Long-term fitness benefits of polyandry in a small mammal, the bank vole Clethrionomys glareolus

Polyandry, i.e. mating with multiple males within one reproductive event, is a common female mating strategy but its adaptive function is often unclear. We tested whether polyandrous females gain genetic benefits by comparing fitness traits of monandrous (mated twice with a single male) and polyandrous (mated twice with two different males) female bank voles Clethrionomys glareolus. We raised the offspring in the laboratory until adulthood and measured their body size, before releasing them to outdoor enclosures to overwinter. At the onset of the breeding season in the following spring, we found that offspring of polyandrous females performed significantly better at reproduction than those of monandrous females. This was mainly due to sons of polyandrous females producing significantly more offspring than those of monandrous females. No significant differences were found for offspring body mass or winter survival between the two treatments. Our results appear to provide evidence that bank vole females gain long-term benefits from polyandry.     

Behaviour and resource use of two competing vole species under shared predation risk

Indirect interaction between two competing species via a shared predator may be an important determinant of population and community dynamics. We studied the effect of predation risk imposed by the least weasel Mustela nivalis nivalis on space use, foraging and activity of two competing vole species, the grey-sided vole Myodes rufocanus, and the bank vole Myodes glareolus. The experiment was conducted in a large indoor arena, consisting of microhabitat structures providing food, shelter, trees for refuge and separated areas with high and low predation risk. Voles were followed for 5 days: 2 days before, 1 day during and 2 days after the presence of weasel. Our results suggest an effect of weasel presence on the vole community. Voles of both species shifted their activity from risky to less risky areas, climbed trees more often and were less active. Seed consumption was not affected by weasel presence. The time spent in the risky and less risky area did not differ between species, but bank voles spent more time in trees than grey-sided voles. Males of both species were more exposed to predation risk than females, i.e. generally spent more time in the risky area. Proportion of time spent in the risky area, the use of area, trees and food stations were sex dependent. Activity and use of trees were species dependent. We found no evidence for despotic distribution between our two species, although bank voles seemed to be more affected by coexistence, since they lost weight during the experiment. Based on our results we conclude that predator response was largely similar between species, while the sex-specific responses dominated. Besides a stronger escape response in the bank vole, the strongest individual differences were sex specific, i.e. males were more prone to take risks in space use and activity.     

Polyandry promotes enhanced offspring survival in decorated crickets

Although female multiple mating is ubiquitous in insects, its adaptive significance remains poorly understood. Benefits to multiple mating can accrue via direct material benefits, indirect genetic benefits, or both. We investigated the effects of multiple mating in the decorated cricket, Gryllodes sigillatus, by simultaneously varying the number of times that females mated and the number of different males with which they mated, measuring aspects of female fecundity and elements of offspring performance and viability. Multiple matings resulted in enhanced female fitness relative to single matings when females mated with different partners, but not when females mated repeatedly with the same male. Specifically, polyandrous females produced significantly more offspring surviving to reproductive maturity than did monogamous females mating once or mating repeatedly with the same male. These results suggest that the benefit females gain from multiple mating is influenced primarily by genetic and not material benefits.     

Relative costs of offspring sex and offspring survival in a polygynous mammal

Costs of reproduction are expected to be ubiquitous in wild animal populations and understanding the drivers of variation in these costs is an important aspect of life-history evolution theory. We use a 43 year dataset from a wild population of red deer to examine the relative importance of two factors that influence the costs of reproduction to mothers, and to test whether these costs vary with changing ecological conditions. Like previous studies, our analyses indicate fitness costs of lactation: mothers whose calves survived the summer subsequently showed lower survival and fecundity than those whose calves died soon after birth, accounting for 5% and 14% of the variation in mothers'' survival and fecundity, respectively. The production of a male calf depressed maternal survival and fecundity more than production of a female, but accounted for less than 1% of the variation in either fitness component. There was no evidence for any change in the effect of calf survival or sex with increasing population density.     

Sex- and concentration-dependent effects of predator feces on seasonal regulation of body mass in the bank vole Clethrionomys glareolus

Increased perception of predation risk can cause changes in activity, feeding and reproductive behavior in a wide range of taxa. Many small mammals in the temperate zone exhibit fluctuations in body mass in response to changing photoperiod. Bank voles lose body mass in winter which they regain when photoperiod increases in the spring. To determine if predation risk affects seasonal changes in body mass (BM), bank voles were exposed to two concentrations (low: LC and high: HC) of weasel feces. Food intake (FI) and daily energy expenditure (DEE) were measured to establish if differences in body mass were due to adjustment in energy intake or expenditure. Fecal corticosterone (CORT) was measured to assess whether the voles had detected and responded to predator feces as a physiological stressor. Voles of both sexes had higher levels of fecal CORT in the groups exposed to weasel feces compared to controls. Voles responded to the predator feces in a sex- and concentration-dependent manner. Males responded to LC feces by gaining less mass following the change in photoperiod. This was mediated by reduced FI and higher DEE. Female voles also gained less BM in response to HC feces, but increased both FI and DEE. We hypothesize that males may gain a short-term advantage by lowering BM in response to predation risk, which may be regained without affecting reproductive success. The consequences of mass loss in females may be more significant as this may delay the onset of breeding or reduce the size or number of young, thereby negatively affecting breeding success.     

The Celtic fringe of Britain: insights from small mammal phylogeography

Recent genetic studies have challenged the traditional view that the ancestors of British Celtic people spread from central Europe during the Iron Age and have suggested a much earlier origin for them as part of the human recolonization of Britain at the end of the last glaciation. Here we propose that small mammals provide an analogue to help resolve this controversy. Previous studies have shown that common shrews (Sorex araneus) with particular chromosomal characteristics and water voles (Arvicola terrestris) of a specific mitochondrial (mt) DNA lineage have peripheral western/northern distributions with striking similarities to that of Celtic people. We show that mtDNA lineages of three other small mammal species (bank vole Myodes glareolus, field vole Microtus agrestis and pygmy shrew Sorex minutus) also form a ‘Celtic fringe’. We argue that these small mammals most reasonably colonized Britain in a two-phase process following the last glacial maximum (LGM), with climatically driven partial replacement of the first colonists by the second colonists, leaving a peripheral geographical distribution for the first colonists. We suggest that these natural Celtic fringes provide insight into the same phenomenon in humans and support its origin in processes following the end of the LGM.     

Breeding suppression in the bank vole as antipredatory adaptation in a predictable environment

Summary In northern Fennoscandia, microtine rodent populations fluctuate cyclically. The environment of an individual vole can be considered to be predictable when the risks of predation and intra- and interspecific competition change with the cycle, such that both are high during the population highs of voles. The risk of predation is also high during the vole crash. After the crash, the vole population is characterized by low intra- and interspecific competition and low predation pressure. The main predators affecting voles during the crash are the small mustelids, least weasel and stoat. The density of these specialist predators declines drastically during the winter after the vole crash. We studied experimentally the impact of the perceived presence of stoats on the breeding and mating behaviour of voles. In a series of breeding experiments with bank voles,Clethrionomys glareolus, both old and young females suppressed breeding when exposed to the odour of stoats,Mustela erminea. The weights of females decreased in both experimental and control groups, but more among the voles under odour exposition. It seems that females actively avoided copulations under high predation risk and that breeding suppression is mediated by a change in female mating behaviour. There was no change in male behaviour or physical condition between the experimental and control treatments. An alternative mechanism for the observed breeding suppression could be the one caused by decreased feeding in females mediated with low energy intake which does not allow breeding. Regardless of its mechanism, delay of breeding should increase the probability of non-breeding females to survive to the next breeding season. The females surviving the crash should gain a strong selective advantage in a predator-free environment of the subsequent breeding season, which could explain the adaptive function of this antipredatory strategy.     

Landscape features and helminth co-infection shape bank vole immunoheterogeneity,with consequences for Puumala virus epidemiology

Heterogeneity in environmental conditions helps to maintain genetic and phenotypicdiversity in ecosystems. As such, it may explain why the capacity of animals to mountimmune responses is highly variable. The quality of habitat patches, in terms ofresources, parasitism, predation and habitat fragmentation may, for example, triggertrade-offs ultimately affecting the investment of individuals in various immunologicalpathways. We described spatial immunoheterogeneity in bank vole populations with respectto landscape features and co-infection. We focused on the consequences of thisheterogeneity for the risk of Puumala hantavirus (PUUV) infection. We assessed theexpression of the Tnf-α and Mx2 genes and demonstrated a negativecorrelation between PUUV load and the expression of these immune genes in bank voles.Habitat heterogeneity was partly associated with differences in the expression of thesegenes. Levels of Mx2 were lower in large forests than in fragmented forests,possibly due to differences in parasite communities. We previously highlighted thepositive association between infection with Heligmosomum mixtum and infectionwith PUUV. We found that Tnf-α was more strongly expressed in volesinfected with PUUV than in uninfected voles or in voles co-infected with thenematode H. mixtum and PUUV. H. mixtum may limit the capacity of thevole to develop proinflammatory responses. This effect may increase the risk of PUUVinfection and replication in host cells. Overall, our results suggest that closeinteractions between landscape features, co-infection and immune gene expression may shapePUUV epidemiology.     

Experience pays: offspring survival increases with female age

Life-history theory predicts that, in long-lived organisms, effort towards reproduction will increase with age, and research from oviparous vertebrates largely supports this prediction. In reptiles, where parental care occurs primarily via provisioning of the egg, older females tend to produce larger eggs, which in turn produce larger hatchlings that have increased survival. We conducted an experimental release study and report that maternal age positively influences offspring survivorship in the painted turtle (Chrysemys picta) and predicts offspring survival at least as well as hatchling body size does. These data suggest that, although increasing hatchling size is a major component of reproductive success in older individuals, other factors also contribute.     

Environmental transmission of a personality trait: foster parent exploration behaviour predicts offspring exploration behaviour in zebra finches

Consistent behavioural differences among individuals are common in many species and can have important effects on offspring fitness. To understand such ‘personality’ variation, it is important to determine the mode of inheritance, but this has been quantified for only a few species. Here, we report results from a breeding experiment in captive zebra finches, Taeniopygia guttata, in which we cross-fostered offspring to disentangle the importance of genetic and non-genetic transmission of behaviour. Genetic and foster-parents’ exploratory type was measured in a novel environment pre-breeding and offspring exploratory type was assessed at adulthood. Offspring exploratory type was predicted by the exploratory behaviour of the foster but not the genetic parents, whereas offspring size was predicted by genetic but not foster-parents’ size. Other aspects of the social environment, such as rearing regime (uni- versus biparental), hatching position, brood size or an individual''s sex did not influence offspring exploration. Our results therefore indicate that non-genetic transmission of behaviour can play an important role in shaping animal personality variation.     

Reproductive isolation in a nascent species pair is associated with aneuploidy in hybrid offspring

Speciation may occur when the genomes of two populations accumulate genetic incompatibilities and/or chromosomal rearrangements that prevent inter-breeding in nature. Chromosome stability is critical for survival and faithful transmission of the genome, and hybridization can compromise this. However, the role of chromosomal stability on hybrid incompatibilities has rarely been tested in recently diverged populations. Here, we test for chromosomal instability in hybrids between nascent species, the ‘dwarf’ and ‘normal’ lake whitefish (Coregonus clupeaformis). We examined chromosomes in pure embryos, and healthy and malformed backcross embryos. While pure individuals displayed chromosome numbers corresponding to the expected diploid number (2n = 80), healthy backcrosses showed evidence of mitotic instability through an increased variance of chromosome numbers within an individual. In malformed backcrosses, extensive aneuploidy corresponding to multiples of the haploid number (1n = 40, 2n = 80, 3n = 120) was found, suggesting meiotic breakdown in their F₁ parent. However, no detectable chromosome rearrangements between parental forms were identified. Genomic instability through aneuploidy thus appears to contribute to reproductive isolation between dwarf and normal lake whitefish, despite their very recent divergence (approx. 15–20 000 generations). Our data suggest that genetic incompatibilities may accumulate early during speciation and limit hybridization between nascent species.     

Different effects of paternal trans-generational immune priming on survival and immunity in step and genetic offspring

Paternal trans-generational immune priming, whereby fathers provide immune protection to offspring, has been demonstrated in the red flour beetle Tribolium castaneum exposed to the insect pathogen Bacillus thuringiensis. It is currently unclear how such protection is transferred, as in contrast to mothers, fathers do not directly provide offspring with a large amount of substances. In addition to sperm, male flour beetles transfer seminal fluids in a spermatophore to females during copulation. Depending on whether paternal trans-generational immune priming is mediated by sperm or seminal fluids, it is expected to either affect only the genetic offspring of a male, or also their step offspring that are sired by another male. We therefore conducted a double-mating experiment and found that only the genetic offspring of an immune primed male show enhanced survival upon bacterial challenge, while phenoloxidase activity, an important insect immune trait, and the expression of the immune receptor PGRP were increased in all offspring. This indicates that information leading to enhanced survival upon pathogen exposure is transferred via sperm, and thus potentially constitutes an epigenetic effect, whereas substances transferred with the seminal fluid could have an additional influence on offspring immune traits and immunological alertness.     

Aerial and soil seed banks enable populations of an annual species to cope with an unpredictable dune ecosystem

Background and Aims

Simultaneous formation of aerial and soil seed banks by a species provides a mechanism for population maintenance in unpredictable environments. Eolian activity greatly affects growth and regeneration of plants in a sand dune system, but we know little about the difference in the contributions of these two seed banks to population dynamics in sand dunes.

Methods

Seed release, germination, seedling emergence and survival of a desert annual, Agriophyllum squarrosum (Chenopodiaceae), inhabiting the Ordos Sandland in China, were determined in order to explore the different functions of the aerial and soil seed banks.

Key Results

The size of the aerial seed bank was higher than that of the soil seed bank throughout the growing season. Seed release was positively related to wind velocity. Compared with the soil seed bank, seed germination from the aerial seed bank was lower at low temperature (5/15 °C night/day) but higher in the light. Seedling emergence from the soil seed bank was earlier than that from the aerial seed bank. Early-emerged (15 April–15 May) seedlings died due to frost, but seedlings that emerged during the following months survived to reproduce successfully.

Conclusions

The timing of seed release and different germination behaviour resulted in a temporal heterogeneity of seedling emergence and establishment between the two seed banks. The study suggests that a bet-hedging strategy for the two seed banks enables A. squarrosum populations to cope successfully with the unpredictable desert environment.     

Introduced Siberian chipmunks are more heavily infested by ixodid ticks than are native bank voles in a suburban forest in France

By serving as hosts for native vectors, introduced species can surpass native hosts in their role as major reservoirs of local pathogens. During a 4-year longitudinal study, we investigated factors that affected infestation by ixodid ticks on both introduced Siberian chipmunks Tamias sibiricus barberi and native bank voles Myodes glareolus in a suburban forest (Forêt de Sénart, Ile-de-France). Ticks were counted on adult bank voles and on adult and young chipmunks using regular monthly trapping sessions, and questing ticks were quantified by dragging. At the summer peak of questing Ixodes ricinus availability, the average tick load was 27-69 times greater on adult chipmunks than on adult voles, while average biomass per hectare of chipmunks and voles were similar. In adult chipmunks, individual effects significantly explained 31% and 24% of the total variance of tick larvae and nymph burdens, respectively. Male adult chipmunks harboured significantly more larvae and nymphs than adult females, and than juveniles born in spring and in summer. The higher tick loads, and more specifically the ratio of nymphs over larvae, observed in chipmunks may be caused by a higher predisposition - both in terms of susceptibility and exposure - to questing ticks. Tick burdens were also related to habitat and seasonal variation in age- and sex-related space use by both rodents. Introduced chipmunks may thus have an important role in the dynamics of local vector-borne pathogens compared with native reservoir hosts such as bank voles.     

Regulation of vole populations by the nematode <Emphasis Type="Italic">Trichuris arvicolae</Emphasis>: insights from modelling

The goal of this study is to determine whether a parasitic nematode may regulate, or destabilise by inducing demographic cycles, its host populations. We explore three host–parasite systems through population dynamic models. The hosts considered are the fossorial water vole, Arvicola terrestris, the common vole Microtus arvalis and the bank vole Myodes (Clethrionomys) glareolus and the parasitic nematode is Trichuris arvicolae. Three differential equation-based mathematical models are developed including host immunity and the existence of trade-off between immunity and host survival. Using parameters estimated from field data and laboratory observations, all these models show that T. arvicolae can induce host population regulation but not demographic cycles. The regulation effect of the nematode is un-ambiguous for the water vole (reduction of 50.2% of the host population size), but less obvious for the common vole (5.9%) and even less for the bank vole (1.4%). Important biological parameters to be taken into account in such models are discussed. Experimental confirmation of the regulatory potential of the nematode and of the costs of mounting an immune response against this nematode are now required. Communicated by W. Lutz     

Polyandry in two South American harvester ants

Although monandry (single mating) is the ancestral state in social hymenopteran insects, effective mating frequencies greater than 2 have been confirmed for a fair amount of ant species: Cataglyphis cursor, the leaf-cutters of the genera Atta and Acromyrmex, army ants of the genera Eciton, Dorylus, Aenictus and Neivamyrmex, and some North American seed harvester species of the genus Pogonomyrmex. This last genus spreads throughout open arid habitats from Patagonia to southwestern Canada. Whereas some North American Pogonomyrmex species are thoroughly studied, we know much less about these ants in South America. The objective of this study was to estimate the effective mating frequency of Pogonomyrmex inermis and P. pronotalis, two Pogonomyrmex sensu stricto species from the central Monte desert of Argentina. A total of 477 P. pronotalis workers from 24 colonies and 402 P. inermis workers from 20 colonies were analyzed using six and four highly polymorphic microsatellites, respectively. The multilocus analysis revealed that all colonies were monogynous and all queens multiply-mated. The effective mating frequency was 8.75 and 6.52 for queens of P. pronotalis and P. inermis, respectively; those values increased up to 15.66 and 9.78, respectively, when corrected for sampling errors. This is the first demonstration that queens in at least some members of the South American Pogonomyrmex sensu stricto are strictly polyandrous, with mating numbers per queen at least as high as those previously found for North American species. We suggest that multiple mating probably arose early in the evolution of the genus Pogonomyrmex and may be the basis of its ecological success and wide distribution. Received 11 October 2006; revised 10 August 2007 and 19 November 2007; accepted 21 November 2007.     

Genetic structure, habitat fragmentation and bottlenecks in Danish bank voles (Clethrionomys glareolus)

Tissue-samples from 161 bank voles (Clethrionomys glareolus) collected in three forests (five sampling localities) situated in eastern Jutland (Denmark) were analysed by nine microsatellite loci. The genetic diversity found within the populations was high (H_e=0.753–0.806).Bank voles have specific habitat requirements favouring woodlots, hedgerows and deciduous forests as their prime living area. Hence, a natural or human-induced fragmentation of the forest may cause a sub-structuring of the populations and thereby a restriction of dispersal among populations. The sub-structuring indicated by the observed significant genetic differentiation among the five geographically distinct localities (F_st =0.033, P<0.05) could either result from habitat fragmentation or a combination of home range behaviour and different tree composition in the forests. A road situated between two adjacent forests was not found to exert any barrier effect to the gene flow of bank voles. In one out of five localities investigated, genetic evidence for a recent bottleneck-like situation was found. Bank voles are known to exhibit sometimes huge density fluctuations not only from year to year but also from season to season. The bottleneck-like situation found could therefore be due to the low number of individuals during the low-density phase.     

Anti-pathogen protection versus survival costs mediated by an ectosymbiont in an ant host

The fitness effects of symbionts on their hosts can be context-dependent, with usually benign symbionts causing detrimental effects when their hosts are stressed, or typically parasitic symbionts providing protection towards their hosts (e.g. against pathogen infection). Here, we studied the novel association between the invasive garden ant Lasius neglectus and its fungal ectosymbiont Laboulbenia formicarum for potential costs and benefits. We tested ants with different Laboulbenia levels for their survival and immunity under resource limitation and exposure to the obligate killing entomopathogen Metarhizium brunneum. While survival of L. neglectus workers under starvation was significantly decreased with increasing Laboulbenia levels, host survival under Metarhizium exposure increased with higher levels of the ectosymbiont, suggesting a symbiont-mediated anti-pathogen protection, which seems to be driven mechanistically by both improved sanitary behaviours and an upregulated immune system. Ants with high Laboulbenia levels showed significantly longer self-grooming and elevated expression of immune genes relevant for wound repair and antifungal responses (β-1,3-glucan binding protein, Prophenoloxidase), compared with ants carrying low Laboulbenia levels. This suggests that the ectosymbiont Laboulbenia formicarum weakens its ant host by either direct resource exploitation or the costs of an upregulated behavioural and immunological response, which, however, provides a prophylactic protection upon later exposure to pathogens.