Keynote papers on sandhopper orientation and navigation

This article analyses the relevant studies that have made sandhoppers a model subject for the study of orientation, and traces the development of the paradigm through innovative hypotheses and empirical evidence. Sandhoppers are able to maintain their direction without sensorial contact with the goal, which is their burrowing zone extended along the beach, but very narrow across it. They actively determine the direction of their movements, according to their internal state and the environmental features encountered. Each population shows an 'innate directional tendency' adapted to the shoreline of origin, and the inexpert laboratory-born young behave in a similar way to the adults. Genetic differences have been demonstrated between, as well as within natural populations. The question of the calibration of the sun compass to orientation on a particular shoreline implies a redundancy of mechanisms of orientation. Orientation mechanisms may involve environmental cues perceived through diverse sensory modalities, and range from simple orientation reflexes to sun compass navigational systems. These include scototaxis and geotaxis, and the response to the silhouette of the dune, in addition to sun and moon orientation, which is dependent on the time of the day and orientates daily migrations on the beach. Different modalities of orientation may operate singly, or in conjunction with each other, and their ecological significance may vary according to the habitat and lifestyle of the animals. Taken collectively, the orientation behaviour of the group appears to be a most accommodating phenotype, with considerable adaptive potential. The evidence from comparative studies of different populations promotes consideration of behavioural plasticity as an adaptation to changing coastlines.     

Inheritance of solar direction finding in sandhoppers

Summary The capacity ofTalitrus saltator populations to adapt to variations in shoreline directions within a limited space was evaluated by testing both adults collected at different points along continuous sandy arcs, and the 1st and 2nd generations of their laboratory-born offspring (exposed to the sun for the first time during testing). Solar orientation of the adults was adapted to the direction of the shoreline at the capture point, and significant statistical differences appeared between lots from different points. The innate directional tendency of the laboratory-born populations differed between collecting points only a few km apart. Solar direction-finding is thus genetically determined, and these results presuppose a genetic heterogeneity within the natural populations. Individually acquired components could improve orientation in nature.Abbreviations TED theorical escape direction - IED innate escape direction     

Orientation of the sandhopperTalitrus saltator (Amphipoda,Talitridae) living on dynamic sandy shores

Summary The littoral sandhopperTalitrus saltator Montagu maintains its position along the beach mainly by means of an innate solar orientation. Different populations show different directional tendencies depending on the direction of the sealand axis. Experiments were designed which aimed to disentangle the innate and acquired components of the escape orientation. Therefore, the solar orientation of experienced adults living on shores subject to fluctuations of the shoreline and of their laboratory-born (inexperienced) offspring were compared. The innate sun compass orientation shown by the young is modified by learning during life under natural conditions, depending on the variability of the shore. Results showed: (1) an improvement in the solar orientation in individuals living on relatively constant shores; (2) a loss of precision in individuals living on highly dynamic shores; (3) a change to a new ecologically efficient escape direction in individuals living on a relatively stable lagoon shore.Abbreviation TED theoretical escape direction     

Experimental Change of the Orientation of Two Populations of Talitrus saltator (Crustacea Amphipoda Talitridae) from Cap Bon (North‐Eastern Tunisia)

The orientation of sandhopper populations is adapted to the direction of the shoreline of the sandy beaches where they live; this behaviour was shown to be inherited in some Mediterranean populations. The question was open whether this behaviour could be adaptively modified in case of changing shoreline or passive transfer to a new differently oriented shoreline. The Cap Bon beaches in north‐eastern Tunisia are particularly interesting because they belong to two different Mediterranean Basins, the central and the eastern one, and their supra‐tidal populations do not come together. This work verified the effect of experimental change of the shoreline direction in two populations of Talitrus saltator from Cap Bon (north‐eastern Tunisia) through a displacement experiment. We transferred samples of T. saltator from two different localities (Korba and Ratiba) from their original beach to the familiar one and tested their solar and landscape orientation on the new beach that had an almost opposite direction with respect to the previous one. The comparisons of the results on the home beach and the new one confirmed the use of the solar compass in both populations, as well as the importance of landscape view and optical local sky factor in adjusting the escape direction. In both populations, an increase of scatter was observed on the new beach, especially when individuals could see the landscape. Also, a clear behavioural difference between the two populations was recorded, being Ratiba population not significantly oriented to the shoreline when tested on the unfamiliar beach, while Korba population maintained its home direction also on the new beach.     

Constitutive and Operational Variation of Learning in Foraging Predatory Mites

Learning is widely documented across animal taxa but studies stringently scrutinizing the causes of constitutive or operational variation of learning among populations and individuals are scarce. The ability to learn is genetically determined and subject to constitutive variation while the performance in learning depends on the immediate circumstances and is subject to operational variation. We assessed variation in learning ability and performance of plant-inhabiting predatory mites, Amblyseius swirskii, caused by population origin, rearing diet, and type of experience. Using an early learning foraging paradigm, we determined that homogeneous single prey environments did not select for reduced learning ability, as compared to natural prey-diverse environments, whereas a multi-generational pollen diet resulted in loss of learning, as compared to a diet of live prey. Associative learning produced stronger effects than non-associative learning but both types of experience produced persistent memory. Our study represents a key example of environmentally caused variation in learning ability and performance.     

The genetic population structure of the ant Plagiolepis xene-implications for genetic vulnerability of obligate social parasites

Obligatory social parasites, such as ant species that need colonies of other ant species for reproduction, are rare and many of them are classified as vulnerable. This is especially the case with highly adapted permanent inquilines that are specialised on one or a few host species. Their rarity may be due to reduced dispersal abilities, as a result of reduced body size, altered wing morphology, and curtailed nuptial flight, eventually leading to inbreeding. Furthermore, the host populations may differ in their ability to resist the parasite, yet the conditions of successful parasite invasion are largely unknown. Here we investigated the population structure of the inquiline ant Plagiolepis xene and its host P. pygmaea, using microsatellite data. Genetic differentiation, inbreeding, the effective population size and nest kin structure were analysed. We found that populations of P. xene are established by a single or at most a few individuals, and that the populations were genetically highly differentiated. However, within individual host populations the parasite is able to maintain panmixia, although data on the host suggests that the local distribution of the parasite also follows patterns of substructuring in the host population. Altogether our results suggest that inquiline parasite populations are genetically highly vulnerable.     

Demographic variability and heterogeneity among individuals within and among clonal bacteria strains

Identifying what drives individual heterogeneity has been of long interest to ecologists, evolutionary biologists and biodemographers, because only such identification provides deeper understanding of ecological and evolutionary population dynamics. In natural populations one is challenged to accurately decompose the drivers of heterogeneity among individuals as genetically fixed or selectively neutral. Rather than working on wild populations we present here data from a simple bacterial system in the lab, Escherichia coli. Our system, based on cutting‐edge microfluidic techniques, provides high control over the genotype and the environment. It therefore allows to unambiguously decompose and quantify fixed genetic variability and dynamic stochastic variability among individuals. We show that within clonal individual variability (dynamic heterogeneity) in lifespan and lifetime reproduction is dominating at about 90–92%, over the 8–10% genetically (adaptive fixed) driven differences. The genetic differences among the clonal strains still lead to substantial variability in population growth rates (fitness), but, as well understood based on foundational work in population genetics, the within strain neutral variability slows adaptive change, by enhancing genetic drift, and lowering overall population growth. We also revealed a surprising diversity in senescence patterns among the clonal strains, which indicates diverse underlying cell‐intrinsic processes that shape these demographic patterns. Such diversity is surprising since all cells belong to the same bacteria species, E. coli, and still exhibit patterns such as classical senescence, non‐senescence, or negative senescence. We end by discussing whether similar levels of non‐genetic variability might be detected in other systems and close by stating the open questions how such heterogeneity is maintained, how it has evolved, and whether it is adaptive.     

MicroRNA predictors of longevity in Caenorhabditis elegans

Neither genetic nor environmental factors fully account for variability in individual longevity: genetically identical invertebrates in homogenous environments often experience no less variability in lifespan than outbred human populations. Such variability is often assumed to result from stochasticity in damage accumulation over time; however, the identification of early-life gene expression states that predict future longevity would suggest that lifespan is least in part epigenetically determined. Such "biomarkers of aging," genetic or otherwise, nevertheless remain rare. In this work, we sought early-life differences in organismal robustness in unperturbed individuals and examined the utility of microRNAs, known regulators of lifespan, development, and robustness, as aging biomarkers. We quantitatively examined Caenorhabditis elegans reared individually in a novel apparatus and observed throughout their lives. Early-to-mid-adulthood measures of homeostatic ability jointly predict 62% of longevity variability. Though correlated, markers of growth/muscle maintenance and of metabolic by-products ("age pigments") report independently on lifespan, suggesting that graceful aging is not a single process. We further identified three microRNAs in which early-adulthood expression patterns individually predict up to 47% of lifespan differences. Though expression of each increases throughout this time, mir-71 and mir-246 correlate with lifespan, while mir-239 anti-correlates. Two of these three microRNA "biomarkers of aging" act upstream in insulin/IGF-1-like signaling (IIS) and other known longevity pathways, thus we infer that these microRNAs not only report on but also likely determine longevity. Thus, fluctuations in early-life IIS, due to variation in these microRNAs and from other causes, may determine individual lifespan.     

Variable pathogenicity determines individual lifespan in Caenorhabditis elegans

A common property of aging in all animals is that chronologically and genetically identical individuals age at different rates. To unveil mechanisms that influence aging variability, we identified markers of remaining lifespan for Caenorhabditis elegans. In transgenic lines, we expressed fluorescent reporter constructs from promoters of C. elegans genes whose expression change with age. The expression levels of aging markers in individual worms from a young synchronous population correlated with their remaining lifespan. We identified eight aging markers, with the superoxide dismutase gene sod-3 expression being the best single predictor of remaining lifespan. Correlation with remaining lifespan became stronger if expression from two aging markers was monitored simultaneously, accounting for up to 49% of the variation in individual lifespan. Visualizing the physiological age of chronologically-identical individuals allowed us to show that a major source of lifespan variability is different pathogenicity from individual to individual and that the mechanism involves variable activation of the insulin-signaling pathway.     

Experimental evidence for innate predator recognition in the Seychelles warbler.

Nest predation is a major determinant of fitness in birds and costly nest defence behaviours have evolved in order to reduce nest predation. Some avian studies have suggested that predator recognition is innate whereas others have stressed the importance of learning. However, none of these studies controlled for the genetic origin of the populations investigated and the effect of unfamiliarity with the predator. Here we determined whether experience with a nest predator is a prerequisite for nest defence by comparing predator recognition responses between two isolated but genetically similar Seychelles warbler (Acrocephalus sechellensis) populations, only one of which had experience of the egg predating Seychelles fody (Foudia sechellarum). Individuals in the predator-free population significantly reduced nest guarding compared to individuals in the population with the predator, which indicates that this behaviour was adjusted to the presence of nest predators. However, recognition responses (measured as both alarm call and attack rates) towards a mounted model of the fody were equally strong in both populations and significantly higher than the responses towards either a mounted familiar non-predator and a mounted, novel, non-predator bird species. Responses did not differ with a warbler's age and experience with the egg predator, indicating that predator recognition is innate.     

Allozyme Diversity in Non-social Spiders: Pattern, Process and Conservation Implications

In this article we summarize estimates of genetic variation based on allozymes for 30 non-social spider species. Overall, these species show moderate levels of genetic variability (mean H_o = 6.8%) compared to other invertebrate species surveyed for allozymes, although a number of spiders possess only minimal variation. Fossorial spiders, especially those which are coastal dune dwellers, typically display less variation than other non-social arachnids. In general, differences in heterozygosity estimates between groups of non-social spiders in this article are not confounded by the varying mix of proteins that have been assayed by individual investigators. There is a significant positive relationship between genetic variability and gene flow (Nm), indicating that non-social spider populations which exhibit reduced variability are likely to be genetically isolated. Population bottlenecks, directional selection and environmental homogeneity have all been cited to account for reduced variability in particular non-social spiders. In addition, an analysis using the genus Lutica suggests that low genetic variation may be accompanied by decreased population fitness. Since the potential for evolutionary change is dependent on the existence of genetic variability, our findings indicate that a number of non-social spiders may be at risk in terms of long-term population viability. This conclusion should be verified/extended via a combination of more genetic surveys; genetic and ecological monitoring of populations and their fitnesses in the wild; and experimental studies of the mechanisms underlying fitness differences.     

Predation, individual variability and vertebrate population dynamics

Both predation and individual variation in life history traits influence population dynamics. Recent results from laboratory predator–prey systems suggest that differences between individuals can also influence predator–prey dynamics when different genotypes experience different predation-associated mortalities. Despite the growing number of studies in this field, there is no synthesis identifying the overall importance of the interactions between predation and individual heterogeneity and their role in shaping the dynamics of free-ranging populations of vertebrates. We aim to fill this gap with a review that examines how individual variability in prey susceptibility, in predation costs, in predator selectivity, and in predatory performance, might influence prey population dynamics. Based on this review, it is clear that (1) predation risk and costs experienced by free-ranging prey are associated with their phenotypic attributes, (2) many generalist predator populations consist of individual specialists with part of the specialization associated with their phenotypes, and (3) a complete understanding of the population dynamic consequences of predation may require information on individual variability in prey selection and prey vulnerability. Altogether, this work (1) highlights the importance of maintaining long-term, detailed studies of individuals of both predators and prey in contrasting ecological conditions, and (2) advocates for a better use of available information to account for interactive effects between predators and their prey when modelling prey population dynamics.     

The adaptive significance of population differentiation in offspring size of the least killifish,Heterandria formosa

We tested the hypothesis that density‐dependent competition influences the evolution of offspring size. We studied two populations of the least killifish (Heterandria formosa) that differ dramatically in population density; these populations are genetically differentiated for offspring size, and females from both populations produce larger offspring when they experience higher social densities. To look at the influences of population of origin and relative body size on competitive ability, we held females from the high‐density population at two different densities to create large and small offspring with the same genetic background. We measured the competitive ability of those offspring in mesocosms that contained either pure or mixed population treatments at either high or low density. High density increased competition, which was most evident in greatly reduced individual growth rates. Larger offspring from the high‐density population significantly delayed the onset of maturity of fish from the low‐density population. From our results, we infer that competitive conditions in nature have contributed to the evolution of genetically based interpopulation differences in offspring size as well as plasticity in offspring size in response to conspecific density.     

Talitrid orientation as bioindicator of shoreline stability: Protected headland-bays versus exposed extended beaches

The behaviour of talitrids, being a local adaptation to beaches, is known to be related to environmental stability. The use of behavioural responses of resident populations as bioindicator of shoreline stability has been tested under various conditions, including after soft and hard engineering actions to stabilise eroded beaches. Port structures likely have impact on sediment longshore transportation and shoreline stability. The question was whether talitrid orientation behaviour could be proposed as bioindicator of impacts also for sandy bays of limited extension and highly used for recreation, such as those in the vicinity of touristic port structures. Orientation experiments were carried out on a set of sandy beaches of different extension and morphology, each of them in the vicinity of a touristic port, across the Mediterranean coasts. The protocol included field orientation tests of populations of talitrids, then analysed in terms of orientation precision seawards (considering sun compass orientation as the most locally adapted behavioural mechanism) in different seasons (before and after the touristic season) and times of day. The populations from more protected (either naturally or artificially) headland-bays showed a higher precision of orientation with respect to the shoreline direction than those from extended beaches, more subject to changes in longshore sedimentary transport as consequence of natural and human activities. The distance from the port and touristic pressure had no influence on talitrid orientation. An important stabilising factor for the sandy beach ecosystems, including talitrid populations and their behavioural adaptation, appeared to be the presence of seagrass banquette. The behavioural data point out that biotic information proceeding from local animal populations linked to beach sediments may complement sedimentology data and allow scaling the impacts occurring on a developed coastline. This becomes particularly relevant when considering interdisciplinary approaches to monitoring strategies.     

Periodic Selection, Infectious Gene Exchange and the Genetic Structure of E. COLI Populations

As a consequence of sequential replacements by clones of higher fitness (periodic selection), bacterial populations would be continually purged of genetic variability, and the fate of selectively neutral alleles in very large populations of bacteria would be similar to that in demes of sexually reproducing organisms with small genetically effective population sizes. The significance of periodic selection in reducing genetic variability in these clonally reproducing species is dependent on the amount of genetic exchange between clones (recombination). In an effort to determine the relationship between the rates of periodic selection, recombination and the genetically effective sizes of bacterial populations, a model for periodic selection and infectious gene exchange has been developed and its properties analyzed. It shows that, for a given periodic selection regime, genetically effective population size increases exponentially with the rate of recombination.—With the parameters of this model in the range anticipated for natural populations of E. coli, the purging effects of periodic selection on genetic variability are significant; individual populations or lineages of this bacterial species would have very small genetically effective population sizes.—Based on this result, some other a priori considerations and a review of the results of epidemiological and genetic variability studies, it is postulated that E. coli is composed of a relatively limited number of geographically widespread and genetically nearly isolated and monomorphic lineages. The implications of these considerations of the genetic structure of E. coli populations of the interpretation of protein variation and the neutral gene hypothesis are discussed.     

Congruent population structure inferred from dispersal behaviour and intensive genetic surveys of the threatened Florida scrub-jay (Aphelocoma coerulescens)

The delimitation of populations, defined as groups of individuals linked by gene flow, is possible by the analysis of genetic markers and also by spatial models based on dispersal probabilities across a landscape. We combined these two complimentary methods to define the spatial pattern of genetic structure among remaining populations of the threatened Florida scrub-jay, a species for which dispersal ability is unusually well-characterized. The range-wide population was intensively censused in the 1990s, and a metapopulation model defined population boundaries based on predicted dispersal-mediated demographic connectivity. We subjected genotypes from more than 1000 individual jays screened at 20 microsatellite loci to two Bayesian clustering methods. We describe a consensus method for identifying common features across many replicated clustering runs. Ten genetically differentiated groups exist across the present-day range of the Florida scrub-jay. These groups are largely consistent with the dispersal-defined metapopulations, which assume very limited dispersal ability. Some genetic groups comprise more than one metapopulation, likely because these genetically similar metapopulations were sundered only recently by habitat alteration. The combined reconstructions of population structure based on genetics and dispersal-mediated demographic connectivity provide a robust depiction of the current genetic and demographic organization of this species, reflecting past and present levels of dispersal among occupied habitat patches. The differentiation of populations into 10 genetic groups adds urgency to management efforts aimed at preserving what remains of genetic variation in this dwindling species, by maintaining viable populations of all genetically differentiated and geographically isolated populations.     

Genetic and morphological differentiation between remnant populations of an endangered species: the case of the Seychelles White-eye

The Seychelles White-eye Zosterops modestus is a critically endangered species that survives in two remnant populations on the islands of Mahé and Conception. Multilocus minisatellite DNA fingerprinting and morphometric measurements were used to assess the levels of variation between these populations. Mahé White-eyes are on average significantly larger than Conception birds, as are males compared to females. The mean level of bandsharing ( c.  60%) indicates low levels of genetic variability within both populations. Bandsharing is significantly lower between populations (32%), suggesting that the two populations are genetically isolated from each other, and that one is not a subsample from the other. Both populations should therefore be considered as equally important genetic reservoirs that deserve to be safeguarded. Although each population appears locally adapted to its particular island environment, such limited differentiation is not considered of major taxonomic significance. Recombining genetic variation by mixing individuals from both populations may be beneficial for the species in view of future island transfers. This illustrates the importance of investigating differentiation between remnant populations of a threatened species to orientate future conservation and management measures.     

Nocturnal homing in pigeons

• 1.1. A total of 541 pigeons from 3 populations was tested for the ability of nocturnal homing over increasing distances from 1 to 33 km.
• 2.2. Nocturnal homing over 20 km was an individual characteristic found only in a fraction of pigeons in a loft (30–35%). Its expression was not affected by variables influencing diurnal homing performance such as age, experience and breeding status.
• 3.3. This particular ability is likely to reflect superior navigational abilities related to non-visual orientation mechanisms.
• 4.4. The ability for nocturnal homing is probably genetically dependent: offspring from good nocturnal homers performed significantly better than offspring from poor homers.

     

GENETIC DIVERGENCE IN PERIPHERALLY ISOLATED POPULATIONS OF CHAFFINCHES IN THE ATLANTIC ISLANDS

Peripherally isolated populations of common chaffinches (Fringilla coelebs) in the Canaries, Madeira, and Azores were compared genetically with their putative ancestral stock in Iberia and Morocco, and with a population of blue chaffinches (F. teydea) from Tenerife, using protein electrophoresis of 42 loci. The continental populations are only weakly differentiated genetically (F_ST = 0.092), despite distinctive subspecific differences in plumage and morphometrics between Iberia and Morocco populations. Estimated levels of gene flow among continental populations are high enough to account for their relative genetic homogeneity, and it is unlikely that homogenizing selection is operating to mimic the effects of gene flow. In contrast, the Atlantic island populations are well differentiated genetically (F_ST = 0.321), and have diverged considerably from their continental conspecifics. The development of significant genetic differentiation within the Canaries but not the Azores likely results from smaller population sizes, very restricted gene flow, and enhanced random drift in the former populations. There is no convincing evidence in support of stronger directional selection acting on genotypes or phenotypes to reduce within-population variability in Canaries populations as proposed by Grant (1979), although other tenets of his model of island evolution are supported by our analysis. Although genetic variability is reduced in four of the Canaries populations, only the Hierro population appears to have encountered a severe bottleneck. Yet it has not differentiated markedly from the La Palma population to which it is subspecifically allied. We conclude that gradual divergence in isolated populations of small to moderate size is the most plausible explanation for the evolution of intraspecific and interspecific diversity in Atlantic island chaffinches.