that T. ni herbivory is strongly deterred by higher glucosinolate levels, faster breakdown rates, and specific chemical structures. In contrast, P. xylostella herbivory is uncorrelated with variation in the glucosinolate-myrosinase system. This agrees with evolutionary theory stating that specialist insects may overcome host plant chemical defenses, whereas generalists will be sensitive to these same defenses.     

Predator–prey systems in streams and rivers

Many predator–prey systems are found in environments with a predominantly unidirectional flow such as streams and rivers. Alterations of natural flow regimes (e.g., due to human management or global warming) put biological populations at risk. The aim of this paper is to devise a simple method that links flow speeds (currents) with population retention (persistence) and wash-out (extinction). We consider systems of prey and specialist, as well as generalist, predators, for which we distinguish the following flow speed scenarios: (a) coexistence, (b) persistence of prey only or (c) predators only (provided they are generalists), and (d) extinction of both populations. The method is based on a reaction–advection–diffusion model and traveling wave speed approximations. We show that this approach matches well spread rates observed in numerical simulations. The results from this paper can provide a useful tool in the assessment of instream flow needs, estimating the flow speed necessary for preserving riverine populations.     

Insights on the functional composition of specialist and generalist birds throughout continuous and fragmented forests

A decline in species number often occurs after forest fragmentation and habitat loss, which usually results in the loss of ecological functions and a reduction in functional diversity in the forest fragments. However, it is uncertain whether these lost ecological functions are consistently maintained throughout continuous forests, and so the importance of these functions in continuous forests remains unknown. Point counts were used to assess both the taxonomic and functional diversity of specialist and generalist birds from sampling in a continuous primary forest compared with forest fragments in order to investigate the responses of these groups to forest fragmentation. We also measured alpha and beta diversity. The responses of specialists and generalists were similar when we assessed all bird species but were different when only passerines were considered. When examining passerines we found lower total taxonomic beta diversity for specialists than for generalists in the continuous forest, while taxonomic beta diversity was higher in the fragmented forest and similar between bird groups. However, total functional beta‐diversity values indicated clearly higher trait regularity in continuous forest for specialists and higher trait regularity in fragments for generalists. Specialists showed significantly higher functional alpha diversity in comparison with generalists in the continuous forest, while both groups showed similar values in fragments. In passerines, species richness and alpha functional diversity of both specialist and generalist were explained by forest connectivity; but, only fragment size explained those parameters for specialist passerines. We suggest that considering subsets of the community with high similarity among species, as passerines, provides a better tool for understanding responses to forest fragmentation. Due to the regularity of specialists in continuous forest, their lost could highly affect functionality in forest fragments.     

Mistletoe specialist frugivores: latterday ‘Johnny Appleseeds’ or self-serving market gardeners?

Many plants use birds to disperse their propagules, but mistletoes are especially reliant on their services. As aerial parasites, mistletoe seeds need to be deposited upon branches of suitable hosts, and mistletoe specialist frugivores (from eight different avian families) have long been regarded as their coevolved dispersers. Like the pioneer Johnny ‘Appleseed’ Chapman who established nurseries that helped open up land for settlement, these birds are considered benevolent dispersers of this keystone resource and often invoked as illustrative examples of mutualistic interactions. We have compared recent research on these specialists with studies of other birds with broader diets (generalists) which also disperse mistletoe seed. Rather than mutualists, we suggest that mistletoe specialist frugivores are better considered exploitative, with multiple lineages evolving independently to capitalize on this reliable, nutritious resource. Although mistletoe specialist frugivores are quantitatively important seed dispersers in some regions, their specialized diet restricts them to areas with high mistletoe densities, resulting in contagious dispersal patterns. By intensifying existing infections, mistletoe specialist frugivores increase their own medium-term food security—akin to market gardeners profiting from intensive cultivation. Exploring the ecological and evolutionary implications of this proposition, we evaluate the consequences of different dispersal patterns on mistletoe fitness and highlight the neglected role of dietary generalists in the stabilization of plant–animal interactions.     

Task allocation in ant colonies within variable environments (A study of temporal polyethism: Experimental)

We briefly review the literature on the division of labour in ant colonies with monomorphic worker populations, and show that there are anomalies in current theories and in the interpretation of existing data sets. Most ant colonies are likely to be in unstable situations and therefore we doubt if an age-based division of labour can be sufficiently flexible. We present data for a type of small ant colony in a highly seasonal environment, concentrating on individually marked older workers. We show that contrary to expectation such workers undertake a wide variety of tasks and can even retain their ability to reproduce, even whilst younger workers are actively foraging. Our analysis shows that old workers occupy four distinct spatial stations within the nest and that these are related to the tasks they perform. We suggest that correlations between age and task in many ant colonies might simply be based on ants foraging for work, i.e. actively seeking tasks to perform and remaining faithful to these as long as they are profitably employed. For this reason, employed older workers effectively displace unemployed younger workers into other tasks. In a companion paper, Tofts 1993,Bull. math. Biol. develops an algorithm that shows how foraging for work can be an efficient and flexible mechanism for the division of labour in social insects. The algorithm creates a correlation between age and task purely as a by-product of itsmodus operandi.     

Specialized avian Haemosporida trade reduced host breadth for increased prevalence

Parasite specialization on one or a few host species leads to a reduction in the total number of available host individuals, which may decrease transmission. However, specialists are thought to be able to compensate by increased prevalence in the host population and increased success in each individual host. Here, we use variation in host breadth among a community of avian Haemosporida to investigate consequences of generalist and specialist strategies on prevalence across hosts. We show that specialist parasites are more prevalent than generalist parasites in host populations that are shared between them. Moreover, the total number of infections of generalist and specialist parasites within the study area did not vary significantly with host breadth. This suggests that specialists can infect a similar number of host individuals as generalists, thus compensating for a reduction in host availability by achieving higher prevalence in a single host species. Specialist parasites also tended to infect older hosts, whereas infections by generalists were biased towards younger hosts. We suggest that this reflects different abilities of generalists and specialists to persist in hosts following infection. Higher abundance and increased persistence in hosts suggest that specialists are more effective parasites than generalists, supporting the existence of a trade‐off between host breadth and average host use among these parasites.     

Specificity of extrafloral nectar induction by herbivores differs among native and invasive populations of tallow tree

Background and Aims

Invasive plants can be released from specialist herbivores and encounter novel generalists in their introduced ranges, leading to variation in defence among native and invasive populations. However, few studies have examined how constitutive and induced indirect defences change during plant invasion, especially during the juvenile stage.

Methods

Constitutive extrafloral nectar (EFN) production of native and invasive populations of juvenile tallow tree (Triadica sebifera) were compared, and leaf clipping, and damage by a native specialist (Noctuid) and two native generalist caterpillars (Noctuid and Limacodid) were used to examine inducible EFN production.

Key results

Plants from introduced populations had more leaves producing constitutive EFN than did native populations, but the content of soluble solids of EFN did not differ. Herbivores induced EFN production more than simulated herbivory. The specialist (Noctuid) induced more EFN than either generalist for native populations. The content of soluble solids in EFN was higher (2·1 times), with the specialist vs. the generalists causing the stronger response for native populations, but the specialist response was always comparable with the generalist responses for invasive populations.

Conclusions

These results suggest that constitutive and induced indirect defences are retained in juvenile plants of invasive populations even during plant establishment, perhaps due to generalist herbivory in the introduced range. However, responses specific to a specialist herbivore may be reduced in the introduced range where specialists are absent. This decreased defence may benefit specialist insects that are introduced for classical biological control of invasive plants.