The influence of predator community composition on photoprotective traits of copepods

Trait expression of natural populations often jointly depends on prevailing abiotic environmental conditions and predation risk. Copepods, for example, can vary their expression of compounds that confer protection against ultraviolet radiation (UVR), such as astaxanthin and mycosporine‐like amino acids (MAAs), in relation to predation risk. Despite ample evidence that copepods accumulate less astaxanthin in the presence of predators, little is known about how the community composition of planktivorous fish can affect the overall expression of photoprotective compounds. Here, we investigate how the (co‐)occurrence of Arctic charr (Salvelinus alpinus) and threespine stickleback (Gasterosteus aculeatus) affects the photoprotective phenotype of the copepod Leptodiaptomus minutus in lake ecosystems in southern Greenland. We found that average astaxanthin and MAA contents were lowest in lakes with stickleback, but we found no evidence that these photoprotective compounds were affected by the presence of charr. Furthermore, variance in astaxanthin among individual copepods was greatest in the presence of stickleback and the astaxanthin content of copepods was negatively correlated with increasing stickleback density. Overall, we show that the presence and density of stickleback jointly affect the content of photoprotective compounds by copepods, illustrating how the community composition of predators in an ecosystem can determine the expression of prey traits that are also influenced by abiotic stressors.     

Frequency dependent natural selection during character displacement in sticklebacks

Abstract We know little about how natural selection on a species is altered when a closely related species consuming similar resources appears in its environment. In a pond experiment with threespine sticklebacks I tested the prediction that divergent natural selection between competitors is frequency-dependent, changing with the distribution of phe-notypes in the environment. Differential growth and survival of phenotypes in a target stickleback population were contrasted between two treatments. In one treatment an offshore zooplankton feeder (the limnetic stickleback species) was added to the same pond as the target. In the other treatment I added the benthic stickleback instead, a species adapted to feeding on invertebrates from sediments and inshore vegetation. The target population was ecologically and morphologically intermediate with phenotypic variance artificially inflated by hybridization. Growth rates of phenotypes within the target population differed between treatments as predicted by character displacement. The impact of adding a second species always fell most heavily on those phenotypes in the target population resembling the added species most closely. However, those individuals in the target population that most resembled the added species did not experience reduced survival. Instead, consistent survival differences between populations suggested the presence of an inshore –offshore gradient in mortality risk. These results provide further support for the hypothesis of character displacement in sympatric sticklebacks. They suggest that displacement along the resource gradient also led to divergence in vulnerability to agents of mortality, probably including predation.     

BODY SIZE,NATURAL SELECTION,AND SPECIATION IN STICKLEBACKS

There is little evidence from nature that divergent natural selection is crucial to speciation. However, divergent selection is implicated if traits conferring adaptation to alternative environments also form the basis of reproductive isolation. We tested the importance of body size differences to premating isolation between two sympatric sticklebacks. The species differ greatly in size, and several lines of evidence indicate that this difference is an adaptation to alternative foraging habitats. Strong assortative mating was evident in laboratory trials, but a few hybridization events occurred. Probability of interspecific mating was strongly correlated with body size: interspecific spawning occurred only between the largest individuals of the smaller species and the smallest individuals of the larger species. Probability of spawning between similar-sized individuals from different species was comparable to spawning rates within species. Disruption of mating between individuals from different species can be traced to increased levels of male aggression and decreased levels of male courtship as size differences increased between paired individuals. Interspecific mate preferences in sympatric sticklebacks appears to be dominated by body size, implicating natural selection in the origin of species.     

Modular Skeletal Evolution in Sticklebacks Is Controlled by Additive and Clustered Quantitative Trait Loci

Understanding the genetic architecture of evolutionary change remains a long-standing goal in biology. In vertebrates, skeletal evolution has contributed greatly to adaptation in body form and function in response to changing ecological variables like diet and predation. Here we use genome-wide linkage mapping in threespine stickleback fish to investigate the genetic architecture of evolved changes in many armor and trophic traits. We identify >100 quantitative trait loci (QTL) controlling the pattern of serially repeating skeletal elements, including gill rakers, teeth, branchial bones, jaws, median fin spines, and vertebrae. We use this large collection of QTL to address long-standing questions about the anatomical specificity, genetic dominance, and genomic clustering of loci controlling skeletal differences in evolving populations. We find that most QTL (76%) that influence serially repeating skeletal elements have anatomically regional effects. In addition, most QTL (71%) have at least partially additive effects, regardless of whether the QTL controls evolved loss or gain of skeletal elements. Finally, many QTL with high LOD scores cluster on chromosomes 4, 20, and 21. These results identify a modular system that can control highly specific aspects of skeletal form. Because of the general additivity and genomic clustering of major QTL, concerted changes in both protective armor and trophic traits may occur when sticklebacks inherit either marine or freshwater alleles at linked or possible “supergene” regions of the stickleback genome. Further study of these regions will help identify the molecular basis of both modular and coordinated changes in the vertebrate skeleton.     

Innate versus adaptive immunity in sticklebacks: evidence for trade-offs from a selection experiment

In vertebrates, the immune system consists of two arms of different characteristics: the innate and the acquired immune response. Parasites that are only shortly exposed to the immune system are most efficiently attacked by fast, constitutive innate immune mechanisms. Here, we experimentally selected within four fish families for high innate resistance versus susceptibility of three-spined sticklebacks (Gasterosteus aculeatus) against infection with the eye-fluke (Diplostomum pseudospathacaeum), a parasite whose metacercariae are protected from the immune system within the eye lens. We predicted that in families with high susceptibility, the adaptive immune system would be upregulated when challenged with infection. In accordance, we found that MHC class IIB expression is increased by approximately 50% in those lines selected for higher parasite load (i.e. low innate response). This suggests extensive genetic correlations between innate and adaptive immune system and/or crosstalk between both lines of defense. An efficient, specific innate immune response might reduce overall activation of the immune system and potentially alleviate associated effects of immunopathology.     

Nutritional state influences shoaling preference for familiars

Preferences for grouping with familiar individuals are shown in many animal species, including the three-spined stickleback (Gasterosteus aculeatus). Shoaling with familiars is advantageous because of more precise anti-predator behaviours or more stable dominance hierarchies. Additionally, associations with familiar individuals facilitate the evolution of altruistic behaviour. Thus, in situations of increased competition one might expect an increased preference for familiar fish. We gave single juvenile sticklebacks of different nutritional state the choice between shoals composed either of familiar or unfamiliar individuals. Satiated fish preferred to shoal with familiar individuals. A comparative analysis of 8 stickleback studies with 15 different tests using familiars showed that all tests gave similar results, i.e. sticklebacks of all age classes preferred to shoal with familiars in a non-sexual context. In contrast, hungry test fish did not prefer to shoal with familiar fish, but even showed a preference for the unfamiliar group. Because sticklebacks use early-life familiarity to recognize kin, the results suggest the avoidance of competition with relatives. To our knowledge, this is the first study showing an impact of nutritional state on social interactions with familiar individuals.     

The influence of turbidity on three-spined stickleback foraging

Three-spined sticklebacks Gasterosteus aculeatus were used as a model to test for the effects of turbidity on visual-predator foraging. While the number of feeding lunges and number of prey consumed did not change with increasing turbidity, reactive distance to prey decreased.