Maternally-inherited sex ratio distorting microbes (SRDMs) are common among arthropod species. Typically, these microbes cause female-biased sex ratios in host broods, either by; killing male offspring, feminising male offspring, or inducing parthenogenesis. As a result, infected populations can experience drastic ecological and evolutionary change. The mechanism by which SRDMs operate is likely to alter their impact on host evolutionary ecology; despite this, the current literature is heavily biased towards a single mechanism of sex ratio distortion, male-killing. Furthermore, amidst the growing concerns surrounding the loss of arthropod diversity, research into the impact of SRDMs on the viability of arthropod populations is generally lacking. In this study, using a theoretical approach, we model the epidemiology of an understudied mechanism of microbially-induced sex ratio distortion-feminisation-to ask an understudied question-how do SRDMs impact extinction risk in a changing environment? We constructed an individual-based model and measured host population extinction risk under various environmental and epidemiological scenarios. We also used our model to identify the precise mechanism modulating extinction. We find that the presence of feminisers increases host population extinction risk, an effect that is exacerbated in highly variable environments. We also identified transmission rate as the dominant epidemiological trait responsible for driving extinction. Finally, our model shows that sex ratio skew is the mechanism driving extinction. We highlight feminisers and, more broadly, SRDMs as important determinants of the resilience of arthropod populations to environmental change.
Functional redundancy, the potential for the functional role of one species to be fulfilled by another, is a key determinant of ecosystem viability. Scavenging transfers huge amount of energy through ecosystems and is, therefore, crucial for ecosystem viability and healthy ecosystem functioning. Despite this, relatively few studies have examined functional redundancy in scavenger communities. Moreover, the results of these studies are mixed and confined to a very limited range of habitat types and taxonomic groups. This study attempts to address this knowledge gap by conducting a field experiment in an undisturbed natural environment assessing functional roles and redundancy in vertebrate and invertebrate scavenging communities in a South African savanna. We used a large-scale field experiment to suppress ants in four 1 ha plots in a South African savanna and paired each with a control plot. We distributed three types of small food bait: carbohydrate, protein and seed, across the plots and excluded vertebrates from half the baits using cages. Using this combination of ant suppression and vertebrate exclusion, allowed us explore the contribution of non-ant invertebrates, ants and vertebrates in scavenging and also to determine whether either ants or vertebrates were able to compensate for the loss of one another. In this study, we found the invertebrate community carried out a larger proportion of overall scavenging services than vertebrates. Moreover, although scavenging was reduced when either invertebrates or vertebrates were absent, the presence of invertebrates better mitigated the functional loss of vertebrates than did the presence of vertebrates against the functional loss of invertebrates. There is a commonly held assumption that the functional role of vertebrate scavengers exceeds that of invertebrate scavengers; our results suggest that this is not true for small scavenging resources. Our study highlights the importance of invertebrates for securing healthy ecosystem functioning both now and into the future. We also build upon many previous studies which show that ants can have particularly large effects on ecosystem functioning. Importantly, our study suggests that scavenging in some ecosystems may be partly resilient to changes in the scavenging community, due to the potential for functional compensation by vertebrates and ants. This is a large-scale, factorial study which is the first of its kind to demonstrate the capacity for functional compensation amongst scavenger guilds in African savannas. We suggest that scavenging in some ecosystems may be partially resilient to changes in scavenging communities, due to functional compensation by vertebrates and ants.image
ABSTRACTWe are still largely reliant on pesticides for the suppression of arthropod pests which threaten human health and food production, but the recent rise of evolved resistance among important pest species has reduced pesticide efficacy. Despite this, our understanding of strategies that effectively limit the evolution of resistance remains weak. Male‐killing sex ratio distorting microbes (SRDMs), such as Wolbachia and Spiroplasma, are common among arthropod species. Previous theoretical work has suggested that they could limit adaptive potential in two ways: first, because by distorting sex ratios they reduce the effective population size, and second, because infected females produce no male offspring which restricts gene flow. Here we present the results of a novel experiment in which we test the extent by which these two mechanisms limit the adaptive response of arthropods to pesticide. Using a fully factorial design, we manipulated the adult sex ratio of laboratory populations of Drosophila melanogaster, both in the presence and absence of SRDMs, and exposed these populations to six generations of pesticide poisoning. This design allows the effects of SRDMs on sex ratio and their effects on gene flow to be estimated separately. After six generations, individuals from populations with even sex ratios displayed a higher resistance to pesticide relative to individuals from female‐biased populations. By contrast, we found no effect of the presence of SRDMs in host populations on pesticide resistance independent of sex ratio. In addition, males were more susceptible to pesticide than females—this was true of flies from both naïve and previously exposed populations. These findings provide the first empirical proof of concept that sex ratio distortion arising from SRDMs can limit adaptation to pesticides, but cast doubt on the theoretical effect of male‐killers limiting adaptation by disrupting gene flow.
Wild animals are naturally infected with a range of viruses, some of which may be zoonotic. During the human COVID pandemic there was also the possibility of rodents acquiring SARS-CoV-2 from people, so-called reverse zoonoses. To investigate this, we sampled rats (Rattus norvegicus) and mice (Apodemus sylvaticus) from urban environments in 2020 during the human COVID-19 pandemic. We metagenomically sequenced lung and gut tissue and faeces for viruses, PCR screened for SARS-CoV-2, and serologically surveyed for anti-SARS-CoV-2 Spike antibodies. We describe the range of viruses that we found in these two rodent species. We found no molecular evidence of SARS-CoV-2 infection, though in rats we found lung antibody responses and evidence of neutralization ability that are consistent with rats being exposed to SARS-CoV-2 and/or exposed to other viruses that result in cross-reactive antibodies.
Datasets and R scripts for the above article.
Many arthropod species are vulnerable to infection by bacteria that kill the male offspring of their female hosts. These male‐killing bacteria (MKB) can greatly impact the ecology and evolution of their hosts, particularly when MKB prevalence is high and persistent through time. However, we still do not have a holistic understanding of the key determinants of MKB ecological epidemiology, particularly regarding the interplay between host‐MKB traits and environmental conditions. Here, we derived a mathematical model to analyse the role that several intrinsic and extrinsic factors play in determining MKB epidemiology, and how these factors interact with one another. We found that the invasion threshold and prevalence of MKB is determined by transmission rate and the rate at which female hosts recover from MKB infections. The invasion and prevalence of MKB is also highly sensitive to the extent that MKB can reduce intra‐brood competition by killing male offspring. Environmentally‐induced periodic changes to the epidemiological characteristics of MKB caused a sharp decline and a slow recovery of MKB prevalence and, in some cases, environmental disturbance can drive MKB extinct. Furthermore, the magnitude of the impact that environmental disturbance had on the dynamics of MKB prevalence was heavily modulated by intrinsic factors, particularly intra‐brood competition. This is the first study to explore how both intrinsic and extrinsic factors interact to influence the dynamics of MKB infections over large timescales; our findings are central to predicting the current and future impacts of MKB on host populations.
1. Cannibalism is taxonomically widespread and can have large impacts on individual fitness and population-level processes. As such, identifying how cannibalism rates vary in response to ecological cues is important for predicting species evolution and population dynamics. 2. In this study, we aimed to identify several eco-evolutionary factors that affect cannibalism rate and measure how they interacted with one another. 3. To do this, we conducted two experiments using complimentary methods to measure how cannibalism rates varied among larval Drosophila melanogaster and Drosophila simulans in response to changes in conspecific relatedness, social familiarity and density. 4. We found that larvae were more likely to cannibalise non-related larval victims in both species, and that this effect increased at high densities in D. simulans. We found no evidence that Drosophila larvae use social familiarity to assess relatedness. Finally, in D. melanogaster, cannibalistic larvae prefer to cannibalise larvae that are being attacked by a greater number of conspecifics, implying that cues linked to conspecific abundance encourage cooperative cannibalism. 5. By showing that cannibalism frequency in Drosophila spp. is sensitive to relatedness and several other factors, we reveal the complex relationship between cannibalism frequency and species ecology. Also, by showing that the effect of relatedness on cannibalism frequency is density dependent, we advance the current understanding of how ecological variables interact to affect kin selection. A free Plain Language Summary can be found within the Supporting Information of this article.
Dietary niche is fundamental for determining species ecology; thus, a detailed understanding of what drives variation in dietary niche is vital for predicting ecological shifts and could have implications for species management. Gut microbiota can be important for determining an organism’s dietary preference, and therefore which food resources they are likely to exploit. Evidence for whether the composition of the gut microbiota is plastic in response to changes in diet is mixed. Also, the extent to which dietary preference can be changed following colonisation by new gut microbiota from different species is unknown. Here, we use Drosophila spp. to show that: (1) the composition of an individual’s gut microbiota can change in response to dietary changes, and (2) ingestion of foreign gut microbes can cause individuals to be attracted to food types they previously had a strong aversion to. Thus, we expose a mechanism for facilitating rapid shifts in dietary niche over short evolutionary timescales.
Understanding the evolution of pathogen niche width is important for predicting disease spread and the probability that pathogens can emerge in novel hosts. Findings from previous theoretical studies often suggest that pathogens will evolve to be specialists in specific host environments. However, several of these studies make unrealistic assumptions regarding demographic stochasticity and the ability of pathogens to select their hosts. Here, an individual-based model was used to predict how population size, virulence and pathogen mutation rate affects the evolution niche specialism in pathogens. Pathogen specialism evolved regardless of virulence or populations size; thus, the findings of this study are somewhat consistent with those of previous work. However, because specialist pathogens had only a weak selective advantage over generalist pathogens, high mutation rates caused random trait variation to accumulate, preventing the evolution of specialism. Mutation rate varies greatly across different species and strains of pathogen. By showing that high mutation rates may prevent pathogen specialism evolving, this study highlights an intrinsic pathogen trait that may influence the evolution of pathogen niche width.
Allee effects occur when individual or population survival decreases due to populations being small or sparse. A key mechanism underlying Allee effects is difficulty in finding mates at low densities. Species may be particularly vulnerable to mate-finding Allee effects if females rely on an abundance of males to reproduce successfully. In sexually cannibalistic species, females may consume males before or after copulation, potentially reducing the supply of males to the point where a mate-finding Allee effect occurs. In this study, we investigate the extent to which sexual cannibalism can modulate mate-finding Allee effects, and the conditions under which sexual cannibalism is likely to be particularly detrimental to population viability. We created an individual-based model that tracked specific females throughout the breeding season and used extinction risk and per capita growth rate to measure the strength of the Allee effects. We varied both founder population size and mate encounter rate independently of each other to expose the mechanism driving the Allee effects. We also analysed how cannibalism-derived female fecundity benefits affected extinction risk. We found that sexual cannibalism could lead to high extinction risk, particularly when cannibalism occurred before copulation, founder population size was small and mate encounter rates were low. However, post-copulatory cannibalism reduced extinction risk, if cannibalism increased female fecundity enough. We found that there were strong threshold effects, in which small changes in encounter rate could strongly alter population extinction risk. We find that sexual cannibalism is likely to negatively impact population survival as population size and mate encounter rate decrease. This may be exacerbated if male quality declines and female hunger increases in declining populations. As many top invertebrate predators, such as spiders and mantises, are sexually cannibalistic, this may have ecosystem-wide impacts. We also suggest that other reproductive behaviours, such as rejecting all but high-quality mates or requiring multiple mates to ensure fertility, are also likely to cause mate-finding Allee effects when habitat quality degrades.
We currently face significant, anthropogenic, global environmental challenges and the role of ecologists in mitigating these challenges is arguably more important than ever. Consequently there is an urgent need to recruit and train future generations of ecologists, both those whose main area is ecology, but also those involved in the geological, biological and environmental sciences.Here we present the results of a horizon scanning exercise that identified current and future challenges facing the teaching of ecology, through surveys of teachers, students and employers of ecologists. Key challenges identified were grouped in terms of the perspectives of three groups: students, for example the increasing disconnect between people and nature; teachers, for example the challenges associated with teaching the quantitative skills that are inherent to the study of ecology; and society, for example poor societal perceptions of the field of ecology.In addition to the challenges identified, we propose a number of solutions developed at a workshop by a team of ecology teaching experts, with supporting evidence of their potential to address many of the problems raised. These proposed solutions include developing living labs, teaching students to be ecological entrepreneurs and influencers, embedding skills‐based learning and coding in the curriculum, an increased role for learned societies in teaching and learning, and using new technology to enhance fieldwork studies including virtual reality, artificial intelligence and real‐time spoken language translation.Our findings are focused towards UK higher education, but they should be informative for students and teachers of a wide range of educational levels, policy makers and professional ecologists worldwide.
Distinct behaviours can co-vary within individuals. As such, the magnitude of certain behaviours may be partly predicted by other behaviours, rather than the environment. This can constrain behaviours, potentially reducing behavioural variability. Pre-copulatory sexual cannibalism, the consumption of potential mates before copulation, can lead to females remaining unmated, particularly if males are rare. One possible explanation for the persistence of pre-copulatory cannibalism is that sexual cannibalism is correlated with high levels of aggression towards prey. Here, we test this in two species of praying mantis: the highly cannibalistic Miomantis caffra and the less cannibalistic Orthodera novaezealandiae . If cannibalism in M. caffra is linked to aggression towards prey, we predicted that (1) M. caffra would be more aggressive towards prey than O. novaezealandiae , (2) female M. caffra would be more aggressive than males, (3) aggression towards prey would be correlated across juvenile and adult instars for M. caffra but not O. novaezealandiae , and (4) aggression towards prey would be associated with a propensity for sexual cannibalism among individual M. caffra . We found evidence supporting predictions one and two, but not predictions three and four. Surprisingly, aggression was shown to be repeatable and correlated across instars for O. novaezealandiae but not M. caffra . Our results suggest sexual cannibalism is not a product of behavioural co-variation, even in clades where sexual cannibalism is common. This suggests that sexual cannibalism evolves due to the direct benefits it brings to females, rather than being a by-product of high aggression towards heterospecific prey. Significance statement In some animals, different behaviours co-vary within individuals. This may lead to the emergence of costly behaviours and reduce behavioural plasticity. It is theorized that pre-copulatory cannibalism is a costly behavioural by-product of selection for high levels of aggression towards prey. However, there are very few studies that explicitly test this. Here, we provide a behavioural comparison between two species of praying mantis that vary in their propensity to cannibalize and tested whether general aggression is linked cannibalism. We found that aggression towards prey in adults can be linked to juvenile aggression but not a propensity for cannibalism. Although cannibalism rates were higher in the species that was more aggressive towards prey, aggression towards prey was not linked to cannibalism within individuals. This suggests that pre-copulatory cannibalism is not a behavioural by-product but a result of direct selection.
Adaptation to a novel food source can have significant evolutionary advantages. The fruit fly, Drosophila sechellia, is a specialist of the toxic plant noni (Morinda citrifolia). Little is known as to how D. sechellia has become resistant to the toxins in the fruit - comprised predominantly of octanoic acid - but to date, the behavioural preferences for the fruit and genetic architecture underlying them, have been well studied. Here, we examine whether the gut microbiota could have played a role in adaptation to the fruit. In the first series of experiments, we examine the gut microbiota of wild-type, laboratory reared flies and characterise the gut microbiota when reared on the natural host plant, versus a standard Drosophila diet. We show a rapid transition in the core bacterial diversity and abundance within this species and discover sole precedence of Lactobacillus plantarum when reared on M. citrifolia. We also discover that flies reared on a laboratory diet are more likely to carry bacterial pathogens such as Bacillus cereus, although their function in Drosophila is unknown. Flies reared on a laboratory diet have a significantly reduced weight but with no impact on the risk of death before adulthood, when compared to the wild noni diet. In the second series of experiments, we examine the potential role of the gut microbiota in adaptation to octanoic acid resistance in this species and its sister species, Drosophila melanogaster, to which the fruit is usually fatal. We use a combination of methods to analyse resistance to octanoic acid by conducting life history analysis, behavioural assays and bacterial analysis in both D. sechellia and D. melanogaster. We find that by creating experimental evolution lines of D. melanogaster supplemented with gut microbiota from D. sechellia, we can decrease D. melanogaster aversion to octanoic acid, with the flies even preferring to feed on food supplemented with the acid. We suggest this represents the first step in the evolutionary and ecological specialisation of D. sechellia to its toxic host plant, and that the gut microbiota, Lactobacillus plantarum in particular, may have played a key role in host specialisation.
Some behaviours that typically increase fitness at the individual level may reduce population persistence, particularly in the face of environmental changes. Sexual cannibalism is an extreme mating behaviour which typically involves a male being devoured by the female immediately before, during or after copulation, and is widespread amongst predatory invertebrates. Although the individual-level effects of sexual cannibalism are reasonably well understood, very little is known about the population-level effects. We constructed both a mathematical model and an individual-based model to predict how sexual cannibalism might affect population growth rate and extinction risk. We found that in the absence of any cannibalism-derived fecundity benefit, sexual cannibalism is always detrimental to population growth rate and leads to a higher population extinction risk. Increasing the fecundity benefits of sexual cannibalism leads to a consistently higher population growth rate and likely a lower extinction risk. However, even if cannibalism-derived fecundity benefits are large, very high rates of sexual cannibalism (>70%) can still drive the population to negative growth and potential extinction. Pre-copulatory cannibalism was particularly damaging for population growth rates and was the main predictor of growth declining below the replacement rate. Surprisingly, post-copulatory cannibalism had a largely positive effect on population growth rate when fecundity benefits were present. This study is the first to formally estimate the population-level effects of sexual cannibalism. We highlight the detrimental effect sexual cannibalism may have on population viability if (1) cannibalism rates become high, and/or (2) cannibalism-derived fecundity benefits become low. Decreased food availability could plausibly both increase the frequency of cannibalism, and reduce the fecundity benefit of cannibalism, suggesting that sexual cannibalism may increase the risk of population collapse in the face of environmental change.