Kin association during brood care in a facultatively social bird: active discrimination or by‐product of partner choice and demography?

Intra-group relatedness does not necessarily imply kin selection, a leading explanation for social evolution. An overlooked mechanism for generating population genetic structure is variation in longevity and fecundity, referred to as individual quality, affecting kin structure and the potential for cooperation. Individual quality also affects choosiness in partner choice, a key process explaining cooperation through direct fitness benefits. Reproductive skew theory predicts that relatedness decreases with increasing group size, but this relationship could also arise because of quality-dependent demography and partner choice, without active kin association. We addressed whether brood-rearing eider (Somateria mollissima) females preferentially associated with kin using a 6-year data set with individuals genotyped at 19 microsatellite loci and tested whether relatedness decreased with increasing female group size. We also determined the relationship between local relatedness and indices of female age and body condition. We further examined whether the level of female intracoalition relatedness differed from background relatedness in any year. As predicted, median female intra-group relatedness decreased with increasing female group size. However, the proportion of related individuals increased with advancing female age, and older females prefer smaller brood-rearing coalitions, potentially producing a negative relationship between group size and relatedness. There were considerable annual fluctuations in the level of relatedness between coalition-forming females, and in 1year this level exceeded that expected by random association. Thus, both passive and active mechanisms govern kin associations in brood-rearing eiders. Eiders apparently can discriminate between kin, but the benefits of doing so may vary over time.     

Parasite‐induced surfacing in the cockle Austrovenus stuchburyi: adaptation or not?

Parasite manipulation of host behaviour is a compelling example of the extended phenotype. However, in many cases, such manipulation may be incorrectly assumed. Previous work has demonstrated that Austrovenus stuchburyi cockles stranded on mud-flat surfaces due to an inability to re-burrow both contain significantly more metacercariae of the trematode Curtuteria australis and are predated by the definitive host of this parasite at a faster rate than burrowed cockles. These results have been interpreted as strong evidence for a manipulation of cockle behaviour by the trematode to facilitate transmission to the definitive host. The model presented here, however, indicates that the selective advantage to the parasite of the altered host behaviour is currently of a negligible level at our study site that is highly unlikely to have been realized as an adaptation over evolutionary time. Hence, there are no grounds on which the more parsimonious explanation, that the altered host behaviour observed is simply an incidental side-effect of infection, can be rejected. We thus maintain that for any change in the behaviour of infected hosts to be confirmed as potentially a parasite trait that has evolved in response to selection, the adaptive benefit taking into account the entire parasite life cycle may need to be considered.     

Are habitat fragmentation,local adaptation and isolation‐by‐distance driving population divergence in wild rice Oryza rufipogon?

Habitat fragmentation weakens the connection between populations and is accompanied with isolation by distance (IBD) and local adaptation (isolation by adaptation, IBA), both leading to genetic divergence between populations. To understand the evolutionary potential of a population and to formulate proper conservation strategies, information on the roles of IBD and IBA in driving population divergence is critical. The putative ancestor of Asian cultivated rice (Oryza sativa) is endangered in China due to habitat loss and fragmentation. We investigated the genetic variation in 11 Chinese Oryza rufipogon populations using 79 microsatellite loci to infer the effects of habitat fragmentation, IBD and IBA on genetic structure. Historical and current gene flows were found to be rare (m_h = 0.0002–0.0013, m_c = 0.007–0.029), indicating IBD and resulting in a high level of population divergence (F_ST = 0.343). High within‐population genetic variation (H_E = 0.377–0.515), relatively large effective population sizes (N_e = 96–158), absence of bottlenecks and limited gene flow were found, demonstrating little impact of recent habitat fragmentation on these populations. Eleven gene‐linked microsatellite loci were identified as outliers, indicating local adaptation. Hierarchical AMOVA and partial Mantel tests indicated that population divergence of Chinese O. rufipogon was significantly correlated with environmental factors, especially habitat temperature. Common garden trials detected a significant adaptive population divergence associated with latitude. Collectively, these findings imply that IBD due to historical rather than recent fragmentation, followed by local adaptation, has driven population divergence in O. rufipogon.     

Clonal genetic variation in a Wolbachia‐infected asexual wasp: horizontal transmission or historical sex?

Wolbachia are endocellular bacteria known for manipulating the reproductive systems of many of their invertebrate hosts. Wolbachia are transmitted vertically from mother to offspring. In addition, new infections result from horizontal transmission between different host species. However, to what extent horizontal transmission plays a role in the spread of a new infection through the host population is unknown. Here, we investigate whether horizontal transmission of Wolbachia can explain clonal genetic variation in natural populations of Leptopilina clavipes, a parasitoid wasp infected with a parthenogenesis‐inducing Wolbachia. We assessed variance of markers on the nuclear, mitochondrial and Wolbachia genomes. The nuclear and mitochondrial markers displayed significant and congruent variation among thelytokous wasp lineages, showing that multiple lineages have become infected with Wolbachia. The alternative hypothesis in which a single female became infected, the daughters of which mated with males (thus introducing nuclear genetic variance) cannot account for the presence of concordant variance in mtDNA. All Wolbachia markers, including the hypervariable wsp gene, were invariant, suggesting that only a single strain of Wolbachia is involved. These results show that Wolbachia has transferred horizontally to infect multiple female lineages during the early spread through L. clavipes. Remarkably, multiple thelytokous lineages have persisted side by side in the field for tens of thousands of generations.     

Speciation‐by‐depth on coral reefs: Sympatric divergence with gene flow or cryptic transient isolation?

The distributions of many sister species in the sea overlap geographically but are partitioned along depth gradients. The genetic changes leading to depth segregation may evolve in geographic isolation as a prerequisite to coexistence or may emerge during primary divergence leading to new species. These alternatives can now be distinguished via the power endowed by the thousands of scorable loci provided by second‐generation sequence data. Here, we revisit the case of two depth‐segregated, genetically isolated ecotypes of the nominal Caribbean candelabrum coral Eunicea flexuosa. Previous analyses based on a handful of markers could not distinguish between models of genetic exchange after a period of isolation (consistent with secondary contact) and divergence with gene flow (consistent with primary divergence). Analyses of the history of isolation, genetic exchange and population size based on 15,640 new SNP markers derived from RNAseq data best support models where divergence began 800K BP and include epochs of divergence with gene flow, but with an intermediate period of transient isolation. Results also supported the previous conclusion that recent exchange between the ecotypes occurs asymmetrically from the Shallow lineage to the Deep. Parallel analyses of data from two other corals with depth‐segregated populations (Agaricia fragilis and Pocillopora damicornis) suggest divergence leading to depth‐segregated populations may begin with a period of symmetric exchange, but that an epoch of population isolation precedes more complete isolation marked by asymmetric introgression. Thus, while divergence‐with‐gene flow may account for much of the differentiation that separates closely related, depth‐segregated species, it remains to be seen whether any critical steps in the speciation process only occur when populations are isolated.     

Testing alternative models for sexual isolation in natural populations of Littorina saxatilis: indirect support for by‐product ecological speciation?

Two ecotypes of the rough periwinkle Littorina saxatilis occur at different shore levels, showing assortative mating for size and partial reproductive isolation when they meet at the mid-shore. This system represents a putative case of incomplete speciation in sympatry. Two processes contribute to the assortative mating: morph-specific microhabitat aggregation and mate choice. The estimation of mate choice coefficients in nature and a simulation of the aggregation effects on sexual isolation were used to disentangle these processes as well as to test alternative mechanisms of mate choice. Mate choice significantly increased the frequency of within-morph pairs and significantly decreased the frequency of between-morph pairs, whereas those pairs including at least one hybrid morph mated randomly. These results allow us to reject a discriminant mate choice and support a model of evolution of sexual isolation as a side-effect of size-assortative mating in a context of divergent natural selection for size in the population. This mechanism is more compatible with a model of incomplete by-product ecological speciation, as suggested by previous evidence.     

Why does the magnitude of genotype‐by‐environment interaction vary?

Genotype‐by‐environment interaction (G × E), that is, genetic variation in phenotypic plasticity, is a central concept in ecology and evolutionary biology. G×E has wide‐ranging implications for trait development and for understanding how organisms will respond to environmental change. Although G × E has been extensively documented, its presence and magnitude vary dramatically across populations and traits. Despite this, we still know little about why G × E is so evident in some traits and populations, but minimal or absent in others. To encourage synthetic research in this area, we review diverse hypotheses for the underlying biological causes of variation in G × E. We extract common themes from these hypotheses to develop a more synthetic understanding of variation in G × E and suggest some important next steps.     

Superparasitism evolution: adaptation or manipulation?

Superparasitism refers to the oviposition behavior of parasitoid females who lay their eggs in an already parasitized host. This often yields intense competition among larvae that are sharing the same host. Why would a female oviposit in such hostile habitat instead of looking for a better quality, unparasitized host? Here we present a continuous-time model of host-parasitoid interaction and discuss alternative scenarios. This model is first used to analyze the evolution of the superparasitism behavior of a solitary proovigenic parasitoid under both time and egg limitation. Then, following the recent discovery by Varaldi et al., we allow the parasitoid to be infected by a virus that alters the superparasitism behavior of its host to enhance its own horizontal transmission. The analysis of the coevolution of this manipulative behavior with the oviposition behavior of uninfected females clarifies and quantifies the conflict that emerges between the parasitoid and its virus. The model also yields new testable predictions. For example, we expect that uninfected parasitoids should superparasite less after coevolving with the manipulative virus. More generally, this model provides a theoretical framework for analyzing the evolution of the manipulation of parasitoid life-history traits by microparasites.     

Diet mixing in a parasitic plant: adaptation or constraint?

Some herbivores deliberately consume a mixed diet, either to obtain a superior mix of nutrients or to avoid consuming too much of any one toxin. Few studies have examined diet mixing in parasitic plants, which typically have very broad host ranges. We offered the parasitic plant Cuscuta indecora (dodder), a range of mixtures of two hosts (Iva frutescens and Borrichia frutescens) in the greenhouse, and observed correlations between the host community and Cuscuta infection in the field. In the greenhouse, Cuscuta performed better on mixtures with a higher relative abundance of Iva. Cuscuta selectively foraged on whichever host was more abundant (diet switching), the exact opposite of the behavior that would be expected if diet mixing was advantageous. In the field, the intensity of Cuscuta infections was decreased by the presence of non-hosts (grasses), not strongly affected by the presence of intermediate hosts, and increased by the presence of Borrichia. We conclude that Cuscuta does not obtain nutritional benefits from a broad diet, but instead is constrained by its relative lack of mobility to attack hosts of intermediate value. In general, the lack of mobility of parasitic plants compared to herbivores probably selects for broad host ranges in parasitic plants.     

Local adaptation to salinity in the three‐spined stickleback?

Different lines of evidence suggest that the occurrence and extent of local adaptation in high gene flow marine environments – even in mobile and long‐lived vertebrates with complex life cycles – may be more widespread than earlier thought. We conducted a common garden experiment to test for local adaptation to salinity in Baltic Sea sticklebacks (Gasterosteus aculeatus). Fish from three different native salinity regimes (high, mid and low) were subjected to three salinity treatments (high, mid and low) in a full‐factorial experimental design. Irrespective of their origin, fish subjected to low (and mid) salinity treatments exhibited higher juvenile survival, grew to largest sizes and were in better condition than fish subjected to the high salinity treatment. However, a significant interaction between native and treatment salinities – resulting mainly from the poor performance of fish native to low salinity in the high salinity treatment – provided clear cut evidence for adaptation to local variation in salinity. Additional support for this inference was provided by the fact that the results concur with an earlier demonstration of significant differentiation in a number of genes with osmoregulatory functions across the same populations and that the population‐specific responses to salinity treatments exceeded that to be expected by random genetic drift.     

Transgene integration in plants: poking or patching holes in promiscuous genomes?

Transgene integration in plants transformed by either Agrobacterium or direct DNA delivery methods occurs through illegitimate recombination (IR). The precise mechanism(s) for IR-mediated transgene integration and the role of host double-strand break repair enzymes remain unknown. A recent wealth of sequenced transgene loci and investigations aimed at genetically dissecting transgene integration mechanism(s) have provided new insights into the process.     

Male genes: X‐pelled or X‐cluded?

Two recent studies by Parisi et al. and Ranz et al., catalogue sex differences in gene expression across the whole genome of the fruit fly Drosophila melanogaster. Both report striking associations of sex-biased gene expression with the X chromosome. Genes with male-biased expression are depauperate on the X chromosome, whereas genes with female-biased expression show weaker evidence of being in excess. A number of evolutionary hypotheses for the expulsion or exclusion of male-biased genes from the X chromosome have been suggested. None is entirely consistent with the available evidence.     

Mahonia invasions in different habitats: local adaptation or general-purpose genotypes?

Rapid evolutionary adaptations and phenotypic plasticity have been suggested to be two important, but not mutually exclusive, mechanisms contributing to the spread of invasive species. Adaptive evolution in invasive plants has been shown to occur at large spatial scales to different climatic regions, but local adaptation at a smaller scale, e.g. to different habitats within a region, has rarely been studied. Therefore, we performed a case study on invasive Mahonia populations to investigate whether local adaptation may have contributed to their spread. We hypothesized that the invasion success of these populations is promoted by adaptive differentiation in response to local environmental conditions, in particular to the different soils in these habitats. To test this hypothesis, we carried out a reciprocal transplantation experiment in the field using seedlings from five Mahonia populations in Germany that are representative for the range of habitats invaded, and a greenhouse experiment that specifically compared the responses to the different soils of these habitats. We found no evidence for local adaptation of invasive Mahonia populations because seedlings from all populations responded similarly to different habitats and soils. In a second greenhouse experiment we examined genetic variation within populations, but seedlings from different maternal families did not vary in their responses to soil conditions. We therefore suggest that local adaptation of seedlings does not play a major role for the invasion success of Mahonia populations and that phenotypic plasticity, instead, could be an important trait in this stage of the life cycle.     

Predator‐induced phenotypic plasticity in tadpoles: extension or innovation?

Phenotypic plasticity, the ability of a trait to change as a function of the environment, is central to many ideas in evolutionary biology. A special case of phenotypic plasticity observed in many organisms is mediated by their natural predators. Here, we used a predator-prey system of dragonfly larvae and tadpoles to determine if predator-mediated phenotypic plasticity provides a novel way of surviving in the presence of predators (an innovation) or if it represents a simple extension of the way noninduced tadpoles survive predation. Tadpoles of Limnodynastes peronii were raised in the presence and absence of predation, which then entered a survival experiment. Induced morphological traits, primarily tail height and tail muscle height, were found to be under selection, indicating that predator-mediated phenotypic plasticity may be adaptive. Although predator-induced animals survived better, the multivariate linear selection gradients were similar between the two tadpole groups, suggesting that predator-mediated phenotypic plasticity is an extension of existing survival strategies. In addition, nonlinear selection gradients indicated a cost of predator-induced plasticity that may limit the ability of phenotypic plasticity to enhance survival in the presence of predators.     

Trophic control of mesopredators in terrestrial ecosystems: top‐down or bottom‐up?

It has been argued that widespread extinctions of top predators have changed terrestrial ecosystem structures through mesopredator release, where increased abundances of medium-sized predators have detrimental effects on prey communities. This top-down concept has received much attention within conservation biology, but few studies have demonstrated the phenomenon. The concept has been criticized since alternative explanations involving bottom-up impacts from bioclimatic effects on ecosystem productivity and from anthropogenic habitat change are rarely considered. We analyse the response of a mesopredator (the red fox) to declines in top predators (wolf and Eurasian lynx) and agricultural expansion over 90 years in Sweden, taking bioclimatic effects into account. We show a top-down mesopredator release effect, but ecosystem productivity determined its strength. The impacts of agricultural activity were mediated by their effects on top predator populations. Thus, both top-down and bottom-up processes need to be understood for effective preservation of biodiversity in anthropogenically transformed ecosystems.