Matthew K. Oliver

Spatio-temporal variation in the strength and mode of selection acting on major histocompatibility complex diversity in water vole (Arvicola terrestris) metapopulations

Patterns of spatio‐temporal genetic variation at a class II major histocompatibility complex (MHC) locus and multiple microsatellite loci were analysed within and between three water vole metapopulations in Scotland, UK. Comparisons of MHC and microsatellite spatial genetic differentiation, based on standardised tests between two demographically asynchronous zones within a metapopulation, suggested that spatial MHC variation was affected by balancing selection, directional selection and random genetic drift, but that the relative effects of these microevolutionary forces vary temporally. At the metapopulation level, between‐year differentiation for MHC loci was significantly correlated with that of microsatellites, signifying that neutral factors such as migration and drift were primarily responsible for overall temporal genetic change at the metapopulation scale. Between metapopulations, patterns of genetic differentiation implied that, at large spatial scales, MHC variation was primarily affected by directional selection and drift. Levels of MHC heterozygosity in excess of Hardy–Weinberg expectations were consistent with overdominant balancing selection operating on MHC variation within metapopulations. However, this effect was not constant among all samples, indicating temporal variation in the strength of selection relative to other factors. The results highlight the benefit of contrasting variation at MHC with neutral markers to separate the effects of stochastic and deterministic microevolutionary forces, and add to a growing body of evidence showing that the mode and relative strength of selection acting on MHC diversity varies both spatially and temporally.

Selection Maintains MHC Diversity through a Natural Population Bottleneck

A perceived consequence of a population bottleneck is the erosion of genetic diversity and concomitant reduction in individual fitness and evolutionary potential. Although reduced genetic variation associated with demographic perturbation has been amply demonstrated for neutral molecular markers, the effective management of genetic resources in natural populations is hindered by a lack of understanding of how adaptive genetic variation will respond to population fluctuations, given these are affected by selection as well as drift. Here, we demonstrate that selection counters drift to maintain polymorphism at a major histocompatibility complex (MHC) locus through a population bottleneck in an inbred island population of water voles. Before and after the bottleneck, MHC allele frequencies were close to balancing selection equilibrium but became skewed by drift when the population size was critically low. MHC heterozygosity generally conformed to Hardy-Weinberg expectations except in one generation during the population recovery where there was a significant excess of heterozygous genotypes, which simulations ascribed to strong differential MHC-dependent survival. Low allelic diversity and highly skewed frequency distributions at microsatellite loci indicated potent genetic drift due to a strong founder affect and/or previous population bottlenecks. This study is a real-time examination of the predictions of fundamental evolutionary theory in low genetic diversity situations. The findings highlight that conservation efforts to maintain the genetic health and evolutionary potential of natural populations should consider the genetic basis for fitness-related traits, and how such adaptive genetic diversity will vary in response to both the demographic fluctuations and the effects of selection.

Do rabbits eat voles? Apparent competition, habitat heterogeneity and large-scale coexistence under mink predation

Habitat heterogeneity is predicted to profoundly influence the dynamics of indirect interspecific interactions; however, despite potentially significant consequences for multi-species persistence, this remains almost completely unexplored in large-scale natural landscapes. Moreover, how spatial habitat heterogeneity affects the persistence of interacting invasive and native species is also poorly understood. Here we show how the persistence of a native prey (water vole, Arvicola terrestris) is determined by the spatial distribution of an invasive prey (European rabbit, Oryctolagus cuniculus) and directly infer how this is defined by the mobility of a shared invasive predator (American mink, Neovison vison). This study uniquely demonstrates that variation in habitat connectivity in large-scale natural landscapes creates spatial asynchrony, enabling coexistence between apparent competitive native and invasive species. These findings highlight that unexpected interactions may be involved in species declines, and also that in such cases habitat heterogeneity should be considered in wildlife management decisions.

Isolation and characterization of a MHC class II DRB locus in the European water vole (Arvicola terrestris)

In so-called model species, such as human and mouse, genes of the major histocompatibility complex (MHC) are characterized by extremely high levels of polymorphism, and it is considered that such diversity is maintained by balancing selection. `There is now a recognized need to expand studies into nonmodel species to examine whether high MHC diversity is mirrored in natural populations, and to determine the ecological, ethological, and evolutionary processes that underpin balancing selection. To address such issues, a necessary prerequisite is the ability to characterize diversity at a single, expressed, polymorphic MHC locus on which selection may be acting. Here, we provide the first description of allelic diversity at exon 2 of an MHC class II DRB locus in the European water vole (Arvicola terrestris), characterize variation across four natural populations, and test whether the patterns of variation are consistent with the effects of balancing selection. Using single-strand conformation polymorphism analysis and subsequent DNA sequencing of gel excisions, five DRB alleles were resolved, each with a unique amino acid sequence, among 100 individuals from four geographically distinct populations. Reverse transcription polymerase chain reaction confirmed that the alleles were products from an expressed locus. Intra-allelic amino acid differences were high (10.5–33.3%), and the nonsynonymous substitution rate exceeded the synonymous substitution rate for the functional peptide-binding region (dN:dS=3.91 and P<0.005). Phylogenetic comparison of resolved alleles with closely related homologues indicated that each allele represented a unique lineage preserved across speciation events. These results indicate that balancing selection has maintained diversity of DRB allelic lineages and amino acid function over evolutionary time scales, but may be less effective at preserving alleles in contemporary populations where stochastic microevolutionary processes may dominate.

Individual variation in dispersal associated with phenotype influences fine-scale genetic structure in weasels

In general, landscape genetic studies have ignored the potential role that the phenotype of individuals plays in determining fine-scale genetic structure in species. This potential over-simplification ignores an important component that dispersal is both condition- and phenotype-dependent. In order to investigate the relationship between potential dispersal, habitat selection and phenotype, we examined the spatial ecology, body mass and fine-scale genetic structure of weasels (Mustela nivalis) in Białowieża Forest in Poland. Our study population is characterized by an almost three-fold phenotypic variation in adult body mass and weasels were segregated in certain habitats according to size. We detected significant genetic structuring associated with habitat within the studied area and analyses of radio-tracking and re-capture data showed that the maximum extent of movement was achieved by weasels of medium body size, whereas the smallest and largest individuals exhibited higher site fidelity. With the unrestricted movement of the medium-sized individuals across optimal habitat, genetic admixture does occur. However, the presence of a barrier leads to unidirectional gene flow, with larger individuals outcompeting smaller individuals and therefore maintaining the genetic break in the study area. This highlights the importance of considering both intrinsic (phenotype) and extrinsic (environmental) factors in understanding dispersal patterns and ultimately, gene flow in complex landscapes.

Beyond splitting hares and rabbiting on about major histocompatibility complex complexity

The genes of the major histocompatibility complex (MHC) have become the target of choice for studies wishing to examine adaptively important genetic diversity in natural populations. Within Molecular Ecology alone, there have been 71 papers on aspects of MHC evolution over the past few years, with an increasing year on year trend. This focus on the MHC is partly driven by the hypothesized links between MHC gene dynamics and ecologically interesting and relevant traits, such as mate choice and host–parasite interactions. However, an ability to pin down the evolutionary causes and ecological consequences of MHC variation in natural populations has proven challenging and has been hampered by the very issue that is attractive about MHC genes – their high levels of diversity. Linking high levels of MHC diversity to ecological factors in inherently complex natural populations requires a level of experimental design and analytical rigour that is extremely difficult to achieve owing to a plethora of potentially confounding and interacting variables. In this issue of Molecular Ecology, Smith et al. (2010) elegantly overcome the challenge of detecting complex interactions in complex systems by using an intricate analytical approach to demonstrate a role for MHC in the reproductive ability of a natural population of the European hare Lepus europaeus ( Fig. 1 ). Also in this issue, Oppelt et al. (2010) demonstrate a role for MHC variation in determining levels of hepatic coccidian infection in the European rabbit Oryctolagus cuniculus ( Fig. 2 ).

Relationship type affects the reliability of dispersal distance estimated using pedigree inferences in partially sampled populations : A case study involving invasive American mink in Scotland

Estimating dispersal—a key parameter for population ecology and management—is notoriously difficult. The use of pedigree assignments, aided by likelihood‐based software, has become popular to estimate dispersal rate and distance. However, the partial sampling of populations may produce false assignments. Further, it is unknown how the accuracy of assignment is affected by the genealogical relationships of individuals and is reflected by software‐derived assignment probabilities. Inspired by a project managing invasive American mink (Neovison vison), we estimated individual dispersal distances using inferred pairwise relationships of culled individuals. Additionally, we simulated scenarios to investigate the accuracy of pairwise inferences. Estimates of dispersal distance varied greatly when derived from different inferred pairwise relationships, with mother–offspring relationship being the shortest (average = 21 km) and the most accurate. Pairs assigned as maternal half‐siblings were inaccurate, with 64%–97% falsely assigned, implying that estimates for these relationships in the wild population were unreliable. The false assignment rate was unrelated to the software‐derived assignment probabilities at high dispersal rates. Assignments were more accurate when the inferred parents were older and immigrants and when dispersal rates between subpopulations were low (1% and 2%). Using 30 instead of 15 loci increased pairwise reliability, but half‐sibling assignments were still inaccurate (>59% falsely assigned). The most reliable approach when using inferred pairwise relationships in polygamous species would be not to use half‐sibling relationship types. Our simulation approach provides guidance for the application of pedigree inferences under partial sampling and is applicable to other systems where pedigree assignments are used for ecological inference.

Early life sensory ability-ventilatory responses of thornback ray embryos (Raja clavata) to predator-type electric fields.

Predator avoidance is fundamental for survival and it can be particularly challenging for prey animals if physical movement away from a predatory threat is restricted. Many sharks and rays begin life within an egg capsule that is attached to the sea bed. The vulnerability of this sedentary life stage is exacerbated in skates (Rajidae) as the compulsory ventilatory activity of embryos makes them conspicuous to potential predators. Embryos can reduce this risk by mediating ventilatory activity if they detect the presence of a predator using an acute electrosense. To determine how early in embryonic life predator elicited behavioral responses can occur, the reactions of three different age groups (1/3 developed, 2/3 developed, and near hatching) of embryonic thornback rays Raja clavata were tested using predator‐type electric field stimuli. Egg capsules were exposed to continuous or intermittent stimuli in order to assess varying predator‐type encounter scenarios on the ventilatory behavior of different developmental stages. All embryos reacted with a “freeze response” following initial electric field (E‐field) exposure, ceasing ventilatory behavior in response to predator presence, demonstrating electroreceptive functionality for the first time at the earliest possible stage in ontogeny. This ability coincided with the onset of egg ventilatory behavior and may represent an effective means to enhance survival. A continuous application of stimuli over time revealed that embryos can adapt their behavior and resume normal activity, whereas when presented intermittently, the E‐field resulted in a significant reduction in overall ventilatory activity across all ages. Recovery from stimuli was significantly quicker in older embryos, potentially indicative of the trade‐off between avoiding predation and adequate respiration.