Harvest selection on Atlantic cod behavioral traits: implications for spatial management

Harvesting wild populations may contrast or reinforce natural agents of selection and potentially cause evolutionary changes in life-history traits such as growth and maturation. Harvest selection may also act on behavioral traits, although this field of research has so far received less attention. We used acoustic tags and a network of receivers to monitor the behavior and fate of individual Atlantic cod (Gadus morhua, N = 60) in their natural habitat on the Norwegian Skagerrak coast. Fish with a strong diel vertical migration, alternating between shallow- and deep-water habitats, had a higher risk of being captured in the fishery (traps, gillnet, hand line) as compared to fish that stayed in deeper water. There was also a significant negative correlation between fish size (30-66 cm) and the magnitude of diel vertical migration. Natural selection on behavior was less clear, but tended to favor fish with a large activity space. On a monthly time scale we found significant repeatabilities for cod behavior, meaning that individual characteristics tended to persist and therefore may be termed personality traits. We argue that an evolutionary approach to fisheries management should consider fish behavior. This would be of particular relevance for spatial management actions such as marine reserve design.     

Selection and genetic drift in captive versus wild populations: an assessment of neutral and adaptive (MHC-linked) genetic variation in wild and hatchery brown trout (<Emphasis Type="Italic">Salmo trutta</Emphasis>) populations

Captive bred individuals are often released into natural environments to supplement resident populations. Captive bred salmonid fishes often exhibit lower survival rates than their wild brethren and stocking measures may have a negative influence on the overall fitness of natural populations. Stocked fish often stem from a different evolutionary lineage than the resident population and thus may be maladapted for life in the wild, but this phenomenon has also been linked to genetic changes that occur in captivity. In addition to overall loss of genetic diversity via captive breeding, adaptation to captivity has become a major concern. Altered selection pressure in captivity may favour alleles at adaptive loci like the Major Histocompatibility Complex (MHC) that are maladaptive in natural environments. We investigated neutral and MHC-linked genetic variation in three autochthonous and three hatchery populations of Austrian brown trout (Salmo trutta). We confirm a positive selection pressure acting on the MHC II β locus, whereby the signal for positive selection was stronger in hatchery versus wild populations. Additionally, diversity at the MHC II β locus was higher, and more uniform among hatchery samples compared to wild populations, despite equal levels of diversity at neutral loci. We postulate that this stems from a combination of stronger genetic drift and a weakening of positive selection at this locus in wild populations that already have well adapted alleles for their specific environments.     

Patterns of natural selection on morphology of male and female collared flycatchers (Ficedula albicollis)

Natural selection may act in different directions among years, life stages, or classes of individuals. Fluctuating selection of this kind is potentially an important mechanism by which additive genetic variation for quantitative traits is maintained, and can prevent populations reaching local adaptive peaks. We analysed natural selection acting on three morphological traits of male and female collared flycatchers via both fecundity and survival, using 15 years' data from a large isolated population on Godand, Sweden. We particularly investigated variation in the direction and magnitude of selection acting: (1) among years over the study period; (2) on different life stages and (3) the consistency of observed patterns of selection with sexual size dimorphism (SSD) in this population. We found little evidence of natural selection on these traits over the study period. Evidence for directional, stabilizing and disruptive selection was found for some year-trait combinations, but these patterns were inconsistent with respect to both the magnitude and form of selection found. Consequently, our results, based on the detailed analysis of natural selection in a large wild population over a period of 15 years, provide evidence for the common assumption that forces of selection acting on quantitative traits are generally weak. They are also consistent with the suggestion that environmental stability is an important determinant of the degree to which organisms fit their environment.     

Harvest-induced disruptive selection increases variance in fitness-related traits

The form of Darwinian selection has important ecological and management implications. Negative effects of harvesting are often ascribed to size truncation (i.e. strictly directional selection against large individuals) and resultant decrease in trait variability, which depresses capacity to buffer environmental change, hinders evolutionary rebound and ultimately impairs population recovery. However, the exact form of harvest-induced selection is generally unknown and the effects of harvest on trait variability remain unexplored. Here we use unique data from the Windermere (UK) long-term ecological experiment to show in a top predator (pike, Esox lucius) that the fishery does not induce size truncation but disruptive (diversifying) selection, and does not decrease but rather increases variability in pike somatic growth rate and size at age. This result is supported by complementary modelling approaches removing the effects of catch selectivity, selection prior to the catch and environmental variation. Therefore, fishing most likely increased genetic variability for somatic growth in pike and presumably favoured an observed rapid evolutionary rebound after fishery relaxation. Inference about the mechanisms through which harvesting negatively affects population numbers and recovery should systematically be based on a measure of the exact form of selection. From a management perspective, disruptive harvesting necessitates combining a preservation of large individuals with moderate exploitation rates, and thus provides a comprehensive tool for sustainable exploitation of natural resources.     

When bigger is not better: selection against large size, high condition and fast growth in juvenile lemon sharks

Selection acting on large marine vertebrates may be qualitatively different from that acting on terrestrial or freshwater organisms, but logistical constraints have thus far precluded selection estimates for the former. We overcame these constraints by exhaustively sampling and repeatedly recapturing individuals in six cohorts of juvenile lemon sharks (450 age-0 and 255 age-1 fish) at an enclosed nursery site (Bimini, Bahamas). Data on individual size, condition factor, growth rate and inter-annual survival were used to test the 'bigger is better', 'fatter is better' and 'faster is better' hypotheses of life-history theory. For age-0 sharks, selection on all measured traits was weak, and generally acted against large size and high condition. For age-1 sharks, selection was much stronger, and consistently acted against large size and fast growth. These results suggest that selective pressures at Bimini may be constraining the evolution of large size and fast growth, an observation that fits well with the observed small size and low growth rate of juveniles at this site. Our results support those of some other recent studies in suggesting that bigger/fatter/faster is not always better, and may often be worse.     

Postcopulatory fertilization bias as a form of cryptic sexual selection

Males and females share most of their genetic material yet often experience very different selection pressures. Some traits that are adaptive when expressed in males may therefore be maladaptive when expressed in females. Recent studies demonstrating negative correlations in fitness between parents and their opposite-sex progeny suggest that natural selection may favor a reduction in trait correlations between the sexes to partially mitigate intralocus sexual conflict. We studied sex-specific forms of selection acting in Anolis lizards in the Greater Antilles, a group for which the importance of natural selection has been well documented in species-level diversification, but for which less is known about sexual selection. Using the brown anole (Anolis sagrei), we measured fitness-related variation in morphology (body size), and variation in two traits reflecting whole animal physiological condition: running endurance and immune function. Correlations between body size and physiological traits were opposite between males and females and the form of natural selection acting on physiological traits significantly differed between the sexes. Moreover, physiological traits in progeny were correlated with the body-size of their sires, but correlations were null or even negative between parents and their opposite-sex progeny. Although results based on phenotypic and genetic correlations, as well as the action of natural selection, suggest the potential for intralocus sexual conflict, females used sire body size as a cue to sort sperm for the production of either sons or daughters. Our results suggest that intralocus sexual conflict may be at least partly resolved through post-copulatory sperm choice in A. sagrei.     

The adaptive value of phenotypic floral integration

Floral integration has been deemed an adaptation to increase the benefits of animal pollination, yet no attempts have been made to estimate its adaptive value under natural conditions. Here, the variation in the magnitude and pattern of phenotypic floral integration and the variance-covariance structure of floral traits in four species of Rosaceae were examined. The intensity of natural selection acting on floral phenotypic integration was also estimated and the available evidence regarding the magnitude of floral integration reviewed. The species studied had similar degrees of floral integration, although significant differences were observed in their variance-covariance structure. Selection acted on subsets of floral traits (i.e. selection on intrafloral integration) rather than on the integration of the whole flower. Average integration was 20% and similar to the estimated mean value of flowering plants. The review indicated that flowering plants present lower integration than expected by chance. Numerical simulations suggest that this pattern may result from selection favouring intrafloral integration. Phenotypic integration at the flower level seems to have a low adaptive value among the species surveyed. Moreover, it is proposed that pollinator-mediated selection promotes the evolution of intrafloral integration.     

Nine decades of decreasing phenotypic variability in Atlantic cod

Changes in phenotypic variability in natural populations have received little attention in comparison with changes in mean trait values. This is unfortunate because trait diversity may influence adaptive evolutionary change and population stability. We combine two unique data sets to illuminate complex trait changes in Atlantic cod along the Norwegian Skagerrak coast: (i) an annual beach seine survey starting in 1919, monitoring juvenile body size and abundance and (ii) capture–mark–recapture data from which we estimated selection on juvenile body size and growth. We demonstrate that the variability of juvenile size has been steadily decreasing across nine decades, with no evidence for a similar trend in mean size. We also report that small, slow-growing fish as well as large, fast-growing fish are selected against. Together, these results suggest long-term stabilizing selection acting on Atlantic cod, and emphasize the need for further studies evaluating the full complexity of trait changes in wild populations.     

Harvest selection on multiple traits in the wild revealed by aquatic animal telemetry

Harvesting can have profound impacts on the ecology and evolution of marine populations. However, little is known about the strength and direction of fisheries‐induced selection acting on multiple traits in the wild. Here, we used acoustic telemetry to directly monitor individual behavior and fate in an intensively harvested species, the European lobster (Homarus gammarus, n = 100), in southern Norway. Overall, 24% of the tracked lobsters survived the two‐month harvest season within the study area. Our results indicated that local survival was not random with respect to phenotype. We found no clear support for fisheries‐induced selection acting directly on body size. However, lobsters with large crusher claws relative to their body size, typical of socially dominant individuals, appeared at higher risk of being captured in the conventional trap fishery. We also detected a fine‐scale spatial gradient in survival. After accounting for this gradient, individuals displaying larger home ranges were more likely to survive the harvest season. Finally, we found significant repeatabilities for lobster behavior on a monthly timescale, indicating that individual behavioral attributes tended to persist and may reflect personality. Our study therefore provides empirical support for the need to consider an evolutionary enlightened approach to fisheries management that considers the influence of harvest on multiple traits of target species.     

Spatio-temporal variation of natural and sexual selection in breeding populations of the coreid bug,Colpula lativentris (Heteroptera: Coreidae)

Spatio-temporal variations of lifetime reproductive succes (LRS) of both male and female individuals of a coreid bugColpula lativentris were measured and analyzed using the multiple regression method of Arnold and Wade (1984a, b). The standardized variance of LRS was larger in males than that in females as males often to secure mates for a long period whereas females could easily find mates and oviposit simply dependent on ovarial maturation. LRS was partitioned into 4 consecutive fitness components: (1) reproductive lifespan, (2) copulating efficiency, (3) guarding efficiency (for males) or oviposition efficiency (for females), and (4) number of eggs per clutch. In males copulating efficiency was the largest determining factor of LRS, whereas in females reproductive lifespan was the most important factor. Such tendencies were stable on both a yearly and local basis. Patterns of relative contribution of natural selection (reproductive lifespan and number of eggs per clutch) and sexual selection (copulating efficiency and guarding or oviposition efficiency) to LRS were clearly different between males and females. This sexual difference is, at least to some extent, thought to be brought about by sexual selection among males for mating opportunity, though no physical fight was observed among males. Directional selection on body length was found only in relation to the clutch size of females because large females tended to lay larger clutches. No significant directional selection was found in other fitness components.     

Onset of maturity and cohort composition at spawning of Baltic sprat Sprattus sprattus on the basis of otolith macrostructure analysis

Data on catch per unit effort (CPUE) from the Danish commercial fishery showed dense aggregations of sprat Sprattus sprattus born in 1997 in the main spawning area of the Baltic Sea during May 1999. After the analysis of their otolith macrostructure, these fish were found to have a shorter distance to the beginning of the first winter zone compared to fish from the same cohort caught in other months. At the same time, the number of fish with large otoliths at the period of winter zone formation tended to decrease or even disappear. The otolith size at winter zone formation ( O _W) was found to be a good predictor of sprat total length ( L _T) and mass ( M ) in age group 0 years. Changes in the otolith size distribution over time were related to variations in cohort composition depending on the L _T and M attained during the juvenile stage. Examination of the gonads suggested two life history patterns: 1) individuals achieving a larger L _T and M during the first growing season may contribute at age 1 years to the spawning stock and the fishery, whereas 2) individuals attaining smaller L _T and M contribute in larger amounts to both the spawning stock and the fishery later, when they are at age 2 years. Moreover, changes in the relationship between O _W and L _T and M were related to differences in growth trajectories for sprat born during the same spawning season. Smaller sprat as group 0 years continued growing during the second growing season delaying maturity compared to larger individuals from the same cohort.     

Haplotype-based inference of the distribution of fitness effects

Recent genome sequencing studies with large sample sizes in humans have discovered a vast quantity of low-frequency variants, providing an important source of information to analyze how selection is acting on human genetic variation. In order to estimate the strength of natural selection acting on low-frequency variants, we have developed a likelihood-based method that uses the lengths of pairwise identity-by-state between haplotypes carrying low-frequency variants. We show that in some nonequilibrium populations (such as those that have had recent population expansions) it is possible to distinguish between positive or negative selection acting on a set of variants. With our new framework, one can infer a fixed selection intensity acting on a set of variants at a particular frequency, or a distribution of selection coefficients for standing variants and new mutations. We show an application of our method to the UK10K phased haplotype dataset of individuals.     

Prehistoric versus modern Baltic Sea cod fisheries: selectivity across the millennia

Combining Stone Age and modern data provides unique insights for management, extending beyond contemporary problems and shifting baselines. Using fish chronometric parts, we compared demographic characteristics of exploited cod populations from the Neolithic Period (4500 BP) to the modern highly exploited fishery in the central Baltic Sea. We found that Neolithic cod were larger (mean 56.4 cm, 95% confidence interval (CI)+/-0.9) than modern fish (weighted mean length in catch =49.5+/-0.2 cm in 1995, 48.2+/-0.2 cm in 2003), and older (mean ages=4.7+/-0.11, 3.1+/-0.02 and 3.6+/-0.02 years for Neolithic, 1995, and 2003 fisheries, respectively). Fishery-independent surveys in 1995 and 2003 show that mean sizes in the stock are 16-17 cm smaller than reflected in the fishery, and mean ages approximately 1-1.5 years younger. Modelled von Bertalanffy growth and back-calculated lengths indicated that Neolithic cod grew to smaller asymptotic lengths, but were larger at younger ages, implying rapid early growth. Very small Neolithic cod were absent and large individuals were rare as in modern times. This could be owing to selective harvests, the absence of small and large fish in the area or a combination. Comparing modern and prehistoric times, fishery selection is evident, but apparently not as great as in the North Atlantic proper.     

Scaling of Size and Dimorphism in Primates II: Macroevolution

Previous researchers found positive scaling of body size and sexual size dimorphism (SSD) in primates, known as Rensch's rule. The pattern is present in Haplorhini, but absent in Strepsirhini. I found that positive evolutionary correlations between size and SSD drive positive scaling relationships within Haplorhini as a whole and Platyrrhini, Cercopithecinae, Colobinae, and Hominoidea individually at the generic level and higher, but that evolutionary correlations within genera in these clades are often nonsignificant or negative. I suggest that positive evolutionary correlations result from greater change in male than in female size, usually because of sexual selection acting on polygynous populations. I suggest that negative evolutionary correlations result from greater change in female size, owing to either natural selection or, in Callitrichidae, sexual selection acting on polyandrous populations. The high incidence of negative evolutionary correlations within Haplorhini suggests a relatively large influence of natural selection on SSD, at least with regard to differences in SSD between congeners. I propose two possible explanations for the difference in intrageneric and supergeneric evolutionary patterns: 1) natural selection is a relatively weak force for modifying SSD and has a noticeable effect only when one compares related species experiencing similar levels of sexual selection, and 2) natural selection is a relatively strong force for modifying SSD but is less likely than sexual selection to affect higher level taxonomic comparisons noticeably because of the cumulative effect over time of marginal differences in mortality rates of these two types of selection. I discuss types of data required to test these explanations and implications for reconstructing fossil behavior.     

Lake Victoria fisheries: the Kenyan reality and environmental implications

Synopsis The introduction of the Nile perch into Lake Victoria has dramatically altered the fishery in that lake and contributed to the decline of the fishery for indigenous tilapias. One sector of the fishery in Lake Victoria has benefitted from the Nile perch introduction, although catches have declined in recent years. Inefficient enforcement of fisheries regulations has had a detrimental effect on indigenous species but may also have contributed to the recent decline in Nile perch catches. Fisheries development plans have tended to favour capital-intensive fisheries and to ignore small scale subsistence fisheries. A case study at Wichlum Beach on the Kenyan shores of Lake Victoria has revealed the efficiency of traditional fishing and fish drying methods as well as the high ecological costs of the practice of kiln-drying Nile perch. Forty-five tons of firewood are used per month at Wichlum Beach alone for kiln-drying perch. The increased economic viability of the fishery has attracted professionals into the industry and resulted in the development of an export-oriented trade. The Yala Swamp adjacent to Lake Victoria has been extensively drained as part of a large land reclamation scheme and more draining is planned. Increased environmental awareness in Kenya, and Kenya's membership in the Convention on Wetlands of International Importance, has resulted in a critical review of these plans.     

Diversifying selection drives parallel evolution of gill raker number and body size along the speciation continuum of European whitefish

Adaptive radiation is the evolution of ecological and phenotypical diversity. It arises via ecological opportunity that promotes the exploration of underutilized or novel niches mediating specialization and reproductive isolation. The assumed precondition for rapid local adaptation is diversifying natural selection, but random genetic drift could also be a major driver of this process. We used 27 populations of European whitefish (Coregonus lavaretus) from nine lakes distributed in three neighboring subarctic watercourses in northern Fennoscandia as a model to test the importance of random drift versus diversifying natural selection for parallel evolution of adaptive phenotypic traits. We contrasted variation for two key adaptive phenotypic traits correlated with resource utilization of polymorphic fish; the number of gill rakers and the total length of fish, with the posterior distribution of neutral genetic differentiation from 13 microsatellite loci, to test whether the observed phenotypic divergence could be achieved by random genetic drift alone. Our results show that both traits have been under diversifying selection and that the evolution of these morphs has been driven by isolation through habitat adaptations. We conclude that diversifying selection acting on gill raker number and body size has played a significant role in the ongoing adaptive radiation of European whitefish morphs in this region.     

Rapid adaptation to a novel host in a seed beetle (Callosobruchus maculatus): the role of sexual selection

Rapid diversification is common among herbivorous insects and is often the result of host shifts, leading to the exploitation of novel food sources. This, in turn, is associated with adaptive evolution of female oviposition behavior and larval feeding biology. Although natural selection is the typical driver of such adaptation, the role of sexual selection is less clear. In theory, sexual selection can either accelerate or impede adaptation. To assess the independent effects of natural and sexual selection on the rate of adaptation, we performed a laboratory natural selection experiment in a herbivorous bruchid beetle (Callosobruchus maculatus). We established replicated selection lines where we varied natural (food type) and sexual (mating system) selection in a 2 x 2 orthogonal design, and propagated our lines for 35 generations. In half of the lines, we induced a host shift whereas the other half was kept on the ancestral host. We experimentally enforced monogamy in half of the lines, whereas the other half remained polygamous. The beetles rapidly adapted to the novel host, which primarily involved increased host acceptance by females and an accelerated rate of larval development. We also found that our mating system treatment affected the rate of adaptation, but that this effect was contingent upon food type. As beetles adapted to the novel host, sexual selection reinforced natural selection whereas populations residing close to their adaptive peak (i.e., those using their ancestral host) exhibited higher fitness in the absence of sexual selection. We discuss our findings in light of current sexual selection theory and suggest that the net evolutionary effect of reproductive competition may critically depend on natural selection. Sexual selection may commonly accelerate adaptation under directional natural selection whereas sexual selection, and the associated load brought by sexual conflict, may tend to depress population fitness under stabilizing natural selection.     

A new test for detecting ongoing selection

Much effort has been made to search for signatures of past natural selection in DNA sequences. However, currently acting selection is rarely detected in natural populations because of its rarity, low detection power of available methods, or both. Here, we develop a new test to detect viability selection over a single generation. In this test, one specific type of chromosomes is chosen as a reference, while all other chromosomes are designated as "focal". The test compares measures of variation between two groups of "focal" chromosomes: those found in reference/focal heterozygous individuals and those found in focal/focal homozygous individuals. In the absence of selection, we do not expect differences between these two groups as long as mating is random. On the other hand, currently acting selection can cause differences in some measures of variation. We applied this test to typing data for In(2L)t inversion polymorphism in a Drosophila melanogaster population, using "standard" (non-inverted) chromosomes as the focal class. Although the frequencies of In(2L)t and standard chromosomes did not deviate from the Hardy-Weinberg equilibrium, we found differences in allele frequency and the number of haplotypes between the two groups of standard chromosomes. This new test, in conjunction with the Hardy-Weinberg test, may shed light on how often strong selection is operating in extant populations.     

Genome‐wide signature of local adaptation linked to variable CpG methylation in oak populations

It has long been known that adaptive evolution can occur through genetic mutations in DNA sequence, but it is unclear whether adaptive evolution can occur through analogous epigenetic mechanisms, such as through DNA methylation. If epigenetic variation contributes directly to evolution, species under threat of disease, invasive competition, climate change or other stresses would have greater stores of variation from which to draw. We looked for evidence of natural selection acting on variably methylated DNA sites using population genomic analysis across three climatologically distinct populations of valley oaks. We found patterns of genetic and epigenetic differentiations that indicate local adaptation is operating on large portions of the oak genome. While CHG methyl polymorphisms are not playing a significant role and would make poor targets for natural selection, our findings suggest that CpG methyl polymorphisms as a whole are involved in local adaptation, either directly or through linkage to regions under selection.