Reducing Mortality of Shrews in Rodent Live Trapping — a Method Increasing Live-Trap Selectivity with Shrew Exits
Shrews have very high metabolic rates and are often unintentionally starved in rodent live-traps during capture-mark-recapture (CMR) studies. Here, we suggest a shrew exit as a modification to rodent traps. To test whether this modification is (1) saving shrews and (2) not jeopardizing results of rodent captures, we compared captures in Ugglan traps with and without shrew exits, studying bank voles (Myodes glareolus) in a spruce forest in central Finland. Numbers of captured bank voles and body size of smallest juvenile bank voles were not affected by the shrew exit, while the number of captured common shrews (Sorex araneus) was reduced from 31 to 0 individuals per 100 trap nights. However,…
Polyandrous females produce sons that are successful at post-copulatory competition.
Some of the genetic benefit hypotheses put forward to explain multiple male mating (polyandry) predict that sons of polyandrous females will have an increased competitive ability under precopulatory or post-copulatory competition via paternally inherited traits, such as attractiveness or fertilization efficiency. Here, we tested these predictions by comparing the competitive ability of sons of experimentally monandrous and polyandrous female bank voles (Myodes glareolus), while controlling for potential material and maternal effects. In female choice experiments, we found no clear preference for sons of either monandrous or polyandrous mothers. Moreover, neither male type was dominant over …
Experience and dominance in fish pairs jointly shape parasite avoidance behaviour
There is increasing evidence that the composition of a social group influences the fitness of its members. For example, group member identities can determine the exposure risk to contact-transmitted parasites and consequently impact the health of all group members. Here, we propose that group composition may also affect host exposure to parasite propagules prevailing in the environment via collective parasite avoidance behaviours. We explored the spatial avoidance of a trematode parasite, Diplostomum pseudospathaceum, using the simplest form of host groups, pairs of sea trout, Salmo trutta trutta. These pairs showed either (1) between-group heterogeneity in their experience with the parasit…
Relatedness Does not Affect Competitive Behavior of Rival Males or Offspring Growth in Multiply Sired Litters of Bank Voles (Myodes glareolus)
Kin selection operates through the fitness of an organism's relatives. In the polyandry context, kin selection may be observable on the one hand in competition between rival males and, on the other hand, in competition between litter mates. Sperm competition theory predicts that males should invest less into mating when competing for fertilizations against a close relative as compared to an unrelated male. We tested this hypothesis with bank voles (Myodes glareolus) by mating each focal male to two females: one of which had previously mated with a full sibling of the focal male and the other one with a male unrelated to the focal male. However, we found no effect of rival male relatedness o…
Within‐host interactions shape virulence‐related traits of trematode genotypes
Within-host interactions between co-infecting parasites can significantly influence the evolution of key parasite traits, such as virulence (pathogenicity of infection). The type of interaction is expected to predict the direction of selection, with antagonistic interactions favouring more virulent genotypes and synergistic interactions less virulent genotypes. Recently, it has been suggested that virulence can further be affected by the genetic identity of co-infecting partners (G × G interactions), complicating predictions on disease dynamics. Here, we used a natural host-parasite system including a fish host and a trematode parasite to study the effects of G × G interactions on infection…
Host infection history modifies co-infection success of multiple parasite genotypes.
Co-infections by multiple parasite genotypes are common and have important implications for host-parasite ecology and evolution through within-host interactions. Typically, these infections take place sequentially, and therefore, the outcome of co-infection may be shaped by host immune responses triggered by previous infections. For example, in vertebrates, specific immune responses play a central role in protection against disease over the course of life, but co-infection research has mostly focused on previously uninfected individuals. Here, we investigated whether sequential exposure and activation of host resistance in rainbow trout Oncorhynchus mykiss affects infection success and inte…
Life-history genotype explains variation in migration activity in Atlantic salmon (Salmo salar)
AbstractOne of the most important life-history continuums is the fast–slow axis, where “fast” individuals mature earlier than “slow” individuals. “Fast” individuals are predicted to be more active than “slow” individuals; high activity is required to maintain a fast life-history strategy. Recent meta-analyses revealed mixed evidence for such integration. Here, we test whether known life-history genotypes differ in activity expression by using Atlantic salmon (Salmo salar) as a model. In salmon, variation in Vgll3, a transcription co-factor, explains ∼40% of variation in maturation timing. We predicted that the allele related to early maturation (vgll3*E) would be associated with increased a…
Opposing health effects of hybridization for conservation
The continuing decline of many natural plant and animal populations emphasizes the importance of conservation strategies. Hybridization as a management tool has proven successful in introducing gene flow to small, inbred populations, but can be also associated with health risks. For example, hybridization can change susceptibility to infection in either direction due to heterosis (hybrid vigor) and outbreeding depression, but such health effects have rarely been considered in the genetic management of populations. Here, we investigated the effects of experimental outcrossing between the critically endangered Saimaa landlocked salmon (Salmo salar m. sebago) and the genetically more diverse A…
Vertebrate defense against parasites: Interactions between avoidance, resistance, and tolerance
Hosts can utilize different types of defense against the effects of parasitism, including avoidance, resistance, and tolerance. Typically, there is tremendous heterogeneity among hosts in these defense mechanisms that may be rooted in the costs associated with defense and lead to trade‐offs with other life‐history traits. Trade‐offs may also exist between the defense mechanisms, but the relationships between avoidance, resistance, and tolerance have rarely been studied. Here, we assessed these three defense traits under common garden conditions in a natural host–parasite system, the trematode eye‐fluke Diplostomum pseudospathaceum and its second intermediate fish host. We looked at host ind…
Infanticide and Population Growth in the Bank Vole (Myodes glareolus): The Effect of Male Turnover and Density
One major intrinsic factor affecting recruitment of young into a population is infanticide, the killing of conspecific young by adult males. It occurs in most mammal species, like our study species the bank vole (Myodes glareolus), and is widely accepted as an adaptive behavior, which may increase male fitness via nutritional gain, decreased competition, or an increased access to mates. A turnover of males in a population increases the risk of infanticide owing to a disruption of social structures. In a controlled field study, we tested the effects of total male turnover and density on juvenile recruitment and female space use in experimental bank vole populations. Juvenile recruitment decl…
Male house mice that have evolved with sperm competition have increased mating duration and paternity success
Sperm competition imposes strong selection on males to gain fertilizations and maximize paternity. Males have been shown to adapt to sperm competition by modifying their behaviour and/or reproductive physiology. We investigated the fitness effects of male responses to sperm competition in house mice, Mus domesticus. Males that had been evolving with (polygamy) and without (monogamy) sperm competition for 18 generations were subject to different frequencies of social encounters with conspecific males to generate a sperm competition ‘risk’ treatment and a ‘no risk’ treatment. After manipulation of their social environment for 15–22 days, males were forced to compete for fertilizations against…
Within-host interactions shape virulence-related traits of trematode genotypes
Within‐host interactions between co‐infecting parasites can significantly influence the evolution of key parasite traits, such as virulence (pathogenicity of infection). The type of interaction is expected to predict the direction of selection, with antagonistic interactions favouring more virulent genotypes and synergistic interactions less virulent genotypes. Recently, it has been suggested that virulence can further be affected by the genetic identity of co‐infecting partners (G × G interactions), complicating predictions on disease dynamics. Here, we used a natural host–parasite system including a fish host and a trematode parasite to study the effects of G × G interactions on infection…
Shoaling with infected conspecifics does not improve resistance to trematode infection
Group‐living animals can gain protection against parasitic infections through social contacts with previously infected conspecifics (social immunization). Recent research suggests that such protective effects can be induced through visual or chemical cues released by infected individuals, resulting in anticipatory immune upregulation among group members. Here, we study cue‐induced social resistance in rainbow trout Oncorhynchus mykiss exposed to a trematode parasite, the eye‐fluke Diplostomum pseudospathaceum. We established groups of naïve individuals (receivers) that were paired with previously infected individuals (donors) at different ratios of donors to receivers and at different time …
Supplementary tables and figures from Negative associations between parasite avoidance, resistance and tolerance predict host health in salmonid fish populations
Genetic variation in defence against parasite infections is fundamental for host–parasite evolution. The overall level of defence of a host individual or population includes mechanisms that reduce parasite exposure (avoidance), establishment (resistance) or pathogenicity (tolerance). However, how these traits operate and evolve in concert is not well understood. Here, we investigated genetic variation in and associations between avoidance, resistance and tolerance in a natural host–parasite system. Replicated populations of Atlantic salmon (Salmo salar) and sea trout (an anadromous form of brown trout, Salmo trutta) were raised under common garden conditions and infected with the eye fluke …
Variable mode of estrus affects female decision for multiple mating
Investigating patterns of variation in mating strategies may shed light on their evolutionary importance as well as their impact on the strength and shape of sexual selection. Multimale mating (polyandry) and mate choice are intensely studied subjects in the area of sexual selection, but little is known about intraspecific patterns of variation that may respond to dynamic cost-benefit balances. In a laboratory study, we investigated the mating behavior of female bank voles (Myodes glareolus) with distinctly different time and energy budgets: They were either in cycling estrus (CE) or postpartum estrus (PPE) shortly after delivery. Postpartum mating is highly constrained by time and energy d…
Quantity and Quality of Aquaculture Enrichments Influence Disease Epidemics and Provide Ecological Alternatives to Antibiotics
Environmental heterogeneity is a central component influencing the virulence and epidemiology of infectious diseases. The number and distribution of susceptible hosts determines disease transmission opportunities, shifting the epidemiological threshold between the spread and fadeout of a disease. Similarly, the presence and diversity of other hosts, pathogens and environmental microbes, may inhibit or accelerate an epidemic. This has important applied implications in farming environments, where high numbers of susceptible hosts are maintained in conditions of minimal environmental heterogeneity. We investigated how the quantity and quality of aquaculture enrichments (few vs. many stones
Population sex-ratio affecting behavior and physiology of overwintering bank voles (Myodes glareolus)
Many boreal rodents are territorial during the breeding season but during winter become social and aggregate for more energy efficient thermoregulation. Communal winter nesting and social interactions are considered to play an important role for the winter survival of these species, yet the topic is relatively little explored. Females are suggested to be the initiators of winter aggregations and sometimes reported to survive better than males. This could be due to the higher social tolerance observed in overwintering females than males. Hormonal status could also affect winter behavior and survival. For instance, chronic stress can have a negative effect on survival, whereas high gonadal ho…
Is reproduction really costly? Energy metabolism of bank vole (Clethrionomys glareolus) females through the reproductive cycle
Energetic requirements during reproduction are important determinants of the onset of reproduction and of breeding strategy (e.g., breeding post-partum) and therefore affect female reproductive output in seasonally varying environments. To balance the energetic needs of breeding with energy availability, females must optimize energy allocation between their own energy use and energy allocated to their litter. Here, we studied energetic costs and potential energetic trade-offs of reproduction in female bank voles (Clethrionomys glareolus). We measured energy consumption, i.e., metabolic rates as determined from carbon dioxide production of females either with their pups (breeding unit) to fi…
Variation in predation risk and vole feeding behaviour: a field test of the risk allocation hypothesis.
Many prey animals experience temporal variation in the risk of predation and therefore face the problem of allocating their time between antipredator efforts and other activities like feeding and breeding. We investigated time allocation of prey animals that balanced predation risk and feeding opportunities. The predation risk allocation hypothesis predicts that animals should forage more in low- than in high-risk situations and that this difference should increase with an increasing attack ratio (i.e. difference between low- and high-risk situations) and proportion of time spent at high risk. To test these predictions we conducted a field test using bank voles ( Clethrionomys glareolus) as…
Polyandry enhances offspring survival in an infanticidal species
The adaptive significance of polyandry is an intensely debated subject in sexual selection. For species with male infanticidal behaviour, it has been hypothesized that polyandry evolved as female counterstrategy to offspring loss: by mating with multiple males, females may conceal paternity and so prevent males from killing putative offspring. Here we present, to our knowledge, the first empirical test of this hypothesis in a combined laboratory and field study, and show that multiple mating seems to reduce the risk of infanticide in female bank voles Myodes glareolus . Our findings thus indicate that females of species with non-resource based mating systems, in which males provide nothing…
Why do female bank voles, Clethrionomys glareolus, mate multiply?
Females of many species actively engage in multiple mating, with either a single male or several males, but the adaptive function of this behaviour is often unclear. We conducted a laboratory experiment on a small mammal species, the bank vole, testing the possible benefits of multiple mating on a female's short-term reproductive success (pregnancy rate, litter size and early postnatal survival). Such benefits may affect a female's fitness either directly or indirectly (genetic benefit). We assigned females to three treatments: a single mating treatment in which females mated once with a single male and two multiple mating treatments in which females mated either twice with a single male or…
Sex-specific variation in the onset of reproduction and reproductive trade-offs in a boreal small mammal
In seasonal environments, the optimal onset of reproduction plays a major role in defining the reproductive success of an individual. Environmental cues, like day length, weather conditions, and food, regulate the initiation and termination of the breeding season. Besides the interspecific variation in response to environmental cues, it has been suggested that due to different selection pressures, females and males can have different responses to environmental stimuli. However, this phenomenon has gained relatively little consideration, and the physiological mechanism behind these differences is not well known. Here, we report how two different environmental cues, variability of temperature…
Cold water reduces the severity of parasite-inflicted damage : support for wintertime recuperation in aquatic hosts
The reduction in host fitness caused by parasite infections (virulence) depends on infection intensity and the degree of damage caused per parasite. Environmental conditions can shape both virulence components, but in contrast to infection intensity, environmental impacts on per-parasite damage are poorly understood. Here, we studied the effect of ambient temperature on per-parasite damage, which is jointly determined by the ability of parasites to induce harm (per-parasite pathogenicity) and the ability of hosts to limit damage (tolerance). We experimentally exposed two salmonid species, Atlantic salmon (Salmo salar) and sea trout (Salmo trutta), to replicated genotypes of the eye fluke Di…
Negative associations between parasite avoidance, resistance and tolerance predict host health in salmonid fish populations
Genetic variation in defence against parasite infections is fundamental for host–parasite evolution. The overall level of defence of a host individual or population includes mechanisms that reduce parasite exposure (avoidance), establishment (resistance) or pathogenicity (tolerance). However, how these traits operate and evolve in concert is not well understood. Here, we investigated genetic variation in and associations between avoidance, resistance and tolerance in a natural host–parasite system. Replicated populations of Atlantic salmon ( Salmo salar ) and sea trout (an anadromous form of brown trout, Salmo trutta ) were raised under common garden conditions and infected with the eye fl…
Host Developmental Stage Effects on Parasite Resistance and Tolerance.
Hosts can defend themselves against parasites either by preventing or limiting infections (resistance) or by limiting parasite-induced damage (tolerance). However, it remains underexplored how these defense types vary over host development with shifting patterns of resource allocation priorities. Here, we studied the role played by developmental stage in resistance and tolerance in Atlantic salmon (Salmo salar). This anadromous fish has distinct life stages related to living in freshwater and seawater. We experimentally exposed 1-year-old salmon, either at the freshwater stage or at the stage transitioning to the marine phase, to the trematode Diplostomum pseudospathaceum. Using 56 pedigree…
Parasite infection in a central sensory organ of fish does not affect host personality
Among the ecological factors acting on the evolution and expression of animal personalities and behavioral syndromes, parasitism has received comparatively little attention. However, infection and host behavior are often strongly intertwined, because host behavior can predict the risk of infection and can also be changed by an infection. We conducted a controlled experimental infection study to explore the effects of infection on host boldness, exploration and activity using rainbow trout Oncorhynchus mykiss and its trematode parasite Diplostomum pseudospathaceum, which infects a central sensory organ of the fish, the eye lens. Contrary to our expectation, infection did not change the withi…
Polyandry and its effect on male and female fitness
Miksi metsämyyränaaraalla on useampia rakastajia, on mielenkiintoinen kysymys evoluutioekologiassa. Yksi koiras riittäisi hyvin hedelmöittämään kaikki naaraan munasolut, ja useamman koiraan kanssa jatkuvat lemmenleikit altistavat naaraan niin pedon hampaille kuin tautiriskille. Useamman koiraan kanssa parittelu näyttää kuitenkin olevan enemmän sääntö kuin poikkeus.Ines Klemmen väitöskirjatutkimuksen aiheena oli selvittää, mitä hyötyä naaraalle on useamman koiraan kanssa parittelusta. Klemme osoitti tutkimuksessaan, että mitä useamman koiraan kanssa metsämyyränaaras parittelee yhden lisääntymiskerran aikana, sitä parempi on sen lisääntymistulos. Metsämyyrän poikuekoko on 5-6, ja naaras saatt…
Changing winter conditions in the boreal forest : the effects of fluctuating temperature and predation risk on activity and physiological stress level in bank voles
Due to global climate change, the winter conditions in the North are predicted to change, as the time with an intact insulating snow cover gets shorter or disappears altogether. For small mammals, this could cause exposure to strong temperature fluctuations and increased predation risk, inducing severe stress and leading to alterations in the physical condition and behavior. To test this, we exposed bank voles (Myodes glareolus) to different temperature regimes and cues of predator threat under laboratory conditions. The test animals experienced either a stable but cool temperature regime resembling the stable conditions under snow cover, or an unstable temperature regime with cold nights a…
Supplementary tables and figures from Negative associations between parasite avoidance, resistance and tolerance predict host health in salmonid fish populations
Genetic variation in defence against parasite infections is fundamental for host–parasite evolution. The overall level of defence of a host individual or population includes mechanisms that reduce parasite exposure (avoidance), establishment (resistance) or pathogenicity (tolerance). However, how these traits operate and evolve in concert is not well understood. Here, we investigated genetic variation in and associations between avoidance, resistance and tolerance in a natural host–parasite system. Replicated populations of Atlantic salmon (Salmo salar) and sea trout (an anadromous form of brown trout, Salmo trutta) were raised under common garden conditions and infected with the eye fluke …
Learned parasite avoidance is driven by host personality and resistance to infection in a fish-trematode interaction
Cognitive abilities related to the assessment of risk improve survival. While earlier studies have examined the ability of animals to learn to avoid predators, learned parasite avoidance has received little interest. In a series of behavioural trials with the trematode parasite Diplostomum pseudospathaceum , we asked whether sea trout ( Salmo trutta trutta ) hosts show associative learning in the context of parasitism and if so, whether learning capacity is related to the likelihood of infection mediated through host personality and resistance. We show that animals are capable of learning to avoid visual cues associated with the presence of parasites. However, avoidance behaviour ceased af…
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 volesClethrionomys 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 o…
Supplementary figures
Supplementary figures S1-S3.
Strategic adjustments in sperm production within and between two island populations of house mice
Sperm production is physiologically costly. Consequently, males are expected to be prudent in their sperm production, and tailor their expenditure according to prevailing social conditions. Differences in sperm production have been found across island populations of house mice that differ in the level of selection from sperm competition. Here, we determined the extent to which these differences represent phenotypic plasticity and/or population divergence in sperm production. We sourced individuals from two populations at the extreme levels of sperm competition, and raised them under common-garden conditions while manipulating the social experience of developing males. Males from the high-sp…
Data from: Parasite infection in a central sensory organ of fish does not affect host personality
Among the ecological factors acting on the evolution and expression of animal personalities and behavioral syndromes, parasitism has received comparatively little attention. However, infection and host behavior are often strongly intertwined, because host behavior can predict the risk of infection and can also be changed by an infection. We conducted a controlled experimental infection study to explore the effects of infection on host boldness, exploration and activity using rainbow trout Oncorhynchus mykiss and its trematode parasite Diplostomum pseudospathaceum, which infects a central sensory organ of the fish, the eye lens. Contrary to our expectation, infection did not change the withi…
Data from: Strategic adjustments in sperm production within and between two island populations of house mice
Sperm production is physiologically costly. Consequently, males are expected to be prudent in their sperm production, and tailor their expenditure according to prevailing social conditions. Differences in sperm production have been found across island populations of house mice that differ in the level of selection from sperm competition. Here, we determined the extent to which these differences represent phenotypic plasticity and/or population divergence in sperm production. We sourced individuals from two populations at the extreme levels of sperm competition, and raised them under common-garden conditions while manipulating the social experience of developing males. Males from the high-sp…
Data from: Learned parasite avoidance is driven by host personality and resistance to infection in a fish–trematode interaction
Cognitive abilities related to the assessment of risk improve survival. While earlier studies have examined the ability of animals to learn to avoid predators, learned parasite avoidance has received little interest. In a series of behavioural trials with the trematode parasite Diplostomum pseudospathaceum, we asked whether sea trout (Salmo trutta trutta) hosts show associative learning in the context of parasitism and if so, whether learning capacity is related to the likelihood of infection mediated through host personality and resistance. We show that animals are capable of learning to avoid visual cues associated with the presence of parasites. However, avoidance behaviour ceased after …
Data from: Host infection history modifies co-infection success of multiple parasite genotypes
1. Co-infections by multiple parasite genotypes are common and have important implications for host-parasite ecology and evolution through within-host interactions. Typically, these infections take place sequentially and therefore, the outcome of co-infection may be shaped by host immune responses triggered by previous infections. For example, in vertebrates specific immune responses play a central role in protection against disease over the course of life, but co-infection research has mostly focused on previously uninfected individuals. 2. Here, we investigated whether sequential exposure and activation of host resistance in rainbow trout Oncorhynchus mykiss affects infection success and …
Original data for manuscript: Quantity and Quality of Aquaculture Enrichments Influence Disease Epidemics and Provide Ecological Alternatives to Antibiotics
The data processed and analyzed in this study are given in a single file: Karvonen et al. exposure data.xlsx. For detailed description of the material, methods and results of the study, see the article.