Parallel signatures of selection at genomic islands of divergence and the major histocompatibility complex in ecotypes of sockeye salmon across Alaska

Understanding the genetic mechanisms that facilitate adaptive radiation is an important component of evolutionary biology. Here, we genotyped 82 neutral SNPs, seven SNPs in islands of divergence identified in a previous study (island SNPs), and a region of the major histocompatibility complex (MHC) in 32 populations of sockeye salmon to investigate whether conserved genes and genomic regions are involved in adaptive radiation. Populations representing three ecotypes were sampled from seven drainages with differing habitats and colonization histories spanning a range of 2,000 km. We found strong signatures of parallel selection across drainages at the island SNPs and MHC, suggesting that the same loci undergo divergent selection during adaptive radiation. However, patterns of differentiation at most island SNPs and the MHC were not associated with ecotypes, suggesting that these loci are responding differently to a mosaic of selective pressures. Our study provides some of the first evidence that conserved genomic islands may be involved in adaptive divergence of salmon populations. Additionally, our data provide further support for the hypothesis that sockeye salmon inhabiting rivers unconnected to lakes harbour similar genetic diversity across large distances, are likely the ancestral form of the species, and have repeatedly recolonized lake systems as they have become available after glacial recession. Finally, our results highlight the value and importance of validating outlier loci by screening additional populations and regions, a practice that will hopefully become more common in the future.     

Lack of parallel genetic patterns underlying the repeated ecological divergence of beach and stream‐spawning kokanee salmon

Recent progress in methods for detecting adaptive population divergence in situ shows promise for elucidating the conditions under which selection acts to generate intraspecific diversity. Rapid ecological diversification is common in fishes; however, the role of phenotypic plasticity and adaptation to local environments is poorly understood. It is now possible to investigate genetic patterns to make inferences regarding phenotypic traits under selection and possible mechanisms underlying ecotype divergence, particularly where similar novel phenotypes have arisen in multiple independent populations. Here, we employed a bottom‐up approach to test for signatures of directional selection associated with divergence of beach‐ and stream‐spawning kokanee, the obligate freshwater form of sockeye salmon (Oncorhynchus nerka). Beach‐ and stream‐spawners co‐exist in many post‐glacial lakes and exhibit distinct reproductive behaviours, life‐history traits and spawning habitat preferences. Replicate ecotype pairs across five lakes in British Columbia, Canada were genotyped at 57 expressed sequence tag‐linked and anonymous microsatellite loci identified in a previous genome scan. Fifteen loci exhibited signatures of directional selection (high F_ST outliers), four of which were identified in multiple lakes. However, the lack of parallel genetic patterns across all lakes may be a result of: 1) an inability to detect loci truly under selection; 2) alternative genetic pathways underlying ecotype divergence in this system; and/or 3) phenotypic plasticity playing a formative role in driving kokanee spawning habitat differences. Gene annotations for detected outliers suggest pathogen resistance and energy metabolism as potential mechanisms contributing to the divergence of beach‐ and stream‐spawning kokanee, but further study is required.     

Parallel morphological evolution and habitat‐dependent sexual dimorphism in cave‐ vs. surface populations of the Asellus aquaticus (Crustacea: Isopoda: Asellidae) species complex

Studying parallel evolution (repeated, independent evolution of similar phenotypes in similar environments) is a powerful tool to understand environment‐dependent selective forces. Surface‐dwelling species that repeatedly and independently colonized caves provide unique models for such studies. The primarily surface‐dwelling Asellus aquaticus species complex is a good candidate to carry out such research, because it colonized several caves in Europe. By comparing 17 functional morphological traits between six cave and nine surface populations of the A. aquaticus species complex, we investigated population divergence in morphology and sexual dimorphism. We found habitat‐dependent population divergence in 10 out of 17 traits, likely reflecting habitat‐driven changes in selection acting on sensory systems, feeding, grooming, and antipredator mechanisms. Sexual dimorphism was present in 15 traits, explained by sexual selection acting on male traits important in male–male agonistic behavior or mate guarding and fecundity selection acting on female traits affecting offspring number and nursing. In eight traits, the degree of sexual dimorphism was habitat dependent. We conclude that cave‐related morphological changes are highly trait‐ and function‐specific and that the strength of sexual/fecundity selection strongly differs between cave and surface habitats. The considerable population variation within habitat type warrants further studies to reveal cave‐specific adaptations besides the parallel patterns.     

Adaptive divergence and the evolution of reproductive isolation in the wild: an empirical demonstration using introduced sockeye salmon

Populations exposed to different ecological environments should diverge for phenotypic traits that influence survival and reproduction. This adaptive divergence should reduce gene flow between populations because immigrants become less fit than residents and because hybrids perform poorly in either environment (i.e., ecologically-dependent reproductive isolation). Here I demonstrate adaptive divergence and the evolution of reproductive isolation in populations of sockeye salmon (Oncorhynchus nerka) introduced from a common ancestral source into a new lake system (Lake Washington, Washington). The introduced fish founded several new populations, two of which experience very different environments during breeding and early development (Cedar River v.s. Pleasure Point beach). Over 13 generations, the two populations diverged for adult traits (female body size, male body depth; measured in the wild) and embryo traits (survival to hatching, development rate, size at emergence; measured in a common environment). The rates of divergence for these characters were similar to those observed in other examples of rapid evolution, and can best be attributed to natural selection. Partial reproductive isolation has evolved in concert with adaptive divergence: the rate of exchange of adults between the populations (determined using natural tags) is higher than the rate of gene flow (determined using DNA microsatellites). The demonstration that adaptive divergence can initiate reproductive isolation in less than 13 generations suggests that the first signs of ecological speciation may appear soon after new environments are first colonized.     

Carnivory maintains cranial dimorphism between males and females: Evidence for niche divergence in extant Musteloidea

The evolution and maintenance of sexual dimorphism has long been attributed to sexual selection. Niche divergence, however, serves as an alternative but rarely tested selective pressure also hypothesized to drive phenotypic disparity between males and females. We reconstructed ancestral social systems and diet and used Ornstein–Uhlenbeck (OU) modeling approaches to test whether niche divergence is stronger than sexual selection in driving the evolution of sexual dimorphism in cranial size and bite force across extant Musteloidea. We found that multipeak OU models favored different dietary regimes over social behavior and that the greatest degree of cranial size and bite force dimorphism were found in terrestrial carnivores. Because competition for terrestrial vertebrate prey is greater than other dietary groups, increased cranial size and bite force dimorphism reduces dietary competition between the sexes. In contrast, neither dietary regime nor social system influenced the evolution of sexual dimorphism in cranial shape. Furthermore, we found that the evolution of sexual dimorphism in bite force is influenced by the evolution of sexual dimorphism in cranial size rather than cranial shape. Overall, our results highlight niche divergence as an important mechanism that maintains the evolution of sexual dimorphism in musteloids.     

Sexual size dimorphism in greater mouse‐eared bat Myotis myotis (Chiroptera: Vespertilionidae) from a Mediterranean region

Although sexual size dimorphism (SSD) is common among mammals, there is no clear explanation for its maintenance in nature. Bats are one of the few groups of mammals where reverse SSD appears. In this group, the size of individuals may have very important ecological consequences related with flight. In this study, we examine sexual dimorphism in the wing measurements of 195 adult individuals (141 males and 54 females) of the greater mouse‐eared bat Myotis myotis in the south‐east of the Iberian Peninsula. We also investigated size differences between paired and single males in a swarming roost. The results indicate that there are significant differences in the wing measurements between sexes, females being bigger than males in this respect. While no significant differences in the wing measurements of paired and single males were observed, significant differences were found in their relative weight and fitness, single males being significantly heavier and having a better physical condition. We discuss the implications of SSD for the female of M. myotis in terms of reproductive advantages, trophic niche segregation and a greater ability to move, which may favour gene flow between populations.     

Sexual dimorphism in conspicuousness and ornamentation in the enigmatic leaf‐nosed lizard Ceratophora tennentii from Sri Lanka

Measures of physiological performance capacity, such as bite force, form the functional basis of sexual selection. Information about fighting ability may be conveyed through a structural feature such as a rostrum (i.e. horn) or a colour signal and thereby help reduce costly conflict. We quantified sexual dimorphism in key traits likely to be the targets of sexual selection in Tennent's leaf‐nosed lizard (Ceratophora tennentii) from Sri Lanka, and examined their relationship to bite force and body condition. We found body length and bite force to be similar for males and females. However, head length was significantly greater in males and they had significantly more conspicuous throats and labials (chromatic contrast and luminance) than females. Males also had a proportionally larger rostrum, which we predicted could be an important source of information about male quality for both sexes. Rostrum length was correlated with throat chromatic contrast in males but not females. Nonetheless, the rostrum and aspects of coloration did not correlate with bite force or body condition as we predicted. We have no information on contest escalation in this species but if they rarely bite, as suggested by a lack of difference in bite force between males and females, then bite force and any associated signals would not be a target of selection. Finally, males and females had similar spectral reflectance of the mouth and tongue and both had a peak in the ultra‐violet, and were conspicuous to birds. Lizards only gaped their mouths during capture and not when threatened by a potential predator (hand waving). We hypothesize that conspicuous mouth colour may act as a deimatic signal, startling a potential predator, although this will need careful experimental testing in the future.     

Sexual dimorphism and synchrony of breeding: variation in polygyny potential among populations in the common brushtail possum, Trichosurus vulpecula

Male-biased sexual dimorphism in both size and body mass isa common characteristic of many polygynous mammals and is oftenattributed to sexual selection favoring large males. The degreeof dimorphism is thought to be related to the potential forsome males to monopolize access to estrous females, which isin turn related to the distribution of receptive females inspace and time. In the present study, we investigated the relationshipbetween the temporal distribution of breeding females and thedegree of mass dimorphism among 11 populations of the commonbrushtail possum from northern Australia. Breeding patternsvaried from complete aseasonality in some populations to a seasonalconcentration of births within 2 or 3 months in others. We predictedthat in populations in which mating opportunities were distributedthroughout the year, dominant males would be able to monopolizeaccess to larger numbers of estrous females than in populationsin which matings were more seasonal, and in such populations,large body size in males would be favored. We found that dimorphismwas related to seasonality of breeding, being greatest in populationswith a more aseasonal pattern. Mean body mass of male possumsalso decreased with increasing population density. Populationdensity may influence the degree of breeding synchrony withinpopulations, particularly in locations with a more seasonalclimate. The present study is the first to demonstrate plasticityin mass dimorphism in response to local variation in the synchronyof breeding in a mammal species.     

Countergradient variation and secondary sexual color: phenotypic convergence promotes genetic divergence in carotenoid use between sympatric anadromous and nonanadromous morphs of sockeye salmon (Oncorhynchus nerka)

Genetically distinct anadromous (sockeye) and nonanadromous (kokanee) morphs of the Pacific salmon, Oncorhynchus nerka, develop identical, brilliant red color at maturity during sympatric breeding in freshwater streams. The marine and lacustrine environments they occupy prior to maturity, however, appear to differ in the availability of dietary carotenoid pigments necessary to produce red coloration. We tested the hypothesis that kokanee, which occupy carotenoid-poor lakes, are more efficient at using the dietary pigments than are sockeye, which occupy the more productive North Pacific Ocean. In a 2-year controlled breeding study, flesh and skin color of mature and immature crosses fed a low-carotenoid diet were quantified with both a chromameter and by chemical extraction of carotenoid pigments. Results revealed striking countergradient variation in carotenoid use, with kokanee approximately three times more efficient at sequestering the pigments to the flesh musculature than similar age sockeye. This difference translated into virtually nonoverlapping differences between pure crosses in secondary sexual color at maturity, when the pigments are mobilized and transported to the skin. Kokanee crosses turned pinkish red over most of their body, whereas sockeye turned olive green. The olive green was similar to the breeding color of residuals in the wild, the progeny of anadromous sockeye that remain in fresh water and are believed to have given rise to kokanee on numerous independent occasions. Reciprocal hybrids were similar to each other and intermediate to the pure crosses, indicating additive genetic inheritance. Mate choice trials with sockeye males in the wild showed the ancestral morph strongly preferred red over green models. These results suggest a preference for red mates maintained in nonanadromous breeding populations drove the reevolution of the red phenotype in kokanee via more efficient use of dietary carotenoid pigments. This is a novel, yet hidden, mechanism by which sexual selection promotes the genetic differentiation of these sympatric populations.     

Sexual dimorphism explains residual variance around the survival‐reproduction tradeoff in lizards: Implications for sexual conflict over life‐history evolution*

The tradeoff between survival and reproduction is a central feature of life‐history variation, but few studies have sought to explain why females of some species exhibit relatively lower survival than expected for a given level of reproductive effort (RE). Intralocus sexual conflict theory proposes that sex differences in selection on survival and RE may, by virtue of shared genes underlying these components of fitness, prevent females from optimizing this life‐history tradeoff. To test this hypothesis, we used a phylogenetically based comparative analysis of published estimates for mean annual survival and RE from females of 82 lizard species to (1) characterize the tradeoff between survival and reproduction and (2) test whether variation around this tradeoff is explained by sexual size dimorphism (SSD), a potential proxy for sexual conflict over life‐history traits. Across species, we found a strong negative correlation between mean annual survival and RE, confirming this classic life‐history tradeoff. Although residual variance around this tradeoff is unrelated to the absolute magnitude of SSD, it is strongly related to the direction of SSD. Specifically, we found that females have lower survival than expected for a given level of RE in female‐larger species, whereas they have higher survival than expected in male‐larger species. Given that female‐larger SSD is thought to reflect selection for increased fecundity, our results suggest that intralocus sexual conflict may be particularly likely to constrain female life‐history evolution in situations where increased RE is favored, but the phenotypes that facilitate this increase (e.g., body size) are constrained by antagonistic selection on males.     

Sexual size dimorphism and morphological divergence in the yellow‐whiskered Greenbul (Andropadus latirostris) in the Guineo‐Congolian rainforest of Africa

Evidence of sexual dimorphism in body size and the existence of morphological differences were studied in the yellow‐whiskered Greenbul Andropadus latirostris. We measured fresh body weight and seven linear parameters of external morphology in mature individuals of this species from three localities in Cameroon and two localities in Ghana. Based on general linear model analysis, we showed that males are significantly larger than females. We applied a discriminant analysis on eight morphometric parameters to create two discriminant functions, one for each country. The overall rate of well‐classified birds was 93.3% for Cameroon and 92.7% for Ghana. Wing length was the most accurate character for separating the sexes in both study areas. Significant sexual size dimorphism might be explained by sexual selection on male competitive ability and intraspecific competition. We also found morphological divergence in this species between the two study areas, including marked differences in size of the beak. This work provides statistical evidence of a substantial sexual size dimorphism in A. latirostris and geographic variation in morphology.     

Origins of female genital diversity: Predation risk and lock‐and‐key explain rapid divergence during an adaptive radiation

The study of male genital diversity has long overshadowed evolutionary inquiry of female genitalia, despite its nontrivial diversity. Here, we identify four nonmutually exclusive mechanisms that could lead to genital divergence in females, and potentially generate patterns of correlated male–female genital evolution: (1) ecological variation alters the context of sexual selection (“ecology hypothesis”), (2) sexually antagonistic selection (“sexual‐conflict hypothesis”), (3) female preferences for male genitalia mediated by female genital traits (“female‐choice hypothesis”), and (4) selection against inter‐population mating (“lock‐and‐key hypothesis”). We performed an empirical investigation of all four hypotheses using the model system of Bahamas mosquitofish inhabiting blue holes that vary in predation risk. We found unequivocal support for the ecology hypothesis, with females exhibiting a smaller genital opening in blue holes containing piscivorous fish. This is consistent with stronger postmating female choice/conflict when predators are present, but greater premating female choice in their absence. Our results additionally supported the lock‐and‐key hypothesis, uncovering a pattern of reproductive character displacement for genital shape. We found no support for the sexual conflict or female choice hypotheses. Our results demonstrate a strong role for ecology in generating female genital diversity, and suggest that lock‐and‐key may provide a viable cause of female genital diversification.     

Independent lineages in a common environment: the roles of determinism and contingency in shaping the migration timing of even‐ versus odd‐year pink salmon over broad spatial and temporal scales

Studies of parallel evolution are seldom able to disentangle the influence of cryptic environmental variation from that of evolutionary history; whereas the unique life history of pink salmon (Oncorhynchus gorbuscha) presents an opportunity to do so. All pink salmon mature at age two and die after breeding. Hence, pink salmon bred in even years are completely reproductively isolated from those bred in odd years, even if the two lineages bred in same location. We used time series (mean = 7 years, maximum = 74 years) of paired even‐ and odd‐year populations from 36 rivers spanning over 2000 km to explore parallelism in migration timing, a trait with a strong genetic basis. Migration timing was highly parallel, being determined almost entirely by local environmental differences among rivers. Interestingly, interannual changes in migration timing different somewhat between lineages. Overall, our findings indicate very strong determinism, with only a minor contribution of contingency.     

Lake‐specific variation in growth,migration timing and survival of juvenile sockeye salmon Oncorhynchus nerka: separating environmental from genetic influences

Time series on juvenile life‐history traits obtained from sockeye salmon Oncorhynchus nerka were analysed to assess lake‐specific environmental influences on juvenile migration timing, size and survival of fish from a common gene pool. Every year for the past two decades, O. nerka have been spawned at a hatchery facility, and the progeny released into two lakes that differ in average summer temperatures, limnological attributes and growth opportunities. Juveniles reared in the warmer, more productive Crosswind Lake were larger and heavier as smolts compared to those from the cooler, less productive Summit Lake and had higher in‐lake and subsequent marine survival. Crosswind Lake smolts migrated from the lake to sea slightly earlier in the season but the migration timing distributions overlapped considerably across years. Fry stocking density had a negative effect on smolt length for both lakes, and a negative effect on in‐lake survival in Summit Lake. Taken together, the results revealed a strong effect of lake‐rearing environment on the expression of life‐history variation in O. nerka. The stocking of these lakes each year with juveniles from a single mixed‐source population provided a large‐scale reverse common‐garden experiment, where the same gene pool was exposed to different environments, rather than the different gene pools in the same environment approach typical of evolutionary ecology studies. Other researchers are encouraged to seek and exploit similar serendipitous situations, which might allow environmental and genetic influences on ecologically important traits to be distinguished in natural or semi‐natural settings.     

Reproduction and sexual dimorphism in the viviparous lizard Sceloporus palaciosi (Squamata: Phrynosomatidae) from the Trans‐Mexican Volcanic Belt,Mexico

In this study, sexual dimorphism, reproductive cycles, litter size and offspring size of a population of the little‐known species Sceloporus palaciosi in central Mexico were analysed. Significant male‐biased sexual size dimorphism was recorded in snout–vent length (SVL), head length, head width, forearm length and tibia length. Both sexes showed asynchronous reproductive cycles, and males reached sexual maturity at a smaller SVL (33 mm) than females (37 mm). Testes volumes were small from January to February, testicular recrudescence began from March to June, and decreased in July, but increased again in August and September, followed by a second decrease from October to December. In females, vitellogenesis began from May until ovulation in December. Embryonic development extended from November to March, and a small number of females carried embryos through July. Mean litter size was 4.0 and was positively correlated with female SVL. The length of the reproductive period in S. palaciosi recorded in this study is longer than that recorded for other populations in other parts of this species range. Further studies are needed to clarify reproductive cycles in the other isolated populations of S. palaciosi, and then extended to other species and chromosome races in the Sceloporus grammicus complex.     

Pike and salmon as sister taxa: Detailed intraclade resolution and divergence time estimation of Esociformes + Salmoniformes based on whole mitochondrial genome sequences

The increasing number of taxa and loci in molecular phylogenetic studies of basal euteleosts has brought stability in a controversial area. A key emerging aspect to these studies is a sister Esociformes (pike) and Salmoniformes (salmon) relationship. We evaluate mitochondrial genome support for a sister Esociformes and Salmoniformes hypothesis by surveying many potential outgroups for these taxa, employing multiple phylogenetic approaches, and utilizing a thorough sampling scheme. Secondly, we conduct a simultaneous divergence time estimation and phylogenetic inference in a Bayesian framework with fossil calibrations focusing on relationships within Esociformes + Salmoniformes. Our dataset supports a sister relationship between Esociformes and Salmoniformes; however the nearest relatives of Esociformes + Salmoniformes are inconsistent among analyses. Within the order Esociformes, we advocate for a single family, Esocidae. Subfamily relationships within Salmonidae are poorly supported as Salmoninae sister to Thymallinae + Coregoninae.     

Interaction of N,N,N′,N′-tetramethyl-p-phenylenediamine with photosystem II as revealed by thermoluminescence: Reduction of the higher oxidation states of the Mn cluster and displacement of plastoquinone from the QB niche

The flash-induced thermoluminescence (TL) technique was used to investigate the action of N,N,N′,N′-tetramethyl-p-phenylenediamine (TMPD) on charge recombination in photosystem II (PSII). Addition of low concentrations (μM range) of TMPD to thylakoid samples strongly decreased the yield of TL emanating from S₂Q_B⁻ and S₃Q_B⁻ (B-band), S₂Q_A⁻ (Q-band), and Y_D⁺Q_A⁻ (C-band) charge pairs. Further, the temperature-dependent decline in the amplitude of chlorophyll fluorescence after a flash of white light was strongly retarded by TMPD when measured in the presence of 3-(3,4-dichlorophenyl)-1,1-dimethylurea (DCMU). Though the period-four oscillation of the B-band emission was conserved in samples treated with TMPD, the flash-dependent yields (Y_n) were strongly declined. This coincided with an upshift in the maximum yield of the B-band in the period-four oscillation to the next flash. The above characteristics were similar to the action of the ADRY agent, carbonylcyanide m-chlorophenylhydrazone (CCCP). Simulation of the B-band oscillation pattern using the integrated Joliot-Kok model of the S-state transitions and binary oscillations of Q_B confirmed that TMPD decreased the initial population of PSII centers with an oxidized plastoquinone molecule in the Q_B niche. It was deduced that the action of TMPD was similar to CCCP, TMPD being able to compete with plastoquinone for binding at the Q_B-site and to reduce the higher S-states of the Mn cluster.