Rapid evolution in response to introduced predators I: rates and patterns of morphological and life-history trait divergence

Background  

Introduced species can have profound effects on native species, communities, and ecosystems, and have caused extinctions or declines in native species globally. We examined the evolutionary response of native zooplankton populations to the introduction of non-native salmonids in alpine lakes in the Sierra Nevada of California, USA. We compared morphological and life-history traits in populations of Daphnia with a known history of introduced salmonids and populations that have no history of salmonid introductions.     

Rapid evolution of thermal plasticity in mountain lake Daphnia populations

Populations at risk of extinction due to climate change may be rescued by adaptive evolution or plasticity. Selective agents, such as introduced predators, may enhance or constrain plastic or adaptive responses to temperature. We tested responses of Daphnia to temperature by collecting populations from lakes across an elevational gradient in the presence and absence of fish predators (long‐term selection). We subsequently grew these populations at two elevations in field mesocosms over two years (short‐term selection), followed by a common‐garden experiment at two temperatures in the lab to measure life‐history traits. Both long‐term and short‐term selection affected traits, suggesting that genetic variation of plasticity within populations enabled individuals to rapidly evolve plasticity in response to high temperature. We found that short‐term selection by high temperature increased plasticity for growth rate in all populations. Fecundity was higher in populations from fishless lakes and body size showed greater plasticity in populations from warm lakes (long‐term selection). Neither body size nor fecundity were affected by short‐term thermal selection. These results demonstrate that plasticity is an important component of the life‐history response of Daphnia, and that genetic variation within populations enabled rapid evolution of plasticity in response to selection by temperature.     

Invasion strategies in clonal aquatic plants: are phenotypic differences caused by phenotypic plasticity or local adaptation?

Background and Aims

The successful spread of invasive plants in new environments is often linked to multiple introductions and a diverse gene pool that facilitates local adaptation to variable environmental conditions. For clonal plants, however, phenotypic plasticity may be equally important. Here the primary adaptive strategy in three non-native, clonally reproducing macrophytes (Egeria densa, Elodea canadensis and Lagarosiphon major) in New Zealand freshwaters were examined and an attempt was made to link observed differences in plant morphology to local variation in habitat conditions.

Methods

Field populations with a large phenotypic variety were sampled in a range of lakes and streams with different chemical and physical properties. The phenotypic plasticity of the species before and after cultivation was studied in a common garden growth experiment, and the genetic diversity of these same populations was also quantified.

Key Results

For all three species, greater variation in plant characteristics was found before they were grown in standardized conditions. Moreover, field populations displayed remarkably little genetic variation and there was little interaction between habitat conditions and plant morphological characteristics.

Conclusions

The results indicate that at the current stage of spread into New Zealand, the primary adaptive strategy of these three invasive macrophytes is phenotypic plasticity. However, while limited, the possibility that genetic diversity between populations may facilitate ecotypic differentiation in the future cannot be excluded. These results thus indicate that invasive clonal aquatic plants adapt to new introduced areas by phenotypic plasticity. Inorganic carbon, nitrogen and phosphorous were important in controlling plant size of E. canadensis and L. major, but no other relationships between plant characteristics and habitat conditions were apparent. This implies that within-species differences in plant size can be explained by local nutrient conditions. All together this strongly suggests that invasive clonal aquatic plants adapt to a wide range of habitats in introduced areas by phenotypic plasticity rather than local adaptation.     

The adaptive value of phenotypic plasticity in two ecotypes of a marine gastropod

Background  

Few surveys have concentrated on studying the adaptive value of phenotypic plasticity within genetically-distinct conspecific ecotypes. Here, we conduct a test to assess the adaptive value that partial phenotypic plasticity may have for survival in the marine gastropod Littorina saxatilis. This species has evolved canalized ecotypes but, nevertheless, the ecotypes show some phenotypic plasticity for the traits under divergent selection between wave-exposed and high-predation habitats.     

Molecular genetic analysis of Daphnia in the English Lake District: species identity, hybridisation and resting egg banks

• 1 Taxonomic issues in many Daphnia species complexes are often confused by a high degree of phenotypic plasticity and by interspecific hybridisation. Here, we employ molecular genetic tools to confirm the species composition and incidence of hybridisation in extant and resting egg populations of Daphnia from Windermere and Esthwaite Water in the English Lake District.
• 2 A combination of species‐diagnostic allozymes and mtDNA, confirms that contemporary populations are dominated by a single species, D. galeata.
• 3 We present the first account of genetic characterisation of dated ‘resting’ eggs using microsatellites and mtDNA, employing PCR‐based DNA recovery, thus providing a temporal dimension to taxonomic patterns. Thirty years ago, two species were present in Esthwaite, D. galeata and D. hyalina, but Windermere populations were dominated by D. galeata only.
• 4 The use of PCR‐based mtDNA RFLP analysis as a species‐diagnostic tool, and microsatellites to monitor clonal diversity, provide a valuable approach for long‐term studies, especially in populations free from the complicating effect of frequent hybridisation. The detailed limnological records available for many large lakes, and associated changes in land‐use, pollutants and climate, combined with long‐term ephippial molecular genetic data, provide opportunities for exploring natural and anthropogenic impacts on genetic and community structure.

     

Patterns and sources of variation in Daphnia phosphorus content in nature

It has recently been shown that Daphnia can vary in the phosphorus (P)-content of their body tissues, but the relative importance of genetic versus environmental causes for this variation is unexplored. We measured variation in P-content (as % body mass) of Daphnia from eight lakes and conducted experiments to contrast three sources of variation: interspecific variation, clonal variation and phenotypic plasticity. Daphnia P-content decreased with increasing seston C:P ratio across lakes. This relationship reflected both inter- and intraspecific variation. Daphnia parvula and D. dubia exhibited high P-content and were found in shallow lakes with low C:P seston, whereas D. pulicaria had low P-content and was found in deep, stratified lakes having high C:P seston. Populations of D. dentifera spanned this lake gradient and exhibited P-content that was negatively related to seston C:P. Evidence for phenotypic plasticity came from experiments with D. pulicaria and D. dentifera collected from a lake with P-deficient seston and fed a P-sufficient diet in the laboratory. In addition, populations of D. dentifera differed in P-content even after 7 d of feeding on P-sufficient resources, suggesting within-species clonal variation. However, mesocosm experiments revealed broad and surprisingly continuous variation in the P-content of individual clones of D. pulex (range 1.54–1.05%) and D. mendotae (1.51–1.07%) over a gradient in dietary C:P. The broad range in P-content exhibited by individual clones, acclimated for generations, suggests that variation in Daphnia P-content from laboratory experiments needs to be interpreted with caution. These results also show that phenotypic variation in response to environment can be a larger source of variation in P-content than genetic differences within or among species.     

Allopatric and sympatric diversification within roach (Rutilus rutilus) of large pre‐alpine lakes

Intraspecific differentiation in response to divergent natural selection between environments is a common phenomenon in some northern freshwater fishes, especially salmonids and stickleback. Understanding why these taxa diversify and undergo adaptive radiations while most other fish species in the same environments do not, remains an open question. The possibility for intraspecific diversification has rarely been evaluated for most northern freshwater fish species. Here, we assess the potential for intraspecific differentiation between and within lake populations of roach (Rutilus rutilus)—a widespread and abundant cyprinid species—in lakes in which salmonids have evolved endemic adaptive radiations. Based on more than 3,000 polymorphic RADseq markers, we detected low but significant genetic differentiation between roach populations of two ultraoligotrophic lakes and between these and populations from other lakes. This, together with differentiation in head morphology and stable isotope signatures, suggests evolutionary and ecological differentiation among some of our studied populations. Next, we tested for intralacustrine diversification of roach within Lake Brienz, the most pristine lake surveyed in this study. We found significant phenotypic evidence for ecological intralacustrine differentiation between roach caught over a muddy substrate and those caught over a rocky substrate. However, evidence for intralacustrine genetic differentiation is at best subtle and phenotypic changes may therefore be mostly plastic. Overall, our findings suggest roach can differ between ecologically distinct lakes, but the extent of intralacustrine ecological differentiation is weak, which contrasts with the strong differentiation among endemic species of whitefish in the same lakes.     

Predators shape distribution and promote diversification of morphological defenses in <Emphasis Type="Italic">Leucorrhinia</Emphasis>, Odonata

Predators strongly influence species assemblages and shape morphological defenses of prey. Interestingly, adaptations that constitute effective defenses against one type of predator may render the prey susceptible to other types of predators. Hence, prey may evolve different strategies to escape predation, which may facilitate adaptive radiation of prey organisms. Larvae of different species in the dragonfly genus Leucorrhinia have various morphological defenses. We studied the distribution of these larvae in relation to the presence of predatory fish. In addition, we examined the variation in morphological defenses within species with respect to the occurrence of fish. We found that well-defended species, those with more and longer spines, were more closely associated with habitats inhabited by predatory fish and that species with weakly developed morphological defenses were more abundant in habitats without fish. The species predominantly connected to lakes with or without fish, respectively, were not restricted to a single clade in the phylogeny of the genus. Our data is suggestive of phenotypic plasticity in morphological defense in three of the studied species since these species showed longer spines in lakes with fish. We suggest that adaptive phenotypic plasticity may have broadened the range of habitats accessible to Leucorrhinia. It may have facilitated colonization of new habitats with different types of predators, and ultimately, speciation through adaptive radiation.     

Predator-induced plasticity does not alter the pathway from evolution to ecology among locally adapted populations of <Emphasis Type="Italic">Daphnia</Emphasis>

In the growing field of eco-evolutionary dynamics, evidence for an influence of rapid shifts in phenotype on ecological processes is accumulating, yet, the contributions of phenotypic plasticity versus genetic change to these observed ecological changes are unclear. In one of the best studied ecosystems in terms of eco-evolutionary dynamics, landlocked versus anadromous alewife (Alosa pseudoharengus) have caused strong evolutionary divergence in their key zooplankton prey (Daphnia ambigua). We previously showed that such evolutionary differences have cascading ecological effects on consumer-resource dynamics and primary production. Yet, these locally adapted populations of Daphnia also differ in trait plasticity, which may, in turn, modify the pathway from evolution to ecology. Here we compared Daphnia from lakes with landlocked versus anadromous alewife for differences in rates of population growth in the presence and absence of predator cues over the course of a 39-day experiment. We predicted that predator-induced shifts in life history traits would facilitate faster rates of population growth. Contrary to our expectations, predator cue exposure did not alter rates of population growth. We instead found that Daphnia from lakes with landlocked alewife ultimately attained higher population densities (and exhibited faster population growth) when compared with Daphnia from lakes with anadromous alewife. Based on our previous work, these population level responses were unexpected, as Daphnia from lakes with landlocked alewife exhibit slower rates of somatic growth and delayed maturation. We discuss our results in lieu of the known differences in plasticity and how the population growth patterns may be influenced by resource limitation.     

Evidence that fish structure the zooplankton communities of turbid lakes and reservoirs

1. Visually foraging fish typically exclude large zooplankton from clear‐water lakes and reservoirs. Do fish have the same effect in turbid waters, or does turbidity provide a refuge from visual predation? 2. To test the hypothesis that fish exclude large zooplankton species from turbid sites, I searched for populations of medium or large Daphnia species in turbid, fish‐containing reservoirs of south‐central Oklahoma and north‐central Texas, U.S.A., and surveyed the literature for accounts of Daphnia species in turbid habitats worldwide. 3. Only small Daphnia species and the exuberantly spined Daphnia lumholtzi were detected in the turbid reservoirs. The Daphnia species in the reservoirs are smaller than other Daphnia species that occur in the area but were not detected. An extensive survey of the literature suggests that large Daphnia may be found in the lakes of extreme turbidity [Secchi disk depth (SD) < 0.2 m] but that only small and spiny Daphnia are likely to occur in more typical turbid locations (1.0 m > SD > 0.2 m) unless some additional factor reduces the influence of fish predation in such sites. 4. The field samples from Texas and Oklahoma together with the literature review suggest that the effect of visually foraging planktivorous fish on the size structure of turbid‐water zooplankton communities may often be as strong or even stronger than the effect of fish on clear‐water zooplankton communities.     

Distinct migratory and non-migratory ecotypes of an endemic New Zealand eleotrid (<Emphasis Type="Italic">Gobiomorphus cotidianus</Emphasis>) – implications for incipient speciation in island freshwater fish species

Background  

Many postglacial lakes contain fish species with distinct ecomorphs. Similar evolutionary scenarios might be acting on evolutionarily young fish communities in lakes of remote islands. One process that drives diversification in island freshwater fish species is the colonization of depauperate freshwater environments by diadromous (migratory) taxa, which secondarily lose their migratory behaviour. The loss of migration limits dispersal and gene flow between distant populations, and, therefore, is expected to facilitate local morphological and genetic differentiation. To date, most studies have focused on interspecific relationships among migratory species and their non-migratory sister taxa. We hypothesize that the loss of migration facilitates intraspecific morphological, behavioural, and genetic differentiation between migratory and non-migratory populations of facultatively diadromous taxa, and, hence, incipient speciation of island freshwater fish species.     

Novel trophic niches drive variable progress towards ecological speciation within an adaptive radiation of pupfishes

Adaptive radiation is recognized by a rapid burst of phenotypic, ecological and species diversification. However, it is unknown whether different species within an adaptive radiation evolve reproductive isolation at different rates. We compared patterns of genetic differentiation between nascent species within an adaptive radiation of Cyprinodon pupfishes using genotyping by sequencing. Similar to classic adaptive radiations, this clade exhibits rapid morphological diversification rates and two species are novel trophic specialists, a scale‐eater and hard‐shelled prey specialist (durophage), yet the radiation is <10 000 years old. Both specialists and an abundant generalist species all coexist in the benthic zone of lakes on San Salvador Island, Bahamas. Based on 13 912 single‐nucleotide polymorphisms (SNPs), we found consistent differences in genetic differentiation between each specialist species and the generalist across seven lakes. The scale‐eater showed the greatest genetic differentiation and clustered by species across lakes, whereas durophage populations often clustered with sympatric generalist populations, consistent with parallel speciation across lakes. However, we found strong evidence of admixture between durophage populations in different lakes, supporting a single origin of this species and genome‐wide introgression with sympatric generalist populations. We conclude that the scale‐eater is further along the speciation‐with‐gene‐flow continuum than the durophage and suggest that different adaptive landscapes underlying these two niche environments drive variable progress towards speciation within the same habitat. Our previous measurements of fitness surfaces in these lakes support this conclusion: the scale‐eating fitness peak may be more distant than the durophage peak on the complex adaptive landscape driving adaptive radiation.     

Trait sorting in Daphnia colonising man‐made lakes

1. We used a zooplankton metacommunity to ask how dispersal, genetic drift and selection act to determine the local and regional distributions of trait variation. Since the formation of the lakes 80 years ago, cladoceran species have sorted into local assemblages that cluster by lake depth. Given this species sorting, we ask whether intraspecific variation in an ecologically important phenotypic trait – body size – has sorted as well. 2. We quantified changes in body size through time by measuring ephippia from D. pulicaria, D. dentifera and D. ambigua recovered from sediment cores from two lakes. We then estimated mean body size of contemporary populations of two competing species, Daphnia pulicaria and D. dentifera, in a laboratory common garden experiment. Finally, we used microsatellite loci to characterise genetic diversity and gene flow among local sites in the metacommunity. 3. Body size was variable both within and among years for the three species of Daphnia examined using sediment cores. For two lakes where we examined body size distributions through time, we observed a significant shift in body size of the first species to arrive after colonisation by other Daphnia species, which suggests selection has occurred historically. 4. Despite heritable variation in body size in the laboratory, evidence for trait sorting was only found for D. pulicaria, which was larger in deeper lakes. Mean body size varied among lakes, but did not sort relative to depth for D. dentifera. 5. Microsatellite data indicated that neutral genetic diversity was low in the region; only 27% of the individuals assayed were unique multi‐locus genotypes. We also found significant patterns of isolation by distance for both species. However, population structure was stronger in D. dentifera than in D. pulicaria. Hence, we conclude that a limited number of colonists have successfully invaded this metacommunity, and those genotypes arriving in this new region have experienced significant dispersal limitation among local sites. 6. Overall, while dispersal and selection have clearly led to the development of predictable community assemblages related to depth in this metacommunity, the distribution of phenotypic traits within species can differ substantially even between two trophically similar species. Our results highlight the complex roles of colonisation history, dispersal, selection and stochasticity in determining inter‐ and intra‐specific patterns in metacommunities.     

The heat is on: Genetic adaptation to urbanization mediated by thermal tolerance and body size

Worldwide, urbanization leads to tremendous anthropogenic environmental alterations, causing strong selection pressures on populations of animals and plants. Although a key feature of urban areas is their higher temperature (“urban heat islands”), adaptive thermal evolution in organisms inhabiting urban areas has rarely been studied. We tested for evolution of a higher heat tolerance (CT_MAX) in urban populations of the water flea Daphnia magna, a keystone grazer in freshwater ecosystems, by carrying out a common garden experiment at two temperatures (20°C and 24°C) with genotypes of 13 natural populations ordered along a well‐defined urbanization gradient. We also assessed body size and haemoglobin concentration to identify underlying physiological drivers of responses in CT_MAX. We found a higher CT_MAX in animals isolated from urban compared to rural habitats and in animals reared at higher temperatures. We also observed substantial genetic variation in thermal tolerance within populations. Overall, smaller animals were more heat tolerant. While urban animals mature at smaller size, the effect of urbanization on thermal tolerance is only in part caused by reductions in body size. Although urban Daphnia contained higher concentrations of haemoglobin, this did not contribute to their higher CT_MAX. Our results provide evidence of adaptive thermal evolution to urbanization in the water flea Daphnia. In addition, our results show both evolutionary potential and adaptive plasticity in rural as well as urban Daphnia populations, facilitating responses to warming. Given the important ecological role of Daphnia in ponds and lakes, these adaptive responses likely impact food web dynamics, top‐down control of algae, water quality, and the socio‐economic value of urban ponds.     

Where Am I? Niche constraints due to morphological specialization in two Tanganyikan cichlid fish species

Food resource specialization within novel environments is considered a common axis of diversification in adaptive radiations. Feeding specializations are often coupled with striking morphological adaptations and exemplify the relation between morphology and diet (phenotype–environment correlations), as seen in, for example, Darwin finches, Hawaiian spiders, and the cichlid fish radiations in East African lakes. The cichlids' potential to rapidly exploit and occupy a variety of different habitats has previously been attributed to the variability and adaptability of their trophic structures including the pharyngeal jaw apparatus. Here we report a reciprocal transplant experiment designed to explore the adaptability of the trophic structures in highly specialized cichlid fish species. More specifically, we forced two common but ecologically distinct cichlid species from Lake Tanganyika, Tropheus moorii (rock‐dweller), and Xenotilapia boulengeri (sand‐dweller), to live on their preferred as well as on an unpreferred habitat (sand and rock, respectively). We measured their overall performance on the different habitat types and explored whether adaptive phenotypic plasticity is involved in adaptation. We found that, while habitat had no effect on the performance of X. boulengeri, T. moorii performed significantly better in its preferred habitat. Despite an experimental duration of several months, we did not find a shift in the morphology of the lower pharyngeal jaw bone that would be indicative of adaptive phenotypic plasticity in this trait.     

Island biology and morphological divergence of the Skyros wall lizard <Emphasis Type="Italic">Podarcis gaigeae</Emphasis>: a combined role for local selection and genetic drift on color morph frequency divergence?

Background  

Patterns of spatial variation in discrete phenotypic traits can be used to draw inferences about the adaptive significance of traits and evolutionary processes, especially when compared to patterns of neutral genetic variation. Population divergence in adaptive traits such as color morphs can be influenced by both local ecology and stochastic factors such as genetic drift or founder events. Here, we use quantitative color measurements of males and females of Skyros wall lizard, Podarcis gaigeae, to demonstrate that this species is polymorphic with respect to throat color, and the morphs form discrete phenotypic clusters with limited overlap between categories. We use divergence in throat color morph frequencies and compare that to neutral genetic variation to infer the evolutionary processes acting on islet- and mainland populations.     

Eutrophication mediates rapid clonal evolution in Daphnia pulicaria

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The evolution of eye size in response to increased fish predation in Daphnia

Variation in eye size is ubiquitous across taxa. Increased eye size is correlated with improved vision and increased fitness via shifts in behavior. Tests of the drivers of eye size evolution have focused on macroevolutionary studies evaluating the importance of light availability. Predator‐induced mortality has recently been identified as a potential driver of eye size variation. Here, we tested the influence of increased predation by the fish predator, the alewife (Alosa pseudoharengus) on eye size evolution in waterfleas (Daphnia ambigua) from lakes in Connecticut. We quantified the relative eye size of Daphnia from lakes with and without alewife using wild‐caught and third‐generation laboratory reared specimens. This includes comparisons between lakes where alewife are present seasonally (anadromous) or permanently (landlocked). Wild‐caught specimens did not differ in eye size across all lakes. However, third‐generation lab reared Daphnia from lakes with alewife, irrespective of the form of alewife predation, exhibited significantly larger eyes than Daphnia from lakes without alewife. This genetically based increase in eye size may enhance the ability of Daphnia to detect predators. Alternatively, such shifts in eye size may be an indirect response to Daphnia aggregating at the bottom of lakes. To test these mechanisms, we collected Daphnia as a function of depth and found that eye size differed in Daphnia found at the surface versus the bottom of the water column between anadromous alewife and no alewife lakes. However, we found no evidence of Daphnia aggregating at the bottom of lakes. Such results indicate that the evolution of a larger eye may be explained by a connection between eyes and enhanced survival. We discuss the cause of the lack of concordance in eye size variation between our phenotypic and genetic specimens and the ultimate drivers of eye size.     

When and how can <Emphasis Type="Italic">Daphnia</Emphasis> prepare their offspring for the threat of predation?

The life history of Daphnia exposed to fish kairomone at different developmental stages was examined in a laboratory experiment. The strongest life history response to the applied predation threat was observed in females exposed during the 4th instar. Compared to Daphnia experiencing the presence of fish at earlier or later instars, these individuals reached maturity at a smaller size and released fewer neonates. Moreover, their offspring also demonstrated the strongest reaction to predation threat, exhibiting the broadest phenotypic plasticity in the life history response to predation. The breadth of their reaction norm was, on average, two times larger comparing with individuals from other treatments. Broader phenotypic plasticity may offer clear selective advantages under the unpredictable predation regime. This finding highlights the adaptive role of maternal effect in shaping life history of cladocerans.