Anthropogenic Change and the Process of Speciation.

Anthropogenic impacts on the environment alter speciation processes by affecting both geographical contexts and selection patterns on a worldwide scale. Here we review evidence of these effects. We find that human activities often generate spatial isolation between populations and thereby promote genetic divergence but also frequently cause sudden secondary contact and hybridization between diverging lineages. Human-caused environmental changes produce new ecological niches, altering selection in diverse ways that can drive diversification; but changes also often remove niches and cause extirpations. Human impacts that alter selection regimes are widespread and strong in magnitude, ranging from local changes in biotic and abiotic conditions to direct harvesting to global climate change. Altered selection, and evolutionary responses to it, impacts early-stage divergence of lineages, but does not necessarily lead toward speciation and persistence of separate species. Altogether, humans both promote and hinder speciation, although new species would form very slowly relative to anthropogenic hybridization, which can be nearly instantaneous. Speculating about the future of speciation, we highlight two key conclusions: (1) Humans will have a large influence on extinction and "despeciation" dynamics in the short term and on early-stage lineage divergence, and thus potentially speciation in the longer term, and (2) long-term monitoring combined with easily dated anthropogenic changes will improve our understanding of the processes of speciation. We can use this knowledge to preserve and restore ecosystems in ways that promote (re-)diversification, increasing future opportunities of speciation and enhancing biodiversity.

Multi stress system: Microplastics in freshwater and their effects on host microbiota.

Microplastics are persistent and complex contaminants that have recently been found in freshwater systems, raising concerns about their presence in aquatic organisms. Plastics tend to be seen as an inert material; however, it is not well known if exposure to plastics for a prolonged time, in combination with organic chemicals, causes organism mortality. Ingestion of microplastics in combination with another pollutant may affect a host organism's fitness by altering the host microbiome. In this study, we investigated how microplastics interact with other pollutants in this multi-stress system, and whether they have a synergistic impact on the mortality of an aquatic organism and its microbiome. We used wild water boatmen Hemiptera (Corixidae) found at lake Erken located in east-central Sweden in a fully factorial two-way microcosm experiment designed with polystyrene microspheres and a commonly used detergent. The microplastic-detergent interaction is manifested as a significant increase in mortality compared to the other treatments at 48 h of exposure. The diversity of the microbial communities in the water was significantly affected by the combined treatment of microplastics and the detergent while the microbial communities in the host were affected by the treatments with microplastics and the detergent alone. Changes in relative abundance in Gammaproteobacteria (family Enterobacteriaceae), were observed in the perturbed treatments mostly associated with the presence of the detergent. This confirms that microplastics can interact with detergents having toxic effects on wild water boatmen. Furthermore, microplastics may impact wild organisms via changes in their microbial communities.

Microplastic exposure across trophic levels: effects on the host-microbiota of freshwater organisms.

BACKGROUND: Microplastics are a pervasive pollutant widespread in the sea and freshwater from anthropogenic sources, and together with the presence of pesticides, they can have physical and chemical effects on aquatic organisms and on their microbiota. Few studies have explored the combined effects of microplastics and pesticides on the host-microbiome, and more importantly, the effects across multiple trophic levels. In this work, we studied the effects of exposure to microplastics and the pesticide deltamethrin on the diversity and abundance of the host-microbiome across a three-level food chain: daphnids-damselfly-dragonflies. Daphnids were the only organism exposed to 1 µm microplastic beads, and they were fed to damselfly larvae. Those damselfly larvae were exposed to deltamethrin and then fed to the dragonfly larvae. The microbiotas of the daphnids, damselflies, and dragonflies were analyzed. RESULTS: Exposure to microplastics and deltamethrin had a direct effect on the microbiome of the species exposed to these pollutants. An indirect effect was also found since exposure to the pollutants at lower trophic levels showed carry over effects on the diversity and abundance of the microbiome on higher trophic levels, even though the organisms at these levels where not directly exposed to the pollutants. Moreover, the exposure to deltamethrin on the damselflies negatively affected their survival rate in the presence of the dragonfly predator, but no such effects were found on damselflies fed with daphnids that had been exposed to microplastics. CONCLUSIONS: Our study highlights the importance of evaluating ecotoxicological effects at the community level. Importantly, the indirect exposure to microplastics and pesticides through diet can potentially have bottom-up effects on the trophic webs.

Single and combined effects of microplastics, pyrethroid and food resources on the life-history traits and microbiome of Chironomus riparius.

There is growing evidence of widespread contamination of freshwater ecosystems with microplastics. However, the effects of chronic microplastic ingestion and its interaction with other pollutants and stress factors on the life-history traits and the host-microbiome of aquatic invertebrates are not well understood. This study investigates the effects of exposure to sediment spiked with 1 µm polystyrene-based latex microplastic spheres, an environmentally realistic concentration of a pyrethroid pesticide (esfenvalerate), and a combination of both treatments on the life-history traits of the benthic-dwelling invertebrate, Chironomus riparius and its microbial community. The chironomid larvae were also exposed to two food conditions: abundant or limited food in the sediment, monitored for 28 and 34 days respectively. The microplastics and esfenvalerate had negative effects on adult emergence and survival, and these effects differed between the food level treatments. The microbiome diversity was negatively affected by the exposure to microplastics, while the relative abundances of the four top phyla were significantly affected only in the high food level treatment. Although the combined exposure to microplastics and esfenvalerate showed some negative effects on survival and emergence, there was little evidence for synergistic effects when compared to the single exposure. The food level affected all life-history traits and the microbiota, and lower food levels intensified the negative effects of the exposure to microplastics, esfenvalerate and their combination. We argue that these pollutants can affect crucial life-history traits such as successful metamorphosis and the host-microbiome. Therefore, it should be taken into consideration for toxicological assessment of pollutant acceptability. Our study highlights the importance of investigating possible additive and synergic activities between stressors to understand the effects of pollutants in the life story traits and host-microbiome.

Sex-specific plasticity in a trophic polymorphic aquatic predator: a modeling approach.

Phenotypic plasticity is common among animal taxa. While there are clearly limits and likely costs to plasticity, these costs are unknown for most organisms. Further, as plasticity is partially genetically determined, the potential magnitude of exhibited plasticity may vary among individuals. In addition to phenotypic plasticity, various animal taxa also display sexual size dimorphism, a feature ultimately thought to arise due to differential size-dependent fitness costs and benefits between sexes. We hypothesized that differential selection acting on males and females can indirectly select for unequal genetically defined plasticity potential between the sexes. We evaluate this possibility for Eurasian perch (Perca fluviatilis), a species that displays modest sexual size dimorphism and habitat-related morphological plasticity. Using 500-year simulations of an ecogenetic agent-based model, we demonstrate that genetically determined morphological plasticity potential may evolve differently for males and females, leading to greater realized morphological variation between habitats for one sex over the other. Genetically determined potential for plasticity evolved differently between sexes across (a) various sex-specific life-history differences and (b) a variety of assumed costs of plasticity acting on both growth and survival. Morphological analyses of Eurasian perch collected in situ were consistent with model predictions: realized morphological variation between habitats was greater for females than males. We suggest that due to sex-specific selective pressures, differences in male and female genetically defined potential for plasticity may be a common feature across organisms.

Can information from citizen science data be used to predict biodiversity in stormwater ponds?

Citizen science data (CSD) have the potential to be a powerful scientific approach to assess, monitor and predict biodiversity. Here, we ask whether CSD could be used to predict biodiversity of recently constructed man-made habitats. Biodiversity data on adult dragonfly abundance from all kinds of aquatic habitats collected by citizen scientists (volunteers) were retrieved from the Swedish Species Observation System and were compared with dragonfly abundance in man-made stormwater ponds. The abundance data of dragonflies in the stormwater ponds were collected with a scientific, standardized design. Our results showed that the citizen science datasets differed significantly from datasets collected scientifically in stormwater ponds. Hence, we could not predict biodiversity in stormwater ponds from the data collected by citizen scientists. Using CSD from past versus recent years or from small versus large areas surrounding the stormwater ponds did not change the outcome of our tests. However, we found that biodiversity patterns obtained with CSD were similar to those from stormwater ponds when we restricted our analyses to rare species. We also found a higher beta diversity for the CSD compared to the stormwater dataset. Our results suggest that if CSD are to be used for estimating or predicting biodiversity, we need to develop methods that take into account or correct for the under-reporting of common species in CSD.

A way forward with eco evo devo: an extended theory of resource polymorphism with postglacial fishes as model systems.

A major goal of evolutionary science is to understand how biological diversity is generated and altered. Despite considerable advances, we still have limited insight into how phenotypic variation arises and is sorted by natural selection. Here we argue that an integrated view, which merges ecology, evolution and developmental biology (eco evo devo) on an equal footing, is needed to understand the multifaceted role of the environment in simultaneously determining the development of the phenotype and the nature of the selective environment, and how organisms in turn affect the environment through eco evo and eco devo feedbacks. To illustrate the usefulness of an integrated eco evo devo perspective, we connect it with the theory of resource polymorphism (i.e. the phenotypic and genetic diversification that occurs in response to variation in available resources). In so doing, we highlight fishes from recently glaciated freshwater systems as exceptionally well-suited model systems for testing predictions of an eco evo devo framework in studies of diversification. Studies on these fishes show that intraspecific diversity can evolve rapidly, and that this process is jointly facilitated by (i) the availability of diverse environments promoting divergent natural selection; (ii) dynamic developmental processes sensitive to environmental and genetic signals; and (iii) eco evo and eco devo feedbacks influencing the selective and developmental environments of the phenotype. We highlight empirical examples and present a conceptual model for the generation of resource polymorphism - emphasizing eco evo devo, and identify current gaps in knowledge.

Asymmetrical habitat coupling of an aquatic predator-The importance of individual specialization.

Predators should stabilize food webs because they can move between spatially separate habitats. However, predators adapted to forage on local resources may have a reduced ability to couple habitats. Here, we show clear asymmetry in the ability to couple habitats by Eurasian perch-a common polymorphic predator in European lakes. We sampled perch from two spatially separate habitats-pelagic and littoral zones-in Lake Erken, Sweden. Littoral perch showed stronger individual specialization, but they also used resources from the pelagic zone, indicating their ability to couple habitats. In contrast, pelagic perch showed weaker individual specialization but near complete reliance on pelagic resources, indicating their preference to one habitat. This asymmetry in the habitat coupling ability of perch challenges the expectation that, in general, predators should stabilize spatially separated food webs. Our results suggest that habitat coupling might be constrained by morphological adaptations, which in this case were not related to genetic differentiation but were more likely related to differences in individual specialization.

Biodiversity loss through speciation collapse: Mechanisms, warning signals, and possible rescue.

Speciation is the process that generates biodiversity, but recent empirical findings show that it can also fail, leading to the collapse of two incipient species into one. Here, we elucidate the mechanisms behind speciation collapse using a stochastic individual-based model with explicit genetics. We investigate the impact of two types of environmental disturbance: deteriorated visual conditions, which reduce foraging ability and impede mate choice, and environmental homogenization, which restructures ecological niches. We find that: (1) Species pairs can collapse into a variety of forms including new species pairs, monomorphic or polymorphic generalists, or single specialists. Notably, polymorphic generalist forms may be a transient stage to a monomorphic population; (2) Environmental restoration enables species pairs to reemerge from single generalist forms, but not from single specialist forms; (3) Speciation collapse is up to four orders of magnitude faster than speciation, while the reemergence of species pairs can be as slow as de novo speciation; (4) Although speciation collapse can be predicted from either demographic, phenotypic, or genetic signals, observations of phenotypic changes allow the most general and robust warning signal of speciation collapse. We conclude that factors altering ecological niches can reduce biodiversity by reshaping the ecosystem's evolutionary attractors.

Predation selects for smaller eye size in a vertebrate: effects of environmental conditions and sex.

Increased eye size in animals results in a larger retinal image and thus improves visual acuity. Thus, larger eyes should aid both in finding food as well as detecting predators. On the other hand, eyes are usually very conspicuous and several studies have suggested that eye size is associated with predation risk. However, experimental evidence is scant. In this study, we address how predation affects variation in eye size by performing two experiments using Eurasian perch juveniles as prey and either larger perch or pike as predators. First, we used large outdoor tanks to compare selection due to predators on relative eye size in open and artificial vegetated habitats. Second, we studied the effects of both predation risk and resource levels on phenotypic plasticity in relative eye size in indoor aquaria experiments. In the first experiment, we found that habitat altered selection due to predators, since predators selected for smaller eye size in a non-vegetated habitat, but not in a vegetated habitat. In the plasticity experiment, we found that fish predators induced smaller eye size in males, but not in females, while resource levels had no effect on eye size plasticity. Our experiments provide evidence that predation risk could be one of the driving factors behind variation in eye size within species.

Warmer and browner waters decrease fish biomass production.

Climate change studies have long focused on effects of increasing temperatures, often without considering other simultaneously occurring environmental changes, such as browning of waters. Resolving how the combination of warming and browning of aquatic ecosystems affects fish biomass production is essential for future ecosystem functioning, fisheries, and food security. In this study, we analyzed individual- and population-level fish data from 52 temperate and boreal lakes in Northern Europe, covering large gradients in water temperature and color (absorbance, 420 nm). We show that fish (Eurasian perch, Perca fluviatilis) biomass production decreased with both high water temperatures and brown water color, being lowest in warm and brown lakes. However, while both high temperature and brown water decreased fish biomass production, the mechanisms behind the decrease differed: temperature affected the fish biomass production mainly through a decrease in population standing stock biomass, and through shifts in size- and age-distributions toward a higher proportion of young and small individuals in warm lakes; brown water color, on the other hand, mainly influenced fish biomass production through negative effects on individual body growth and length-at-age. In addition to these findings, we observed that the effects of temperature and brown water color on individual-level processes varied over ontogeny. Body growth only responded positively to higher temperatures among young perch, and brown water color had a stronger negative effect on body growth of old than on young individuals. Thus, to better understand and predict future fish biomass production, it is necessary to integrate both individual- and population-level responses and to acknowledge within-species variation. Our results suggest that global climate change, leading to browner and warmer waters, may negatively affect fish biomass production, and this effect may be stronger than caused by increased temperature or water color alone.

Microbiomes as Metacommunities: Understanding Host-Associated Microbes through Metacommunity Ecology.

Interest in host-associated microbiomes has skyrocketed recently, yet our ability to explain microbiome variation has remained stubbornly low. Considering scales of interaction beyond the level of the individual host could lead to new insights. Metacommunity theory has many of the tools necessary for modeling multiscale processes and has been successfully applied to host microbiomes. However, the biotic nature of the host requires an expansion of theory to incorporate feedback between the habitat patch (host) and their local (microbial) community. This feedback can have unexpected effects, is predicted to be common, and can arise through a variety of mechanisms, including developmental, ecological, and evolutionary processes. We propose a new way forward for both metacommunity theory and host microbiome research that incorporates this feedback.

Effects of predation stress and food ration on perch gut microbiota.

BACKGROUND: Gut microbiota provide functions of importance to influence hosts' food digestion, metabolism, and protection against pathogens. Factors that affect the composition and functions of gut microbial communities are well studied in humans and other animals; however, we have limited knowledge of how natural food web factors such as stress from predators and food resource rations could affect hosts' gut microbiota and how it interacts with host sex. In this study, we designed a two-factorial experiment exposing perch (Perca fluviatilis) to a predator (pike, Esox lucius), and different food ratios, to examine the compositional and functional changes of perch gut microbiota based on 16S rRNA amplicon sequencing. We also investigated if those changes are host sex dependent. RESULTS: We showed that overall gut microbiota composition among individual perch significantly responded to food ration and predator presence. We found that species richness decreased with predator presence, and we identified 23 taxa from a diverse set of phyla that were over-represented when a predator was present. For example, Fusobacteria increased both at the lowest food ration and at predation stress conditions, suggesting that Fusobacteria are favored by stressful situations for the host. In concordance, both food ration and predation stress seemed to influence the metabolic repertoire of the gut microbiota, such as biosynthesis of other secondary metabolites, metabolism of cofactors, and vitamins. In addition, the identified interaction between food ration and sex emphasizes sex-specific responses to diet quantity in gut microbiota. CONCLUSIONS: Collectively, our findings emphasize an alternative state in gut microbiota with responses to changes in natural food webs depending on host sex. The obtained knowledge from this study provided us with an important perspective on gut microbiota in a food web context.

The interaction between predation risk and food ration on behavior and morphology of Eurasian perch.

The risk of both predation and food level has been shown to affect phenotypic development of organisms. However, these two factors also influence animal behavior that in turn may influence phenotypic development. Hence, it might be difficult to disentangle the behavioral effect from the predator or resource-level effects. This is because the presence of predators and high resource levels usually results in a lower activity, which in turn affects energy expenditure that is used for development and growth. It is therefore necessary to study how behavior interacts with changes in body shape with regard to resource density and predators. Here, we use the classic predator-induced morphological defense in fish to study the interaction between predator cues, resource availability, and behavioral activity with the aim to determine their relative contribution to changes in body shape. We show that all three variables, the presence of a predator, food level, and activity, both additively and interactively, affected the body shape of perch. In general, the presence of predators, lower swimming activity, and higher food levels induced a deep body shape, with predation and behavior having similar effect and food treatment the smallest effect. The shape changes seemed to be mediated by changes in growth rate as body condition showed a similar effect as shape with regard to food-level and predator treatments. Our results suggests that shape changes in animals to one environmental factor, for example, predation risk, can be context dependent, and depend on food levels or behavioral responses. Theoretical and empirical studies should further explore how this context dependence affects fitness components such as resource gain and mortality and their implications for population dynamics.

Synergistic selection between ecological niche and mate preference primes diversification.

The ecological niche and mate preferences have independently been shown to be important for the process of speciation. Here, we articulate a novel mechanism by which ecological niche use and mate preference can be linked to promote speciation. The degree to which individual niches are narrow and clustered affects the strength of divergent natural selection and population splitting. Similarly, the degree to which individual mate preferences are narrow and clustered affects the strength of divergent sexual selection and assortative mating between diverging forms. This novel perspective is inspired by the literature on ecological niches; it also explores mate preferences and how they may contribute to speciation. Unlike much comparative work, we do not search for evolutionary patterns using proxies for adaptation and sexual selection, but rather we elucidate how ideas from niche theory relate to mate preference, and how this relationship can foster speciation. Recognizing that individual and population niches are conceptually and ecologically linked to individual and population mate preference functions will significantly increase our understanding of rapid evolutionary diversification in nature. It has potential to help solve the difficult challenge of testing the role of sexual selection in the speciation process. We also identify ecological factors that are likely to affect individual niche and individual mate preference in synergistic ways and as a consequence to promote speciation. The ecological niche an individual occupies can directly affect its mate preference. Clusters of individuals with narrow, differentiated niches are likely to have narrow, differentiated mate preference functions. Our approach integrates ecological and sexual selection research to further our understanding of diversification processes. Such integration may be necessary for progress because these processes seem inextricably linked in the natural world.

Mechanisms by Which Phenotypic Plasticity Affects Adaptive Divergence and Ecological Speciation.

Phenotypic plasticity is the ability of one genotype to produce different phenotypes depending on environmental conditions. Several conceptual models emphasize the role of plasticity in promoting reproductive isolation and, ultimately, speciation in populations that forage on two or more resources. These models predict that plasticity plays a critical role in the early stages of speciation, prior to genetic divergence, by facilitating fast phenotypic divergence. The ability to plastically express alternative phenotypes may, however, interfere with the early phase of the formation of reproductive barriers, especially in the absence of geographic barriers. Here, we quantitatively investigate mechanisms under which plasticity can influence progress toward adaptive genetic diversification and ecological speciation. We use a stochastic, individual-based model of a predator-prey system incorporating sexual reproduction and mate choice in the predator. Our results show that evolving plasticity promotes the evolution of reproductive isolation under diversifying environments when individuals are able to correctly select a more profitable habitat with respect to their phenotypes (i.e., adaptive habitat choice) and to assortatively mate with relatively similar phenotypes. On the other hand, plasticity facilitates the evolution of plastic generalists when individuals have a limited capacity for adaptive habitat choice. We conclude that plasticity can accelerate the evolution of a reproductive barrier toward adaptive diversification and ecological speciation through enhanced phenotypic differentiation between diverging phenotypes.

Intraspecific Niche Variation Drives Abundance-Occupancy Relationships in Freshwater Fish Communities.

A positive relationship between occupancy and average local abundance of species is found in a variety of taxa, yet the mechanisms driving this association between abundance and occupancy are still enigmatic. Here we show that freshwater fishes exhibit a positive abundance-occupancy relationship across 125 Swedish lakes. For a subset of 9 species from 11 lakes, we estimated species-specific diet breadth from stable isotopes, within-lake habitat breadth from catch data for littoral and pelagic nets, adaptive potential from genetic diversity, abiotic niche position, and dispersal capacity. Average local abundance was mainly positively associated with both within-lake habitat and diet breadth, that is, species with larger intraspecific variation in niche space had higher abundances. No measure was a good predictor of occupancy, indicating that occupancy may be more directly related to abundance or abiotic conditions than to niche breadth per se. This study suggests a link between intraspecific niche variation and a positive abundance-occupancy relationship and implies that management of freshwater fish communities, whether to conserve threatened or control invasive species, should initially be aimed at niche processes.

Individuals in food webs: the relationships between trophic position, omnivory and among-individual diet variation.

Among-individual diet variation is common in natural populations and may occur at any trophic level within a food web. Yet, little is known about its variation among trophic levels and how such variation could affect phenotypic divergence within populations. In this study we investigate the relationships between trophic position (the population's range and average) and among-individual diet variation. We test for diet variation among individuals and across size classes of Eurasian perch (Perca fluviatilis), a widespread predatory freshwater fish that undergoes ontogenetic niche shifts. Second, we investigate among-individual diet variation within fish and invertebrate populations in two different lake communities using stable isotopes. Third, we test potential evolutionary implications of population trophic position by assessing the relationship between the proportion of piscivorous perch (populations of higher trophic position) and the degree of phenotypic divergence between littoral and pelagic perch sub-populations. We show that among-individual diet variation is highest at intermediate trophic positions, and that this high degree of among-individual variation likely causes an increase in the range of trophic positions among individuals. We also found that phenotypic divergence was negatively related to trophic position in a population. This study thus shows that trophic position is related to and may be important for among-individual diet variation as well as to phenotypic divergence within populations.

Plastic responses of a sessile prey to multiple predators: a field and experimental study.

BACKGROUND: Theory predicts that prey facing a combination of predators with different feeding modes have two options: to express a response against the feeding mode of the most dangerous predator, or to express an intermediate response. Intermediate phenotypes protect equally well against several feeding modes, rather than providing specific protection against a single predator. Anti-predator traits that protect against a common feeding mode displayed by all predators should be expressed regardless of predator combination, as there is no need for trade-offs. PRINCIPAL FINDINGS: We studied phenotypic anti-predator responses of zebra mussels to predation threat from a handling-time-limited (crayfish) and a gape-size-limited (roach) predator. Both predators dislodge mussels from the substrate but diverge in their further feeding modes. Mussels increased expression of a non-specific defense trait (attachment strength) against all combinations of predators relative to a control. In response to roach alone, mussels showed a tendency to develop a weaker and more elongated shell. In response to crayfish, mussels developed a harder and rounder shell. When exposed to either a combination of predators or no predator, mussels developed an intermediate phenotype. Mussel growth rate was positively correlated with an elongated weaker shell and negatively correlated with a round strong shell, indicating a trade-off between anti-predator responses. Field observations of prey phenotypes revealed the presence of both anti-predator phenotypes and the trade-off with growth, but intra-specific population density and bottom substrate had a greater influence than predator density. CONCLUSIONS: Our results show that two different predators can exert both functionally equivalent and inverse selection pressures on a single prey. Our field study suggests that abiotic factors and prey population density should be considered when attempting to explain phenotypic diversity in the wild.

Individual diet has sex-dependent effects on vertebrate gut microbiota.

Vertebrates harbour diverse communities of symbiotic gut microbes. Host diet is known to alter microbiota composition, implying that dietary treatments might alleviate diseases arising from altered microbial composition ('dysbiosis'). However, it remains unclear whether diet effects are general or depend on host genotype. Here we show that gut microbiota composition depends on interactions between host diet and sex within populations of wild and laboratory fish, laboratory mice and humans. Within each of two natural fish populations (threespine stickleback and Eurasian perch), among-individual diet variation is correlated with individual differences in gut microbiota. However, these diet-microbiota associations are sex dependent. We document similar sex-specific diet-microbiota correlations in humans. Experimental diet manipulations in laboratory stickleback and mice confirmed that diet affects microbiota differently in males versus females. The prevalence of such genotype by environment (sex by diet) interactions implies that therapies to treat dysbiosis might have sex-specific effects.