Life‐history syndromes: Integrating dispersal through space and time

Recent research has highlighted interdependencies between dispersal and other life‐history traits, i.e. dispersal syndromes, thereby revealing constraints on the evolution of dispersal and opportunities for improved ability to predict dispersal by considering suites of dispersal‐related traits. This review adds to the growing list of life‐history traits linked to spatial dispersal by emphasising the interdependence between dispersal through space and time, i.e. life‐history diversity that distributes individuals into separate reproductive events. We reviewed the literature that has simultaneously investigated spatial and temporal dispersal to examine the prediction that traits of these two dispersal strategies are negatively correlated. Our results suggest that negative covariation is widely anticipated from theory. Empirical studies often reported evidence of weak negative covariation, although more complicated patterns were also evident, including across levels of biological organisation. Existing literature has largely focused on plants with dormancy capability, one or two phases of the dispersal process (emigration and/or transfer) and a single level of biological organisation (theory: individual; empirical: species). We highlight patterns of covariation across levels of organisation and conclude with a discussion of the consequences of dispersal through space and time and future research areas that should improve our understanding of dispersal‐related life‐history syndromes.     

Effects of assay conditions in life history experiments with Drosophila melanogaster

Selection experiments with Drosophila have revealed constraints on the simultaneous evolution of life history traits. However, the responses to selection reported by different research groups have not been consistent. Two possible reasons for these inconsistencies are (i) that different groups used different environments for their experiments and (ii) that the selection environments were not identical to the assay environments in which the life history traits were measured. We tested for the effect of the assay environment in life history experiments by measuring a set of Drosophila selection lines in laboratories working on life history evolution with Drosophila in Basel, Groningen, Irvine and London. The lines measured came from selection experiments from each of these laboratories. In each assay environment, we measured fecundity, longevity, development time and body size. The results show that fecundity measurements were particularly sensitive to the assay environment. Differences between assay and selection environment in the same laboratory or differences between assay environments between laboratories could have contributed to the differences in the published results. The other traits measured were less sensitive to the assay environment. However, for all traits there were cases where the measurements in one laboratory suggested that selection had an effect on the trait, whereas in other laboratories no such conclusion would have been drawn. Moreover, we provide good evidence for local adaptation in early fecundity for lines from two laboratories.     

Long‐term consistency in spatial patterns of primate seed dispersal

Seed dispersal is a key ecological process in tropical forests, with effects on various levels ranging from plant reproductive success to the carbon storage potential of tropical rainforests. On a local and landscape scale, spatial patterns of seed dispersal create the template for the recruitment process and thus influence the population dynamics of plant species. The strength of this influence will depend on the long‐term consistency of spatial patterns of seed dispersal. We examined the long‐term consistency of spatial patterns of seed dispersal with spatially explicit data on seed dispersal by two neotropical primate species, Leontocebus nigrifrons and Saguinus mystax (Callitrichidae), collected during four independent studies between 1994 and 2013. Using distributions of dispersal probability over distances independent of plant species, cumulative dispersal distances, and kernel density estimates, we show that spatial patterns of seed dispersal are highly consistent over time. For a specific plant species, the legume Parkia panurensis, the convergence of cumulative distributions at a distance of 300 m, and the high probability of dispersal within 100 m from source trees coincide with the dimension of the spatial–genetic structure on the embryo/juvenile (300 m) and adult stage (100 m), respectively, of this plant species. Our results are the first demonstration of long‐term consistency of spatial patterns of seed dispersal created by tropical frugivores. Such consistency may translate into idiosyncratic patterns of regeneration.     

Fine scale relationships between sex, life history, and dispersal of masu salmon

Identifying the patterns and processes driving dispersal is critical for understanding population structure and dynamics. In many organisms, sex-biased dispersal is related to the type of mating system. Considerably, less is known about the influence of life-history variability on dispersal. Here we investigated patterns of dispersal in masu salmon (Oncorhynchus masou) to evaluate influences of sex and life history on dispersal. As expected, assignment tests and isolation by distance analysis revealed that dispersal of marine-migratory masu salmon was male-biased. However, dispersal of resident and migratory males did not follow our expectation and marine-migratory individuals dispersed more than residents. This may be because direct competition between marine-migratory and resident males is weak or that the cost of dispersal is smaller for marine-migratory individuals. This study revealed that both sex and migratory life-history influence patterns of dispersal at a local scale in masu salmon.     

Evolutionary tracking is determined by differential selection on demographic rates and density dependence

Recent ecological forecasts predict that ~25% of species worldwide will go extinct by 2050. However, these estimates are primarily based on environmental changes alone and fail to incorporate important biological mechanisms such as genetic adaptation via evolution. Thus, environmental change can affect population dynamics in ways that classical frameworks can neither describe nor predict. Furthermore, often due to a lack of data, forecasting models commonly describe changes in population demography by summarizing changes in fecundity and survival concurrently with the intrinsic growth rate (r). This has been shown to be an oversimplification as the environment may impose selective pressure on specific demographic rates (birth and death) rather than directly on r (the difference between the birth and death rates). This differential pressure may alter population response to density, in each demographic rate, further diluting the information combined to produce r. Thus, when we consider the potential for persistence via adaptive evolution, populations with the same r can have different abilities to persist amidst environmental change. Therefore, we cannot adequately forecast population response to climate change without accounting for demography and selection on density dependence. Using a continuous‐time Markov chain model to describe the stochastic dynamics of the logistic model of population growth and allow for trait evolution via mutations arising during birth events, we find persistence via evolutionary tracking more likely when environmental change alters birth rather than the death rate. Furthermore, species that evolve responses to changes in the strength of density dependence due to environmental change are less vulnerable to extinction than species that undergo selection independent of population density. By incorporating these key demographic considerations into our predictive models, we can better understand how species will respond to climate change.     

A meta‐analysis of dispersal in butterflies

Dispersal has recently gained much attention because of its crucial role in the conservation and evolution of species facing major environmental changes such as habitat loss and fragmentation, climate change, and their interactions. Butterflies have long been recognized as ideal model systems for the study of dispersal and a huge amount of data on their ability to disperse has been collected under various conditions. However, no single ‘best’ method seems to exist leading to the co‐occurrence of various approaches to study butterfly mobility, and therefore a high heterogeneity among data on dispersal across this group. Accordingly, we here reviewed the knowledge accumulated on dispersal and mobility in butterflies, to detect general patterns. This meta‐analysis specifically addressed two questions. Firstly, do the various methods provide a congruent picture of how dispersal ability is distributed across species? Secondly, is dispersal species‐specific? Five sources of data were analysed: multisite mark‐recapture experiments, genetic studies, experimental assessments, expert opinions, and transect surveys. We accounted for potential biases due to variation in genetic markers, sample sizes, spatial scales or the level of habitat fragmentation. We showed that the various dispersal estimates generally converged, and that the relative dispersal ability of species could reliably be predicted from their relative vagrancy (records of butterflies outside their normal habitat). Expert opinions gave much less reliable estimates of realized dispersal but instead reflected migration propensity of butterflies. Within‐species comparisons showed that genetic estimates were relatively invariable, while other dispersal estimates were highly variable. This latter point questions dispersal as a species‐specific, invariant trait.     

Plant DNA barcodes and the influence of gene flow

Success of species assignment using DNA barcodes has been shown to vary among plant lineages because of a wide range of different factors. In this study, we confirm the theoretical prediction that gene flow influences species assignment with simulations and a literature survey. We show that the genome experiencing the highest gene flow is, in the majority of the cases, the best suited for species delimitation. Our results clearly suggest that, for most angiosperm groups, plastid markers will not be the most appropriate for use as DNA barcodes. We therefore advocate shifting the focus from plastid to nuclear markers to achieve an overall higher success using DNA barcodes.     

How is dispersal integrated in life histories: a quantitative analysis using butterflies

As dispersal plays a key role in gene flow among populations, its evolutionary dynamics under environmental changes is particularly important. The inter-dependency of dispersal with other life history traits may constrain dispersal evolution, and lead to the indirect selection of other traits as a by-product of this inter-dependency. Identifying the dispersal's relationships to other life-history traits will help to better understand the evolutionary dynamics of dispersal, and the consequences for species persistence and ecosystem functioning under global changes. Dispersal may be linked to other life-history traits as their respective evolutionary dynamics may be inter-dependent, or, because they are mechanistically related to each other. We identify traits that are predicted to co-vary with dispersal, and investigated the correlations that may constrain dispersal using published information on butterflies. Our quantitative analysis revealed that (1) dispersal directly correlated with demographic traits, mostly fecundity, whereas phylogenetic relationships among species had a negligible influence on this pattern, (2) gene flow and individual movements are correlated with ecological specialisation and body size, respectively and (3) routine movements only affected short-distance dispersal. Together, these results provide important insights into evolutionary dynamics under global environmental changes, and are directly applicable to biodiversity conservation.     

Recent evolutionary history predicts population but not ecosystem‐level patterns

In the face of rapid anthropogenic environmental change, it is increasingly important to understand how ecological and evolutionary interactions affect the persistence of natural populations. Augmented gene flow has emerged as a potentially effective management strategy to counteract negative consequences of genetic drift and inbreeding depression in small and isolated populations. However, questions remain about the long‐term impacts of augmented gene flow and whether changes in individual and population fitness are reflected in ecosystem structure, potentiating eco‐evolutionary feedbacks. In this study, we used Trinidadian guppies (Poecilia reticulata) in experimental outdoor mesocosms to assess how populations with different recent evolutionary histories responded to a scenario of severe population size reduction followed by expansion in a high‐quality environment. We also investigated how variation in evolutionary history of the focal species affected ecosystem dynamics. We found that evolutionary history (i.e., gene flow vs. no gene flow) consistently predicted variation in individual growth. In addition, gene flow led to faster population growth in populations from one of the two drainages, but did not have measurable impacts on the ecosystem variables we measured: zooplankton density, algal growth, and decomposition rates. Our results suggest that benefits of gene flow may be long‐term and environment‐dependent. Although small in replication and duration, our study highlights the importance of eco‐evolutionary interactions in determining population persistence and sets the stage for future work in this area.     

Joint estimation of contemporary seed and pollen dispersal rates among plant populations

There are few statistical methods for estimating contemporary dispersal among plant populations. A maximum-likelihood procedure is introduced here that uses pre- and post-dispersal population samples of biparentally inherited genetic markers to jointly estimate contemporary seed and pollen immigration rates from a set of discrete external sources into a target population. Monte Carlo simulations indicate that accurate estimates and reliable confidence intervals can be obtained using this method for both pollen and seed migration rates at modest sample sizes (100 parents/population and 100 offspring) when population differentiation is moderate (F(ST) ≥ 0.1), or by increasing pre-dispersal samples (to about 500 parents/population) when genetic divergence is weak (F(ST) = 0.01). The method exhibited low sensitivity to the number of source populations and achieved good accuracy at affordable genetic resolution (10 loci with 10 equifrequent alleles each). Unsampled source populations introduced positive biases in migration rate estimates from sampled sources, although they were minor when the proportion of immigration from the latter was comparatively low. A practical application of the method to a metapopulation of the Australian resprouter shrub Banksia attenuata revealed comparable levels of directional seed and pollen migration among dune groups, and the estimate of seed dispersal was higher than a previous estimate based on conservative assignment tests. The method should be of interest to researchers and managers assessing broad-scale nonequilibrium seed and pollen gene flow dynamics in plants.     

The interaction of multiple environmental stressors affects adaptation to a novel habitat in the natterjack toad Bufo calamita

The potential to adapt to novel environmental conditions is a key area of interest for evolutionary biology. However, the role of multiple selection pressures on adaptive responses has rarely been investigated in natural populations. In Sweden, the natterjack toad Bufo calamita inhabits two separate distribution areas, one in southernmost Sweden and one on the west coast. We characterized the larval habitat in terms of pond size and salinity in the two areas, and found that the western populations are more affected by both desiccation risk and pond salinity than the southern populations. In a common garden experiment manipulating salinity and temperature, we found that toads from the west coast populations were locally adapted to shorter pond duration as indicated by their higher development and growth rates. However, despite being subjected to higher salinity stress in nature, west coast toads had a poorer performance in saline treatments. We found that survival in the saline treatments in the west coast populations was positively affected by larger body mass and longer larval period. Furthermore, we found negative genetic correlations between body mass and growth rate and their plastic responses to salinity. These results implicate that the occurrence of multiple environmental stressors needs to be accounted for when assessing the adaptive potential of organisms and suggest that genetic correlations may play a role in constraining adaptation of natural populations.     

Drought survival strategies,dispersal potential and persistence of invertebrate species in an intermittent stream landscape

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Performance of individual vs. group sampling for inferring dispersal under isolation‐by‐distance

Models of isolation‐by‐distance formalize the effects of genetic drift and gene flow in a spatial context where gene dispersal is spatially limited. These models have been used to show that, at an appropriate spatial scale, dispersal parameters can be inferred from the regression of genetic differentiation against geographic distance between sampling locations. This approach is compelling because it is relatively simple and robust and has rather low sampling requirements. In continuous populations, dispersal can be inferred from isolation‐by‐distance patterns using either individuals or groups as sampling units. Intrigued by empirical findings where individual samples seemed to provide more power, we used simulations to compare the performances of the two methods in a range of situations with different dispersal distributions. We found that sampling individuals provide more power in a range of dispersal conditions that is narrow but fits many realistic situations. These situations were characterized not only by the general steepness of isolation‐by‐distance but also by the intrinsic shape of the dispersal kernel. The performances of the two approaches are otherwise similar, suggesting that the choice of a sampling unit is globally less important than other settings such as a study's spatial scale.     

Evaluating the life‐history trade‐off between dispersal capability and reproduction in wing dimorphic insects: a meta‐analysis

A life‐history trade‐off exists between flight capability and reproduction in many wing dimorphic insects: a long‐winged morph is flight‐capable at the expense of reproduction, while a short‐winged morph cannot fly, is less mobile, but has greater reproductive output. Using meta‐analyses, I investigated specific questions regarding this trade‐off. The trade‐off in females was expressed primarily as a later onset of egg production and lower fecundity in long‐winged females relative to short‐winged females. Although considerably less work has been done with males, the trade‐off exists for males among traits primarily related to mate acquisition. The trade‐off can potentially be mitigated in males, as long‐winged individuals possess an advantage in traits that can offset the costs of flight capability such as a shorter development time. The strength and direction of trends differed significantly among insect orders, and there was a relationship between the strength and direction of trends with the relative flight capabilities between the morphs. I discuss how the trade‐off might be both under‐ and overestimated in the literature, especially in light of work that has examined two relevant aspects of wing dimorphic species: (1) the effect of flight‐muscle histolysis on reproductive investment; and (2) the performance of actual flight by flight‐capable individuals.     

The evolution of dispersal polymorphisms in insects: The influence of habitats,host plants and mates

Wing-dimorphic, delphacid planthoppers were used to test hypotheses concerning the effects of habitat persistence and architectural complexity on the occurrence of dispersal. For reasons concerning both the durational stability of the habitat and the reduced availability of mates, selection has favored high levels of dispersal in species occupying temporary habitats. Flightlessness predominates in species occupying persistent habitats, and is promoted by a phenotypic trade-off between reproductive success and flight capability. Wings are retained in tree-inhabiting species, probably for reasons concerning the more effective negotiation of three-dimensional habitats. In contrast, flightlessness is characteristic of those species inhabiting low profile host plants. For several delphacid genera, migratory species are larger than their sedentary congeners. Because body size and fecundity are positively related in planthoppers, the large body size observed in migratory taxa may result from selection for increased fecundity in colonizing species.     

Fragmentation and comparative genetic structure of four mediterranean woody species: complex interactions between life history traits and the landscape context

Aim The effect of habitat fragmentation on population genetic structure results from the interaction between species’ life history traits and the particular landscape context, and both components are inherently difficult to tease apart. Here, we compare the genetic (allozyme) structure of four co‐occurring woody species with contrasting life histories to explore how well their response to the same fragmentation process can be predicted from their functional traits. Location A highly fragmented forest landscape located in the lower Guadalquivir catchment, south‐western Spain. Methods We sampled four species (Cistus salviifolius, Myrtus communis, Pistacia lentiscus and Quercus coccifera) from the same 23 forest fragments known to form a representative array of habitat characteristics in the region. We assessed genetic diversity (A, H_e and N_g) and differentiation (F_IS and F_ST) for each species and explored their potential drivers using a model‐selection approach with four fragment features (size, historical and current connectivity, and stability) as predictor variables. Results Regional‐scale genetic diversity increased from the shortest‐lived to the longest‐lived species, while population differentiation of the self‐compatible species was roughly double that of the three self‐incompatible species. Fragment size was the only feature that did not consistently affect the genetic diversity of local populations across all species. Three species showed signs of being affected by fragmentation, yet each responded differently to the set of fragment features considered. We observed several trends that were at odds with simple life history‐based predictions but could arise from patterns of gene flow and/or local‐scale demographic processes. Main conclusions Our comparative study of various landscape features and species underscores that the same fragmentation process can have very different, and complex, consequences for the population genetic structure of plants. This idiosyncrasy renders generalizations across natural systems very difficult and highlights the need of context‐oriented guidelines for an efficient conservation management of species‐rich landscapes.     

Male sand crickets trade-off flight capability for reproductive potential

In this paper, we test the hypothesis that male sand crickets, Gryllus firmus, experience a trade-off between flight capability and reproductive potential expressed as reduced testis weight in flight-capable morphs. We used a half-sib design with 130 sires, three dams per sire and an average of 5.66 males per dam family, for a total of 2206 F1 offspring. Traits measured were head width, somatic dry weight, testis weight, wing morph (micropterous/macropterous), weight of the dorso-longitudinal flight muscles (DLM) and the functional status of these muscles. Heritabilities of all traits were significant and ranged from 0.14 to 0.43. All traits were positively correlated with body size, but removal of this covariance revealed a highly significant trade-off, both phenotypically and genetically, between testes size and flight capability as measured by wing morph, DLM size or DLM status. The possible implications of this for morph-specific reproductive tactics are discussed.     

The impact of parasite dispersal on antagonistic host-parasite coevolution

Coevolving populations of hosts and parasites are often subdivided into a set of patches connected by dispersal. Higher relative rates of parasite compared with host dispersal are expected to lead to parasite local adaptation. However, we know of no studies that have considered the implications of higher relative rates of parasite dispersal for other aspects of the coevolutionary process, such as the rate of coevolution and extent of evolutionary escalation of resistance and infectivity traits. We investigated the effect of phage dispersal on coevolution in experimental metapopulations of the bacterium Pseudomonas fluorescens SBW25 and its viral parasite, phage SBW25Phi2. Both the rate of coevolution and the breadth of evolved infectivity and resistance ranges peaked at intermediate rates of parasite dispersal. These results suggest that parasite dispersal can enhance the evolutionary potential of parasites through provision of novel genetic variation, but that high rates of parasite dispersal can impede the evolution of parasites by homogenizing genetic variation between patches, thereby constraining coevolution.