The evolution of vertebrate eye size across an environmental gradient: phenotype does not predict genotype in a Trinidadian killifish

Vertebrates exhibit substantial variation in eye size. Eye size correlates positively with visual capacity and behaviors that enhance fitness, such as predator avoidance. This foreshadows a connection between predation and eye size evolution. Yet, the conditions that favor evolutionary shifts in eye size, besides the well‐known role for light availability, are unclear. We tested the influence of predation on the evolution of eye size in Trinidadian killifish, Rivulus hartii. Rivulus are located across a series of communities where they coexist with visually oriented piscivores ("high predation" sites), and no predators (“Rivulus‐only” sites). Wild‐caught Rivulus from high predation sites generally exhibited a smaller relative eye size than communities that lack predators. Yet, such differences were inconsistent across rivers. Second‐generation common garden reared fish revealed repeatable decreases in eye size in Rivulus from high predation sites. We performed additional experiments that tested the importance of light and resources on eye size evolution. Sites that differ in light or resource availability did not differ in eye size. Our results argue that differences in predator‐induced mortality underlie genetically‐based shifts in vertebrate eye size. We discuss the drivers of eye size evolution in light of the nonparallel trends between the phenotypic and common garden results.     

Transplant experiments demonstrate that larger brains are favoured in high-competition environments in Trinidadian killifish

The extent to which the evolution of a larger brain is adaptive remains controversial. Trinidadian killifish (Anablepsoides hartii) are found in sites that differ in predation intensity; fish that experience decreased predation and increased intraspecific competition exhibit larger brains. We evaluated the connection between brain size and fitness (survival and growth) when killifish are found in their native habitats and when fish are transplanted from sites with predators to high-competition sites that lack predators. Selection for a larger brain was absent within locally adapted populations. Conversely, there was a strong positive relationship between brain size and growth in transplanted but not resident fish in high-competition environments. We also observed significantly larger brain sizes in the transplanted fish that were recaptured at the end of the experiment versus those that were not. Our results provide experimental support that larger brains increase fitness and are favoured in high-competition environments.     

Increased juvenile predation is not associated with evolved differences in adult brain size in Trinidadian killifish (Rivulus hartii)

Vertebrates exhibit extensive variation in brain size. The long‐standing assumption is that this variation is driven by ecologically mediated selection. Recent work has shown that an increase in predator‐induced mortality is associated with evolved increases and decreases in brain size. Thus, the manner in which predators induce shifts in brain size remains unclear. Increased predation early in life is a key driver of many adult traits, including life‐history and behavioral traits. Such results foreshadow a connection between age‐specific mortality and selection on adult brain size. Trinidadian killifish, Rivulus hartii, are found in sites with and without guppies, Poecilia reticulata. The densities of Rivulus drop dramatically in sites with guppies because guppies prey upon juvenile Rivulus. Previous work has shown that guppy predation is associated with the evolution of adult life‐history traits in Rivulus. In this study, we compared second‐generation laboratory‐born Rivulus from sites with and without guppies for differences in brain size and associated trade‐offs between brain size and other components of fitness. Despite the large amount of existing research on the importance of early‐life events on the evolution of adult traits, and the role of predation on both behavior and brain size, we did not find an association between the presence of guppies and evolutionary shifts in Rivulus brain size. Such results argue that increased rates of juvenile mortality may not alter selection on adult brain size.     

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.     

Effects of Hatchery Rearing on Brain Structures of Rainbow Trout, Oncorhynchus mykiss

In this study, we contrast brain morphology from hatchery and wild reared stocks to examine the hypothesis that in salmonid fishes, captive rearing produces changes in brain development. Using rainbow trout, Oncorhynchus mykiss, as a model, we measured eight regions of the salmonid brain to examine differences between wild and hatchery reared fish. We find using multiple analysis of covariance (MANCOVA), analysis of covariance (ANCOVA) and discriminant function analysis (DFA) that the brains of hatchery reared fish are relatively smaller in several critical measures than their wild counterparts. Our work may suggest a mechanistic basis for the observed vulnerability of hatchery fish to predation and their general low survival upon release into the wild. Our results are the first to highlight the effects of hatchery rearing on changes in brain development inbreak fishes.     

Adaptive evolution to novel predators facilitates the evolution of damselfly species range shifts

Most species have evolved adaptations to reduce the chances of predation. In many cases, adaptations to coexist with one predator generate tradeoffs in the ability to live with other predators. Consequently, the ability to live with one predator may limit the geographic distributions of species, such that adaptive evolution to coexist with novel predators may facilitate range shifts. In a case study with Enallagma damselflies, we used a comparative phylogenetic approach to test the hypothesis that adaptive evolution to live with a novel predator facilitates range size shifts. Our results suggest that the evolution of Enallagma shifting from living in ancestral lakes with fish as top predators, to living in lakes with dragonflies as predators, may have facilitated an increase in their range sizes. This increased range size likely arose because lakes with dragonflies were widespread, but unavailable as a habitat throughout much of the evolutionary history of Enallagma because they were historically maladapted to coexist with dragonfly predators. Additionally, the traits that have evolved as defenses against dragonflies also likely enhanced damselfly dispersal abilities. While many factors underlie the evolutionary history of species ranges, these results suggest a role for the evolution of predator‐prey interactions.     

Predator–prey interactions,flight initiation distance and brain size

Prey avoid being eaten by assessing the risk posed by approaching predators and responding accordingly. Such an assessment may result in prey–predator communication and signalling, which entail further monitoring of the predator by prey. An early antipredator response may provide potential prey with a selective advantage, although this benefit comes at the cost of disturbance in terms of lost foraging opportunities and increased energy expenditure. Therefore, it may pay prey to assess approaching predators and determine the likelihood of attack before fleeing. Given that many approaching potential predators are detected visually, we hypothesized that species with relatively large eyes would be able to detect an approaching predator from afar. Furthermore, we hypothesized that monitoring of predators by potential prey relies on evaluation through information processing by the brain. Therefore, species with relatively larger brains for their body size should be better able to monitor the intentions of a predator, delay flight for longer and hence have shorter flight initiation distances than species with smaller brains. Indeed, flight initiation distances increased with relative eye size and decreased with relative brain size in a comparative study of 107 species of birds. In addition, flight initiation distance increased independently with size of the cerebellum, which plays a key role in motor control. These results are consistent with cognitive monitoring as an antipredator behaviour that does not result in the fastest possible, but rather the least expensive escape flights. Therefore, antipredator behaviour may have coevolved with the size of sense organs, brains and compartments of the brain involved in responses to risk of predation.     

Experimental test of the influence of light availability on the evolution of eye size and behaviour in Daphnia

There exists extensive variation in eye size. Much work has provided a connection between light availability and differences in eye size across taxa. Experimental tests of the role of the light environment on the evolution of eye size are lacking. Here, we performed a selection experiment that examined the influence of light availability on shifts in eye size and the connection between eye size and phototactic (anti-predator) behaviour in Daphnia. We set-up replicate experimental populations of Daphnia, repeatedly evaluated phenotypic shifts in eye size during the ~50-day experiment, and performed a common garden experiment at the end of the experiment to test for evolutionary shifts in eye size and behaviour. Our phenotypic analyses showed that eye size rapidly diverged between the light treatments; relative eye size was consistently larger in the low versus high light treatments. Selection on eye size was also modified by variation in density as increases in Daphnia density favoured a larger eye. However, we did not observe differences in eye size between the light treatments following two generations of common garden rearing at the end of the experiment. We instead observed strong shifts in anti-predator behaviour. Daphnia from the low light treatment exhibited decreased phototactic responses to light. Our results show that decreased light relaxes selection on anti-predator behaviour. Such trends provide new insights into selection on eye size and behaviour.     

Phylogenetics of pond and lake lifestyles in Chaoborus midge larvae

Abstract . Aquatic invertebrates experience strong trade-offs between habitats due to the selective effects of different predators. Diel vertical migration and small body size are thought to be effective strategies against fish predation in lakes. In the absence of fish in small ponds, migration is ineffective against invertebrate predators and large body size is an advantage. Although widely discussed, this phenomenon has never been tested in a phylogenetic context. We reconstructed a mitochondrial DNA (mtDNA) tree to investigate the phylogenetic distribution of pond and lake lifestyles among 10 species of northern temperate Chaoborus midge larvae. The mtDNA tree is similar to previous morphological trees for Chaoborus , the only difference being the disruption of the subgenus Chaoborus sensu stricto. At least three shifts have occurred between pond and lake lifestyles, each time associated with evolution of diel vertical migration in the lake taxon. The trend in larval body size with habitat type is sensitive to tree and character reconstruction methods, only weakly consistent with the effects of fish predation. Despite long time periods over which adaptation to each habitat type could have occurred, there remains significant phylogenetic heritability in larval body size. The tree provides a framework for comparative studies of the metapopulation genetic consequences of pond and lake lifestyles.     

Adaptive life-history evolution in the livebearing fish Brachyrhaphis rhabdophora: genetic basis for parallel divergence in age and size at maturity and a test of predator-induced plasticity

I document a genetic basis for parallel evolution of life-history phenotypes in the livebearing fish Brachyrhaphis rhabdophora from northwestern Costa Rica. In previous work, I showed that populations of B. rhabdophora that co-occur with predators attain maturity at smaller sizes than populations that live in predator-free environments. I also demonstrated that this pattern of phenotypic divergence in life histories was independently repeated in at least five isolated drainages. However, life-history phenotypes measured from wild-caught fish could be attributed to environmental effects rather than to genetic differences among populations. In the present study, I reared male fish from four populations (two that co-occur with predators and two from predator-free environments) under four sets of environmental conditions. The pattern of phenotypic divergence in maturation size documented in the field between populations collected from different predation environments persisted after two generations in the laboratory. I also found a genetic basis for differences between populations in the age at which males attain maturity and in growth rates. By rearing fish in four different common environments, I tested for phenotypic plasticity in male life-history traits in response to nonlethal exposure to predators. There was a significant delay in the onset of sexual maturity in fish exposed to predators relative to those in the control, but no differences among treatments in size at maturity or growth rates. These results, coupled with previous work on B. rhabdophora, demonstrate a repeated pattern of parallel evolutionary divergence among genetically isolated populations that is strongly associated with predation.     

DISTINCT EVOLUTIONARY PATTERNS OF BRAIN AND BODY SIZE DURING ADAPTIVE RADIATION

Morphological traits are often genetically and/or phenotypically correlated with each other and such covariation can have an important influence on the evolution of individual traits. The strong positive relationship between brain size and body size in vertebrates has attracted a lot of interest, and much debate has surrounded the study of the factors responsible for the allometric relationship between these two traits. Here, we use comparative analyses of the Tanganyikan cichlid adaptive radiation to investigate the patterns of evolution for brain size and body size separately. We found that body size exhibited recent bursts of rapid evolution, a pattern that is consistent with divergence linked to ecological specialization. Brain weight on the other hand, showed no bursts of divergence but rather evolved in a gradual manner. Our results thus show that even highly genetically correlated traits can present markedly different patterns of evolution, hence interpreting patterns of evolution of traits from correlations in extant taxa can be misleading. Furthermore, our results suggest, contrary to expectations from theory, that brain size does not play a key role during adaptive radiation.     

The potential influence of morphology on the evolutionary divergence of an acoustic signal

The evolution of acoustic behaviour and that of the morphological traits mediating its production are often coupled. Lack of variation in the underlying morphology of signalling traits has the potential to constrain signal evolution. This relationship is particularly likely in field crickets, where males produce acoustic advertisement signals to attract females by stridulating with specialized structures on their forewings. In this study, we characterize the size and geometric shape of the forewings of males from six allopatric populations of the black field cricket (Teleogryllus commodus) known to have divergent advertisement calls. We sample from each of these populations using both wild‐caught and common‐garden‐reared cohorts, allowing us to test for multivariate relationships between wing morphology and call structure. We show that the allometry of shape has diverged across populations. However, there was a surprisingly small amount of covariation between wing shape and call structure within populations. Given the importance of male size for sexual selection in crickets, the divergence we observe among populations has the potential to influence the evolution of advertisement calls in this species.     

Parallel and nonparallel behavioural evolution in response to parasitism and predation in Trinidadian guppies

Natural enemies such as predators and parasites are known to shape intraspecific variability of behaviour and personality in natural populations, yet several key questions remain: (i) What is the relative importance of predation vs. parasitism in shaping intraspecific variation of behaviour across generations? (ii) What are the contributions of genetic and plastic effects to this behavioural divergence? (iii) And to what extent are responses to predation and parasitism repeatable across independent evolutionary lineages? We addressed these questions using Trinidadian guppies (Poecilia reticulata) (i) varying in their exposure to dangerous fish predators and Gyrodactylus ectoparasites for (ii) both wild‐caught F0 and laboratory‐reared F2 individuals and coming from (iii) multiple independent evolutionary lineages (i.e. independent drainages). Several key findings emerged. First, a population's history of predation and parasitism influenced behavioural profiles, but to different extent depending on the behaviour considered (activity, shoaling or boldness). Second, we had evidence for some genetic effects of predation regime on behaviour, with differences in activity of F2 laboratory‐reared individuals, but not for parasitism, which had only plastic effects on the boldness of wild‐caught F0 individuals. Third, the two lineages showed a mixture of parallel and nonparallel responses to predation/parasitism, with parallel responses being stronger for predation than for parasitism and for activity and boldness than for shoaling. These findings suggest that different sets of behaviours provide different pay‐offs in alternative predation/parasitism environments and that parasitism has more transient effects in shaping intraspecific variation of behaviour than does predation.     

Body size determines eyespot size and presence in coral reef fishes

Numerous organisms display conspicuous eyespots. These eye‐like patterns have been shown to effectively reduce predation by either deflecting strikes away from nonvital organs or by intimidating potential predators. While investigated extensively in terrestrial systems, determining what factors shape eyespot form in colorful coral reef fishes remains less well known. Using a broadscale approach we ask: How does the size of the eyespot relate to the actual eye, and at what size during ontogeny are eyespots acquired or lost? We utilized publicly available images to generate a dataset of 167 eyespot‐bearing reef fish species. We measured multiple features relating to the size of the fish, its eye, and the size of its eyespot. In reef fishes, the area of the eyespot closely matches that of the real eye; however, the eyespots “pupil” is nearly four times larger than the real pupil. Eyespots appear at about 20 mm standard length. However, there is a marked decrease in the presence of eyespots in fishes above 48 mm standard length; a size which is tightly correlated with significant decreases in documented mortality rates. Above 75–85 mm, the cost of eyespots appears to outweigh their benefit. Our results identify a “size window” for eyespots in coral reef fishes, which suggests that eyespot use is strictly body size‐dependent within this group.     

EVOLUTION OF GIGANTISM IN NINE‐SPINED STICKLEBACKS

The relaxation of predation and interspecific competition are hypothesized to allow evolution toward “optimal” body size in island environments, resulting in the gigantism of small organisms. We tested this hypothesis by studying a small teleost (nine‐spined stickleback, Pungitius pungitius) from four marine and five lake (diverse fish community) and nine pond (impoverished fish community) populations. In line with theory, pond fish tended to be larger than their marine or lake conspecifics, sometimes reaching giant sizes. In two geographically independent cases when predatory fish had been introduced into ponds, fish were smaller than those in nearby ponds lacking predators. Pond fish were also smaller when found in sympatry with three‐spined stickleback (Gasterosteus aculeatus) than those in ponds lacking competitors. Size‐at‐age analyses demonstrated that larger size in ponds was achieved by both increased growth rates and extended longevity of pond fish. Results from a common garden experiment indicate that the growth differences had a genetic basis: pond fish developed two to three times higher body mass than marine fish during 36 weeks of growth under similar conditions. Hence, reduced risk of predation and interspecific competition appear to be chief forces driving insular body size evolution toward gigantism.     

PREDATOR‐DRIVEN TRAIT DIVERSIFICATION IN A DRAGONFLY GENUS: COVARIATION IN BEHAVIORAL AND MORPHOLOGICAL ANTIPREDATOR DEFENSE

Proof for predation as an agent shaping evolutionary trait diversification is accumulating, however, our understanding how multiple antipredator traits covary due to phenotypic differentiation is still scarce. Species of the dragonfly genus Leucorrhinia underwent shifts from lakes with fish as top predators to fishless lakes with large dragonfly predators. This move to fishless lakes was accompanied by a partial loss and reduction of larval spines. Here, we show that Leucorrhinia also reduced burst swimming speed and its associated energy fuelling machinery, arginine kinase activity, when invading fishless lakes. This results in patterns of positive phylogenetic trait covariation between behavioral and morphological antipredator defense (trait cospecialization) and between behavioral antipredator defense and physiological machinery (trait codependence). Across species patterns of trait covariation between spine status, burst swimming speed and arginine kinase activity also matched findings within the phenotypically plastic L. dubia. Our results highlight the importance of predation as a factor affecting patterns of multiple trait covariation during phenotypic diversification.     

Habitat-dependent and -independent plastic responses to social environment in the nine-spined stickleback (Pungitius pungitius) brain

The influence of environmental complexity on brain development has been demonstrated in a number of taxa, but the potential influence of social environment on neural architecture remains largely unexplored. We investigated experimentally the influence of social environment on the development of different brain parts in geographically and genetically isolated and ecologically divergent populations of nine-spined sticklebacks (Pungitius pungitius). Fish from two marine and two pond populations were reared in the laboratory from eggs to adulthood either individually or in groups. Group-reared pond fish developed relatively smaller brains than those reared individually, but no such difference was found in marine fish. Group-reared fish from both pond and marine populations developed larger tecta optica and smaller bulbi olfactorii than individually reared fish. The fact that the social environment effect on brain size differed between marine and pond origin fish is in agreement with the previous research, showing that pond fish pay a high developmental cost from grouping while marine fish do not. Our results demonstrate that social environment has strong effects on the development of the stickleback brain, and on the brain''s sensory neural centres in particular. The potential adaptive significance of the observed brain-size plasticity is discussed.     

Evolution of pleiotropic alleles for maturation and size as a consequence of predation

Understanding life-history evolution requires knowledge about genetic interactions, physiological mechanisms and the nature of selection. For platyfish, Xiphophorus maculatus, extensive information is available about genetic and physiological mechanisms influencing life-history traits. In particular, alleles at the pituitary locus have large and antagonistic effects on age and size at sexual maturation. To examine how predation affects the evolution of these antagonistic traits, I examined pituitary allele evolution in experimental populations differing in predation risk. A smaller size, earlier maturation allele increased in frequency when predators were absent, while a larger size, later maturation allele increased in frequency when predators were present. Thus, predation favours alleles for larger size, at the cost of later maturation and reproduction. These findings are interesting for several reasons. First, predation is often predicted to favour early reproduction at smaller sizes. Second, few studies have shown how selection acts on alleles that affect age and size at sexual maturation. Finally, many studies assume that trade-offs between these life-history traits result from antagonistic pleiotropy, with alleles that positively affect one trait negatively affecting another, yet this is rarely known. This study unequivocally demonstrates that genetically based trade-offs affect life-history evolution in platyfish.     

Brain development and predation: plastic responses depend on evolutionary history

Although the brain is known to be a very plastic organ, the effects of common ecological interactions like predation or competition on brain development have remained largely unexplored. We reared nine-spined sticklebacks (Pungitius pungitius) from two coastal marine (predation-adapted) and two isolated pond (competition-adapted) populations in a factorial experiment, manipulating perceived predatory risk and food supply to see (i) if the treatments affected brain development and (ii) if there was population differentiation in the response to treatments. We detected differences in plasticity of the bulbus olfactorius (chemosensory centre) between habitats: marine fish were not plastic, whereas pond fish had larger bulbi olfactorii in the presence of perceived predation. Marine fish had larger bulbus olfactorius overall. Irrespective of population origin, the hypothalamus was smaller in the presence of perceived predatory risk. Our results demonstrate that perceived predation risk can influence brain development, and that the effect of an environmental factor on brain development may depend on the evolutionary history of a given population in respect to this environmental factor.     

Evolution of eye size and shape in primates

Strepsirrhine and haplorhine primates exhibit highly derived features of the visual system that distinguish them from most other mammals. Comparative data link the evolution of these visual specializations to the sequential acquisition of nocturnal visual predation in the primate stem lineage and diurnal visual predation in the anthropoid stem lineage. However, it is unclear to what extent these shifts in primate visual ecology were accompanied by changes in eye size and shape. Here we investigate the evolution of primate eye morphology using a comparative study of a large sample of mammalian eyes. Our analysis shows that primates differ from other mammals in having large eyes relative to body size and that anthropoids exhibit unusually small corneas relative to eye size and body size. The large eyes of basal primates probably evolved to improve visual acuity while maintaining high sensitivity in a nocturnal context. The reduced corneal sizes of anthropoids reflect reductions in the size of the dioptric apparatus as a means of increasing posterior nodal distance to improve visual acuity. These data support the conclusion that the origin of anthropoids was associated with a change in eye shape to improve visual acuity in the context of a diurnal predatory habitus.