Are parental care trade‐offs in shorebirds driven by parental investment or sexual selection?

Sexual selection, mating systems and parental behaviour are closely linked, although the exact nature of their relationship is controversial. The parental investment hypothesis (PIH) states that parental care disparity drives sexual selection intensity, because the sex providing less care competes for the sex that provides more. In contrast, the sexual selection hypothesis (SSH) asserts that more intense sexual selection on males leads to reduced male parental investment. We tested these hypotheses using directional phylogenetic comparative methods in shorebirds, which have an unusually diverse array of breeding systems. Changes in parental care and sexual selection intensity were tightly correlated, and we carried out three sets of analyses focusing on changes in male behaviour, female behaviour and in either sex. The results from the analyses were consistent with both PIH and SSH, although the patterns in male transition were sensitive to model values. We propose two explanations for these results. First, phylogenetic transitions may be idiosyncratic so that they depend on the ecological circumstances of individual species. Second, transitions in social traits, such as breeding systems, may be rapid and take place in ecological time, so directional phylogenetic methods that work through longer time scales may not infer accurately the timing and direction of all changes.     

The evolution of trade‐offs: where are we?

Trade-offs are a core component of many evolutionary models, particularly those dealing with the evolution of life histories. In the present paper, we identify four topics of key importance for studies of the evolutionary biology of trade-offs. First, we consider the underlying concept of 'constraint'. We conclude that this term is typically used too vaguely and suggest that 'constraint' in the sense of a bias should be clearly distinguished from 'constraint' in the sense of proscribed combinations of traits or evolutionary trajectories. Secondly, we address the utility of the acquisition-allocation model (the 'Y-model'). We find that, whereas this model and its derivatives have provided new insights, a misunderstanding of the pivotal equation has led to incorrect predictions and faulty tests. Thirdly, we ask how trade-offs are expected to evolve under directional selection. A quantitative genetic model predicts that, under weak or short-term selection, the intercept will change but the slope will remain constant. Two empirical tests support this prediction but these are based on comparisons of geographic populations: more direct tests will come from artificial selection experiments. Finally, we discuss what maintains variation in trade-offs noting that at present little attention has been given to this question. We distinguish between phenotypic and genetic variation and suggest that the latter is most in need of explanation. We suggest that four factors deserving investigation are mutation-selection balance, antagonistic pleiotropy, correlational selection and spatio-temporal variation, but as in the other areas of research on trade-offs, empirical generalizations are impeded by lack of data. Although this lack is discouraging, we suggest that it provides a rich ground for further study and the integration of many disciplines, including the emerging field of genomics.     

Germline stem cell maintenance as a proximate mechanism of life‐history trade‐offs?

We suggest that the commonly observed trade-offs between early- and late-life reproduction may be mediated by genetic variation in germline stem cell maintenance. Stem cell biology provides a natural framework and experimental methods for understanding the mechanistic basis of life-history evolution. At the same time, natural variation in life-history strategies can serve as a powerful tool for identifying the genes and molecular pathways involved in the maintenance of stem cells in aging adults. We illustrate the connections between life-history and stem cells with examples drawn primarily from Drosophila melanogaster and Caenorhabditis elegans, and suggest a number of testable hypotheses and avenues for future investigation that can be addressed with existing models and tools.     

Is local adaptation in Mimulus guttatus caused by trade‐offs at individual loci?

Local adaptation is considered to be the result of fitness trade‐offs for particular phenotypes across different habitats. However, it is unclear whether such phenotypic trade‐offs exist at the level of individual genetic loci. Local adaptation could arise from trade‐offs of alternative alleles at individual loci or by complementary sets of loci with different fitness effects of alleles in one habitat but selective neutrality in the alternative habitat. To evaluate the genome‐wide basis of local adaptation, we performed a field‐based quantitative trait locus (QTL) mapping experiment on recombinant inbred lines (RILs) created from coastal perennial and inland annual races of the yellow monkeyflower (Mimulus guttatus) grown reciprocally in native parental habitats. Overall, we detected 19 QTLs affecting one or more of 16 traits measured in two environments, most of small effect. We identified 15 additional QTL effects at two previously identified candidate QTLs [DIV ERGENCE (DIV)]. Significant QTL by environment interactions were detected at the DIV loci, which was largely attributable to genotypic differences at a single field site. We found no detectable evidence for trade‐offs for any one component of fitness, although DIV2 showed a trade‐off involving different fitness traits between sites, suggesting that local adaptation is largely controlled by non‐overlapping loci. This is surprising for an outcrosser, implying that reduced gene flow prevents the evolution of individuals adapted to multiple environments. We also determined that native genotypes were not uniformly adaptive, possibly reflecting fixed mutational load in one of the populations.     

When do trade‐offs occur? The roles of energy constraints and trait flexibility in bushcricket populations

In many animal species, the expression of sexually selected traits is negatively correlated with traits associated with survival such as immune function, a relationship termed a ‘trade‐off’. But an alternative in which sexually selected traits are positively correlated with survival traits is also widespread. We propose that the nature of intertrait relationships is largely determined by overall energy expenditure, energy availability and trait flexibility, with trade‐offs expected when individuals are subject to energy constraints. We tested this hypothesis in Ephippiger diurnus, a European bushcricket in which males are distinguished by two prominent sexually selected traits, acoustic calls and a large spermatophore transferred to the female at mating, and where immune function may be critical in survival. Ephippiger diurnus are distributed as small, isolated populations that are differentiated genetically and behaviourally. We analysed songs, spermatophores and the immune function in male individuals from eight populations spanning a range of song types. As predicted, we only found trade‐offs in those populations that expended more energy on song and were less flexible in their ability to adjust that expenditure. Ultimately, energy constraints and resulting trade‐offs may limit the evolution of song exaggeration in E. diurnus populations broadcasting long calls comprised of multiple ‘syllables’.     

Evolutionary trade‐offs in locomotor capacities in lacertid lizards: are splendid sprinters clumsy climbers?

We tested the hypothesis that an evolutionary trade‐off exists between the capacity to run on level terrain and the ability to climb inclined structures in lacertid lizards. Biomechanical and physiological models of lizard locomotor performance suggest that the morphological design requirements of a ground‐dwelling vs. scansorial life style are difficult to reconcile. This conflict is thought to preclude simultaneous evolution of maximal locomotor performance on level and inclined terrain. This notion has been corroborated by comparative studies on lizard species from other groups (Anolis, Chamaeleo, Sceloporus), but is not supported by our data on 13 species from the family Lacertidae. We found no indication of a negative association between maximal sprint speed of lizards over a level racetrack (indicative of ground‐dwelling locomotor performance), on an inclined stony surface (indicative of climbing performance over rock faces) and inclined mesh surface (indicative of clambering performance among vegetation). Moreover, morphological characteristics associated with fast sprinting capacities (e.g. long hind limbs) apparently enhance, rather than hinder climbing and clambering performance. We conclude that in our sample of lacertid lizards, the evolution of fast sprinting capacity on level terrain has not inflicted major restrictions on climbing and clambering performance.     

Climatic control of dispersal–ecological specialization trade‐offs: a metacommunity process at the heart of the latitudinal diversity gradient?

We outline the potentially important role of dispersal in linking diversity patterns at different spatial and temporal scales, and the resulting potential to link hypotheses explaining macroscale patterns of diversity. We do this by proposing a possible mechanism linking climate to diversity patterns: we argue that climate, via effects of continuity of habitat availability in space and time, mediates a dispersal–ecological specialization trade‐off at the metacommunity level that leads to latitudinal trends in dispersal ability, ecological specialization, range sizes, speciation and species richness, ultimately driving the latitudinal diversity gradient. This trade‐off constitutes a possible mechanism for the strong macroscale correlation between climate and species richness that is consistent with recent ideas about niche conservatism and gradient lengths, as well as other leading hypotheses. We present an overview of predictions derived from our ideas. Of these, some have already been tested and supported and others are still open to debate or need testing. Together they provide a unique set of predictions that allows falsification.     

Do trade‐offs between predation pressures on females versus nests drive nest‐site choice in painted turtles?

Predation strongly influences reproductive behaviours because reproducing individuals must balance mortality risks to themselves and to their offspring. In many freshwater turtles, the nest predation risk decreases with nest distance from water, whereas the predation risk to females increases farther from water. To determine whether predation pressure influences the distance from water at which female turtles nest, we measured predation pressure on nesting females and on nests, as well as the distances of nests to water, in two populations of painted turtles. Using models, we found that female survival in both populations was high and did not vary with distance from water. Nest survival was also uncorrelated with nest distance to water, although it was significantly lower than adult survival in both populations and was only 1.2% in one population. Our results suggest that nest sites are not predictably safe from predators. Instead, turtles may hedge their bets by nesting over a wide range of distances from water because any distance is risky for nests and no distance is particularly risky for the nesting female. We suggest that other factors, such as suitable incubation conditions and/or post‐emergence hatchling survival, probably play a larger role than predation in driving nest‐site choice in painted turtles.     

Trade‐offs in evolutionary immunology: just what is the cost of immunity?

It has become increasingly clear that life-history patterns among the vertebrates have been shaped by the plethora and variety of immunological risks associated with parasitic faunas in their environments. Immunological competence could very well be the most important determinant of life-time reproductive success and fitness for many species. It is generally assumed by evolutionary ecologists that providing immunological defences to minimise such risks to the host is costly in terms of necessitating trade-offs with other nutrient-demanding processes such as growth, reproduction, and thermoregulation. Studies devoted to providing assessments of such costs and how they may force evolutionary trade-offs among life-history characters are few, especially for wild vertebrate species, and their results are widely scattered throughout the literature. In this paper we attempt to review this literature to obtain a better understanding of energetic and nutritional costs for maintaining a normal immune system and examine how costly it might be for a host who is forced to up-regulate its immunological defence mechanisms. The significance of these various costs to ecology and life history trade-offs among the vertebrates is explored. It is concluded that sufficient evidence exists to support the primary assumption that immunological defences are costly to the vertebrate host.     

Optimality modeling and fitness trade‐offs: when should plants become pollinator specialists?

The assumption that flowers readily evolve specializations for pollination by particular animals has been central to a standard view of pollinator-mediated adaptive divergence in angiosperms. Stebbins' Most Effective Pollinator Principle (MEPP) formalized this assumption in proposing that a plant should always evolve specializations to its most effective pollinator. I argue that the MEPP and its corollaries are unsupported by basic models of phenotypic selection which predict that a plant should evolve greater specialization to a particular pollinator when the marginal fitness gain exceeds the marginal fitness loss from becoming less adapted to all other pollinators. Differences in pollinator effectiveness are neither necessary nor sufficient to predict specialization. Differences in effectiveness certainly can foster floral specialization to the most effective pollinator in some cases, but when adaptation to a relatively ineffective pollinator requires little loss in the fitness contribution of a more effective pollinator, plants may exhibit striking specializations for the less effective pollinator. Recognizing that the effectiveness of pollinators is not tightly coupled to their importance in selecting for phenotypic novelty may resolve the mismatch between floral features that appear to represent clear evolutionary responses to specific pollinators and patterns of flower visitation that often seem generalized. To shed light on agents of selection and the adaptive value of floral traits I argue that we must go beyond measures of pollinator effectiveness to investigate pollinator-mediated fitness trade-offs over a range of floral phenotypes.     

Selection on defensive traits in a sterile caste – caste evolution: a mechanism to overcome life‐history trade‐offs?

SUMMARY During development and evolution individuals generally face a trade-off between the development of weapons and gonads. In termites, characterized by reproductive division of labor, a caste evolved—the soldiers—which is completely sterile and which might be released from developmental trade-offs between weapons and testes. These soldiers are exclusively dedicated to defense. First, we investigated whether defensive traits are under selection in sterile termite soldiers using allometric analyses. In soldiers of the genus Cryptotermes phragmotic traits such as a sculptured and foreshortened head evolve rapidly but were also lost twice. Second, we compared the scaling relationships of these weapons with those in solitary insects facing a trade-off between weapons and gonads. Defensive traits consistently had lower slopes than nondefensive traits which supports the existence of stabilizing selection on soldier phragmotic traits in order to plug galleries. Moreover, soldier head widths were colony specific and correlated with the minimum gallery diameter of a colony. This can proximately be explained by soldiers developing from different instars. The scaling relationships of these termite soldiers contrast strikingly with those of weapons of solitary insects, which are generally exaggerated (i.e., overscaling) male traits. These differences may provide important insights into trait evolution. Trade-offs constraining the development of individuals may have been uncoupled in termites by evolving different castes, each specialized for one function. When individuals in social insect are "released" from developmental constraints through the evolution of castes, this certainly contributed to the ecological and evolutionary success of social insects.     

Comparing fecundity in parthenogenetic versus sexual populations of the freshwater snail Campeloma limum: is there a two‐fold cost of sex?

Abstract. The predominance of sexuality in eukaryotes remains an evolutionary paradox, given the "two-fold cost of sex" also known as the "cost of males." [Correction added after online publication 29 January 2009: in the preceding sentence, extraneous words were deleted.] As it requires two sexual parents to reproduce and only one parthenogenetic parent, parthenogens should have twice the reproductive rate compared with their sexual counterparts and their genes should spread twice as fast, if all else is equal. Yet, parthenogenesis is relatively rare and considered an evolutionary dead-end, while sexuality is the dominant form of reproduction in multicellular eukaryotes. Many studies have explored short-term benefits of sex that could outweigh its two-fold cost, but few have compared fecundity between closely related sexuals and parthenogens to first verify that "all else is equal" reproductively. We compared six fecundity measures between sexual and parthenogenetic populations of the freshwater snail, Campeloma limum , during a brooding cycle (1 year) across two drainages. Drainages were analyzed separately because of a significant drainage effect. In the Savannah drainage, fecundity was not significantly different between sexuals and parthenogens, even though parthenogens had significantly more empty egg capsules per brood. In the Ogeechee drainage, parthenogens had significantly more egg capsules with multiple embryos and more hatched embryos than sexuals. Taken over 1 year, embryo size was not significantly different between parthenogens and sexuals in either drainage. Given these results and the close proximity of sexual and parthenogenetic populations, it is perplexing why parthenogenetic populations have not completely replaced sexual populations in C. limum.     

Diet variation of a generalist fish predator,grey snapper Lutjanus griseus,across an estuarine gradient: trade‐offs of quantity for quality?

This study examined diet, prey quality and growth for a generalist fish predator, grey snapper Lutjanus griseus, at five sites across an estuarine gradient in the Loxahatchee River estuary, Florida, U.S.A. Lutjanus griseus diets shifted from dominance by low quality, intertidal crabs upstream to an increased reliance on higher quality shrimp, fishes and benthic crabs downstream. Frequency of L. griseus with empty stomachs was higher at downstream sites. Lutjanus griseus growth rates did not vary among sites. Results indicate that L. griseus may be able to compensate for lower quality prey upstream by consuming more, and thus individuals are able to maintain similar levels of energy balance and growth rates across the estuarine gradient. Elucidating mechanisms, such as compensatory feeding, that enable generalist species to remain successful across habitat conditions are critical to understanding their organismal ecology and may facilitate predictions about the response of generalists to landscape alteration.     

Morphology dependent foraging efficiency in perch: a trade‐off for ecological specialization?

Trade-offs in foraging efficiency leading to divergent natural selection between and within populations exploiting different resources are thought to be a primary cause of trophic polymorphism. In this study we focused on the trade-offs in foraging efficiency and growth in a polymorphic perch population. Specifically, we related habitat-specific growth and diet of perch to perch morphology. In a subsequent laboratory study we experimentally tested the trade-off by testing the efficiency of perch with different morphology feeding on pelagic ( Daphnia sp., Chaoborus sp.) and littoral (mayfly larvae) food resources. The feeding performance was tested in different physical environments to see if we could predict growth patterns in the field based on foraging rate and behavior of perch.
In the field study, we found that the perch from the littoral and the pelagic zones differed in both morphology and diet. Within the littoral zone the deeper-bodied individuals grew faster compared to the more streamlined individuals, whereas the opposite pattern was found in the pelagic zone. In the aquarium experiments, perch from the littoral zone had higher capture rates on the pelagic prey types in vegetation trials and on mayfly larvae in both open water and vegetation trials. The pelagic perch had higher capture rates on the pelagic prey types in open water trials. The littoral perch had lower search velocity than the pelagic perch in open water trials whereas the opposite pattern was found in vegetation trials. The attack velocity of the pelagic perch was also higher than that of the littoral perch independent of vegetation structure. Our results suggest that there is a functional trade-off between performance in alternate habitats and general body form in perch. Such trade-offs may promote divergent natural selection and could be the mechanism that give rise to and upholds the pattern in the field.     

A cry for help or sexual perfumes? An alternative hypothesis for wasp attraction to the scent of caterpillar‐wounded plants

This article comments on: Combined use of herbivore‐induced plant volatiles and sex pheromones for mate location in braconid parasitoids     

The hemolymph proteome of the honeybee: Gel‐based or gel‐free?

The honeybee has an invaluable economic impact and is a model for studying immunity, development and social behavior. The recent sequencing and annotation of the honeybee genome facilitates the study of its hemolymph, which reflects the physiological condition and mediates immune responses. We aimed at making a proteomic reference map of honeybee hemolymph and compared gel‐free and gel‐based techniques. One hundered and four 2‐DE spots corresponding to 62 different proteins were identified. Eight identical 2‐DLC experiments resulted in the identification of 32 unique proteins. One repeat was clearly not representative for the potential of the given 2‐DLC setup. Only 27% of the identified hemolymph proteins were found by both techniques. In addition, we found proteins of three different viruses which creates possibilities for biomarker design. Future hemolymph studies will benefit from this work.     

A meta‐analysis of isolation by distance: relic or reference standard for landscape genetics?

Isolation by distance (IBD) has been a common measure of genetic structure among populations and is based on Euclidean distances among populations. Whereas IBD does not incorporate geographic complexity (e.g. dispersal barriers, corridors) that may better predict genetic structure, a new approach (landscape genetics) joins landscape ecology with population genetics to better model genetic structure. Should IBD be set aside or should it persist as the most simple model in landscape genetics? We evaluated the status of IBD by collecting and analyzing results of 240 IBD data sets among diverse taxa and study systems. IBD typically represented a low proportion of variance in genetic structure (mean r²=0.22) in part because many studies included relatively few populations (mean=11). The number of populations studied (N) was asymptotically related to IBD significance; a study with 9 populations has only 50% probability of significance, while one with >23 populations will have 90% probability of significance. Surprisingly, ectothermic animals were significantly (p=0.0018) more likely to have significant IBD than endotherms, which suggests a metabolic basis underlying gene flow rates. We also observed marginally significant effects on IBD significance for a) taxa in general and b) dispersal modes within actively‐dispersing endotherms. Other factors analyzed (genetic markers, genetic distances, habitats, active or passive dispersal, plant growth form) did not significantly affect IBD, likely related to typical N. For multiple reasons we conclude that IBD should continue as the simplest reference standard against which all other, more complex models should be compared in landscape genetics research.     

Trade‐offs in oviposition choice? Food‐dependent performance and defence against predators of a herbivorous sawfly

The sawfly Athalia rosae L. (Hymenoptera: Tenthredinidae) is a feeding specialist on plant species of the Brassicaceae, which are characterised by secondary metabolites, called glucosinolates. The larvae can take up the respective glucosinolates of their hosts and concentrate them in their haemolymph to protect themselves against predators. Oviposition preferences of naïve females were tested for three species, Sinapis alba L., Brassica nigra (L.) Koch, and Barbarea stricta Andrz., and were related to larval performance patterns. Larvae were reared on either one of these plants and it was investigated how host‐plant quality influences both the developmental times and growth of larvae (bottom‐up) and the defence efficiency against predators (top‐down). Innately, almost all adult females avoided B. stricta for oviposition and clearly preferred B. nigra over S. alba. On average, larvae developed best on B. nigra. Female larvae reached similar final body masses on all host‐plant species, but males reared on S. alba were slightly lighter. The developmental time of larvae reared on B. stricta was significantly longer than on the other two plants. However, larvae reared on B. stricta were best protected against the predatory wasp Polistes dominulus Christ (Hymenoptera: Vespidae). The wasps rejected these larvae most often, while they attacked larvae reared on S. alba most frequently. Thus, larvae feeding on B. stricta theoretically run a higher risk of predation due to a prolonged developmental time, but in practice they are better protected against predators. Overall, oviposition preferences of A. rosae seem to be more influenced by bottom‐up effects on larval performance than by top‐down effects.     

Does the niche breadth or trade‐off hypothesis explain the abundance–occupancy relationship in avian Haemosporidia?

Two hypotheses have been proposed to explain the abundance–occupancy relationship (AOR) in parasites. The niche breadth hypothesis suggests that host generalists are more abundant and efficient at colonizing different host communities than specialists. The trade‐off hypothesis argues that host specialists achieve high density across their hosts' ranges, whereas generalists incur the high cost of adaptation to diverse immuno‐defence systems. We tested these hypotheses using 386 haemosporidian cytochrome‐b lineages (1894 sequences) recovered from 2318 birds of 103 species sampled in NW Africa, NW Iberia, W Greater Caucasus and Transcaucasia. The number of regions occupied by lineages was associated with their frequency suggesting the presence of AOR in avian Haemosporidia. However, neither hypothesis provided a better explanation for the AOR. Although the host generalist Plasmodium SGS1 was over three times more abundant than other widespread lineages, both host specialists and generalists were successful in colonizing all study regions and achieved high overall prevalence.