ON THE EVOLUTION OF SEXUAL REPRODUCTION IN HOSTS COEVOLVING WITH MULTIPLE PARASITES

Host–parasite coevolution has been studied extensively in the context of the evolution of sex. Although hosts typically coevolve with several parasites, most studies considered one‐host/one‐parasite interactions. Here, we study population‐genetic models in which hosts interact with two parasites. We find that host/multiple‐parasite models differ nontrivially from host/single‐parasite models. Selection for sex resulting from interactions with a single parasite is often outweighed by detrimental effects due to the interaction between parasites if coinfection affects the host more severely than expected based on single infections, and/or if double infections are more common than expected based on single infections. The resulting selection against sex is caused by strong linkage‐disequilibria of constant sign that arise between host loci interacting with different parasites. In contrast, if coinfection affects hosts less severely than expected and double infections are less common than expected, selection for sex due to interactions with individual parasites can now be reinforced by additional rapid linkage‐disequilibrium oscillations with changing sign. Thus, our findings indicate that the presence of an additional parasite can strongly affect the evolution of sex in ways that cannot be predicted from single‐parasite models, and that thus host/multiparasite models are an important extension of the Red Queen Hypothesis.     

SEXUAL SELECTION,MULTIPLE MALE ORNAMENTS,AND AGE‐ AND CONDITION‐DEPENDENT SIGNALING IN THE COMMON YELLOWTHROAT

In many animals, sexual selection has resulted in complex signaling systems in which males advertise aspects of their phenotypic or genetic quality through elaborate ornamentation and display behaviors. Different ornaments might convey different information or be directed at different receivers, but they might also be redundant signals of quality that function reliably at different times (ages) or in different contexts. We explored sexual selection and age‐ and condition‐dependent signaling in the common yellowthroat (Geothlypis trichas), a sexually dichromatic warbler with two prominent plumage ornaments—a melanin‐based, black facial “mask” and carotenoid‐based, UV‐yellow “bib.” In a three‐year study, variance among males in the number of social (M_w) and extra‐pair (M_e) mates generated strong sexual selection on mask and bib attributes. Some traits (mask size, bib yellow brightness) were correlated with male age and did not experience selection beyond age‐related increases in M_w and M_e. Other traits showed age‐specific (bib size) or age‐reversed (ultraviolet brightness) patterns of selection that paralleled changes in the information‐content of each ornament. The components of male fitness generating selection in young versus old males were distinct, reflecting different sources of variation in male fertilization success. Age‐ and context‐dependent changes in the strength, direction, and target of selection may help explain the maintenance of multiple ornaments in this and other species.     

SHORT‐TERM AND LONG‐TERM EFFECTS OF TEMPERATURE ON PHOTOSYNTHESIS IN THE DIATOM THALASSIOSIRA PSEUDONANA UNDER UVR EXPOSURES1

Temperature is expected to modify the effects of ultraviolet radiation (UVR) on photosynthesis by affecting the rate of repair. We studied the effect of short‐term (1 h) and long‐term (days) acclimation to temperature on UVR photoinhibition in the diatom Thalassiosira pseudonana Hasle et Heimdal. Photosynthesis was measured during 1 h exposures to varying irradiances of PAR and UVR + PAR at 15, 20, and 25°C, the latter corresponding to the upper temperature limit for optimal growth in T. pseudonana. The exposures allowed the estimation of photosynthesis–irradiance (P–E) curves and biological weighting functions (BWFs) for photoinhibition. For the growth conditions used, temperature did not affect photosynthesis under PAR. However, photoinhibition by UVR was highly affected by temperature. For cultures preacclimated to 20°C, the extent of UVR photoinhibition increased with decreasing temperature, from 63% inhibition of PAR‐only photosynthesis at 25°C to 71% at 20°C and 85% at 15°C. These effects were slightly modified after several days of acclimation: UVR photoinhibition increased from 63% to 75% at 25°C and decreased from 85% to 80% at 15°C. Time courses of photochemical efficiency (Φ_PSII) under UVR + PAR were also fitted to a model of UVR photoinhibition, allowing the estimation of the rates of damage (k) and repair (r). The r/k values obtained for each temperature treatment verified the responses observed with the BWF (R² = 0.94). The results demonstrated the relevance of temperature in determining primary productivity under UVR exposures. However, the results suggested that temperature and UVR interact mainly over short (hours) rather than long (days) timescales.     

DIFFERENCES IN THE REGULATION OF GROWTH AND BIOMINERALIZATION GENES REVEALED THROUGH LONG‐TERM COMMON‐GARDEN ACCLIMATION AND EXPERIMENTAL GENOMICS IN THE PURPLE SEA URCHIN

Across heterogeneous landscapes, populations may have adaptive differences in gene regulation that adjust their physiologies to match local environments. Such differences could have origins in acclimation or in genetically fixed variation between habitats. Here we use common‐garden experiments to evaluate differences in gene expression between populations of the purple sea urchin, Strongylocentrotus purpuratus, spanning 1700 km and average temperature differences of 5°C to 8°C. Across expression profiles from 18,883 genes after 3 years of common conditions, we find highly correlated expression patterns (Pearson's r = 0.992) among most genes. However, 66 genes were differentially expressed, including many ribosomal protein and biomineralization genes, which had higher expression in urchins originally from the southern population. Gene function analyses revealed slight but pervasive expression differences in genes related to ribosomal function, metabolism, transport, “bone” development, and response to stimuli. In accord with gene expression patterns, a post‐hoc spine regrowth experiment revealed that urchins of southern origin regrew spines at a faster rate than northern urchins. These results suggest that there may be genetically controlled, potentially adaptive differences in gene regulation across habitats and that gene expression differences may be under strong enough selection to overcome high, dispersal–mediated gene flow in this marine species.     

DIVERSITY‐DEPENDENT CLADOGENESIS AND TRAIT EVOLUTION IN THE ADAPTIVE RADIATION OF THE AUKS (AVES: ALCIDAE)

Through the course of an adaptive radiation, the evolutionary speed of cladogenesis and ecologically relevant trait evolution are expected to slow as species diversity increases, niches become occupied, and ecological opportunity declines. We develop new likelihood‐based models to test diversity‐dependent evolution in the auks, one of only a few families of seabirds adapted to underwater “flight,” and which exhibit a large variety of bill sizes and shapes. Consistent with the expectations of adaptive radiation, we find both a decline in rates of cladogenesis (a sixfold decline) and bill shape (a 64‐fold decline) evolution as diversity increased. Bill shape diverged into two clades at the basal cladogenesis event with one clade possessing mostly long, narrow bills used to forage primarily on fish, and the other with short thick bills used to forage primarily on plankton. Following this initial divergence in bill shape, size, a known correlate of both prey size and maximum diving depth, diverged rapidly within each of these clades. These results suggest that adaptive radiation in foraging traits underwent initial divergence in bill shape to occupy different food resources, followed by size differentiation to subdivide each niche along the depth axis of the water column.     

LONG‐TERM CHANGES IN THE MACROALGAL VEGETATION OF THE INNER GULLMAR FJORD,SWEDISH SKAGERRAK COAST1

We examined long‐term changes in the macroalgal vegetation at Stora Bornö Island in the inner Gullmar Fjord on the Swedish Skagerrak coast. This was made possible by access to a 1941 diving investigation. The same sites were reinvestigated in 1998. Community composition and depth distributions of species were compared and changes were analyzed with focus on functional groups (size, thallus shape, and life‐history traits). We discovered a significant decrease in the depth extension of macroalgal species and a dramatic decline of species richness in the lower littoral (below 16 m of depth) compared with 57 years earlier. Ordination analysis revealed that there was a significant difference in the community composition between the two study periods. In general, small (<10 cm), thin, filamentous, and aseasonal ephemerals increased in relative abundance, whereas larger (>10 cm), coarsely branched, and perennial algae decreased. Calibrations of individual species to local sediment cover, using canonical correspondence analysis, indicated that part of the change in species composition was related to sediment load. Furthermore, large‐scale climate differences (NAO Winter Index) between the study periods indicated a higher impact of Baltic Sea and Kattegat water in the nutrient dynamics of the fjord in the 1998 study. We concluded that the observed long‐term changes in the macroalgal community at Stora Bornö Island were consistent with an increased nutrient availability.     

DOES MATE LIMITATION IN SELF‐INCOMPATIBLE SPECIES PROMOTE THE EVOLUTION OF SELFING? THE CASE OF LEAVENWORTHIA ALABAMICA

Genetic diversity at the S‐locus controlling self‐incompatibility (SI) is often high because of negative frequency‐dependent selection. In species with highly patchy spatial distributions, genetic drift can overwhelm balancing selection and cause stochastic loss of S‐alleles. Natural selection may favor the breakdown of SI in populations with few S‐alleles because low S‐allele diversity constrains the seed production of self‐incompatible plants. We estimated S‐allele diversity, effective population sizes, and migration rates in Leavenworthia alabamica, a self‐incompatible mustard species restricted to discrete habitat patches in rocky glades. Patterns of polymorphism were investigated at the S‐locus and 15 neutral microsatellites in three large and three small populations with 100‐fold variation in glade size. Populations on larger glades maintained more S‐alleles, but all populations were estimated to harbor at least 20 S‐alleles, and mate availabilities typically exceeded 0.80, which is consistent with little mate limitation in nature. Estimates of the effective size (N_e) in each population ranged from 600 to 1600, and estimated rates of migration (m) ranged from 3 × 10⁻⁴ to nearly 1 × 10⁻³. According to theoretical models, there is limited opportunity for genetic drift to reduce S‐allele diversity in populations with these attributes. Although pollinators or resources limit seed production in small glades, limited S‐allele diversity does not appear to be a factor promoting the incipient breakdown of SI in populations of this species that were studied.     

HANDEDNESS AND ASYMMETRY IN SCALE‐EATING CICHLIDS: ANTISYMMETRIES OF DIFFERENT STRENGTH

Individual symmetry is believed to be advantageous and reflecting developmental stability, but frequency‐dependent selection can also maintain polymorphisms of asymmetric phenotypes. There are many examples of so‐called antisymmetry, where mirror image morphs occur at equal frequencies. With very few exceptions, these are caused by nongenetic variation. One notable exception is handedness and mouth bending variation in the scale‐eating cichlid Perissodus microlepis, which has been suggested to be an example of antisymmetry determined by a single genetic locus of large effect. Here, we report that this handedness and mouth bending asymmetry are not jointly and exclusively determined by a single major locus. We found no evidence of a major locus for asymmetry and some support for a major handedness locus. Also, asymmetry is plastic in this species: it can change in adults. We suggest that behavioral handedness in this system precedes and guides morphological asymmetry.     

COMPARATIVE ANALYSES OF SEX‐RATIO VARIATION IN DIOECIOUS FLOWERING PLANTS

Dioecious plant species commonly exhibit deviations from the equilibrium expectation of 1:1 sex ratio, but the mechanisms governing this variation are poorly understood. Here, we use comparative analyses of 243 species, representing 123 genera and 61 families to investigate ecological and genetic correlates of variation in the operational (flowering) sex ratio. After controlling for phylogenetic nonindependence, we examined the influence of growth form, clonality, fleshy fruits, pollen and seed dispersal vector, and the possession of sex chromosomes on sex‐ratio variation. Male‐biased flowering sex ratios were twice as common as female‐biased ratios. Male bias was associated with long‐lived growth forms (e.g., trees) and biotic seed dispersal and fleshy fruits, whereas female bias was associated with clonality, especially for herbaceous species, and abiotic pollen dispersal. Female bias occurred in species with sex chromosomes and there was some evidence for a greater degree of bias in those with heteromorphic sex chromosomes. Although the role of interactions among these correlates require further study, our results indicate that sex‐based differences in costs of reproduction, pollen and seed dispersal mechanisms and sex chromosomes can each play important roles in affecting flowering sex ratios in dioecious plants.     

EFFECTIVE POPULATION SIZE AND THE FASTER‐X EFFECT: EMPIRICAL RESULTS AND THEIR INTERPRETATION

The X or Z chromosome has several characteristics that distinguish it from the autosomes, namely hemizygosity in the heterogametic sex, and a potentially different effective population size, both of which may influence the rate and nature of evolution. In particular, there may be an accelerated rate of adaptive change for X‐linked compared to autosomal coding sequences, often referred to as the Faster‐X effect. Empirical studies have indicated that the strength of Faster‐X evolution varies among different species, and theoretical treatments have shown that demography and mating system can substantially affect the degree of Faster‐X evolution. Here we integrate genomic data on Faster‐X evolution from a variety of animals with the demographic factors, mating system, and sex chromosome regulatory characteristics that may influence it. Our results suggest that differences in effective population size and mechanisms of dosage compensation may influence the perceived extent of Faster‐X evolution, and help to explain several clade‐specific patterns that we observe.     

LONG‐TERM CHANGES IN THE STRUCTURE OF INTERTIDAL ASSEMBLAGES AFTER INVASION BY SARGASSUM MUTICUM (PHAEOPHYTA)1

The macroalgal assemblages at the low intertidal zone were studied at three localities on the north coast of Spain between 1977 and 2002. Two of these localities were invaded at the end of the 1980s by the brown seaweed Sargassum muticum (Yendo) Fensholt (Phaeophyta, Sargassaceae), whereas the third locality remained free of the invader. In 2002, distinct algal assemblages were noticed in invaded and noninvaded localities. No major changes were detected in the noninvaded locality. Apart from the obvious presence of S. muticum, the changes observed in the invaded localities included a significant reduction in abundance of the previous dominant species (the red alga Gelidium spinosum (S. G. Gmelin) P. C. Silva) as well as an increased number of species and diversity, increased primary productivity, and variations in the seasonal abundance patterns of some species. We speculate that the arrival of S. muticum had a negative effect on the dominant native G. spinosum, probably related to competition for light. This resulted in indirect positive effects on other species of the assemblage (such as Bifurcaria bifurcata R. Ross). Other small epiphytic opportunistic species might also have been benefited from the presence of S. muticum, because the invader has a rich associated epiphytic assemblage.     

MULLER'S RATCHET AND THE ADVANTAGE OF SEX IN THE RNA VIRUS ϟ6

Population genetic models have shown that if genetic drift is strong and the rate of deleterious mutations is high, Muller's ratchet provides an advantage to sex. A previous study tested for the possibility that Muller's ratchet could work in RNA viruses, which are known to have very high mutation rates. Muller's ratchet was found to operate when lineages of the RNA bacteriophage φ6 were subjected to intensified genetic drift. The study did not determine, however, whether sex is advantageous to these viruses. We have examined whether sex can reverse the effects of Muller's ratchet by crossing nine φ6 lineages that were subjected to the ratchet in Chao's study. To determine whether there was a net advantage to sex, we analyzed the effect of crossing three lineages to all other lineages. Crossing increased significantly the fitness of two lineages, but it did not significantly affect the fitness of the third lineage. We argue that the minimal advantage of sex to these nine lineages is small, but positive. These results provide a possible scenario for the evolution of sex in an RNA phage like φ6.     

DEEP DIVERSIFICATION AND LONG‐TERM PERSISTENCE IN THE SOUTH AMERICAN ‘DRY DIAGONAL’: INTEGRATING CONTINENT‐WIDE PHYLOGEOGRAPHY AND DISTRIBUTION MODELING OF GECKOS

The relative influence of Neogene geomorphological events and Quaternary climatic changes as causal mechanisms on Neotropical diversification remains largely speculative, as most divergence timing inferences are based on a single locus and have limited taxonomic or geographic sampling. To investigate these influences, we use a multilocus (two mitochondrial and 11 nuclear genes) range‐wide sampling of Phyllopezus pollicaris, a gecko complex widely distributed across the poorly studied South American ‘dry diagonal’ biomes. Our approach couples traditional and model‐based phylogeography with geospatial methods, and demonstrates Miocene diversification and limited influence of Pleistocene climatic fluctuations on P. pollicaris. Phylogeographic structure and distribution models highlight that persistence across multiple isolated regions shaped the diversification of this species complex. Approximate Bayesian computation supports hypotheses of allopatric and ecological/sympatric speciation between lineages that largely coincide with genetic clusters associated with Chaco, Cerrado, and Caatinga, standing for complex diversification between the ‘dry diagonal’ biomes. We recover extremely high genetic diversity and suggest that eight well‐supported clades may be valid species, with direct implications for taxonomy and conservation assessments. These patterns exemplify how low‐vagility species complexes, characterized by strong genetic structure and pre‐Pleistocene divergence histories, represent ideal radiations to investigate broad biogeographic histories of associated biomes.     

SEX LINKAGE,SEX‐SPECIFIC SELECTION,AND THE ROLE OF RECOMBINATION IN THE EVOLUTION OF SEXUALLY DIMORPHIC GENE EXPRESSION

Sex‐biased genes—genes that are differentially expressed within males and females—are nonrandomly distributed across animal genomes, with sex chromosomes and autosomes often carrying markedly different concentrations of male‐ and female‐biased genes. These linkage patterns are often gene‐ and lineage‐dependent, differing between functional genetic categories and between species. Although sex‐specific selection is often hypothesized to shape the evolution of sex‐linked and autosomal gene content, population genetics theory has yet to account for many of the gene‐ and lineage‐specific idiosyncrasies emerging from the empirical literature. With the goal of improving the connection between evolutionary theory and a rapidly growing body of genome‐wide empirical studies, we extend previous population genetics theory of sex‐specific selection by developing and analyzing a biologically informed model that incorporates sex linkage, pleiotropy, recombination, and epistasis, factors that are likely to vary between genes and between species. Our results demonstrate that sex‐specific selection and sex‐specific recombination rates can generate, and are compatible with, the gene‐ and species‐specific linkage patterns reported in the genomics literature. The theory suggests that sexual selection may strongly influence the architectures of animal genomes, as well as the chromosomal distribution of fixed substitutions underlying sexually dimorphic traits.     

LOCAL ADAPTATION IN A CHANGING WORLD: THE ROLES OF GENE‐FLOW,MUTATION, AND SEXUAL REPRODUCTION

In spatially heterogeneous environments, the processes of gene flow, mutation, and sexual reproduction generate local genetic variation and thus provide material for local adaptation. On the other hand, these processes interchange maladapted for adapted genes and so, in each case, the net influence may be to reduce local adaptation. Previous work has indicated that this is the case in stable populations, yet it is less clear how the factors play out during population growth, and in the face of temporal environmental stochasticity. We address this issue with a spatially explicit, stochastic model. We find that dispersal, mutation, and sexual reproduction can all accelerate local adaptation in growing populations, although their respective roles may depend on the genetic make‐up of the founding population. All three processes reduce local adaptation, however, in the long term, that is when population growth becomes balanced by density‐dependent competition. These relationships are qualitatively maintained, although quantitatively reduced, if the resources are locally ephemeral. Our results suggest that species with high levels of local adaptation within their ranges may not be the same species that harbor potential for rapid local adaptation during population expansion.     

ISOLATION OF THREE NOVEL LONG‐CHAIN POLYUNSATURATED FATTY ACID Δ9‐ELONGASES AND THE TRANSGENIC ASSEMBLY OF THE ENTIRE PAVLOVA SALINA DOCOSAHEXAENOIC ACID PATHWAY IN NICOTIANA BENTHAMIANA1

The transgenic aerobic synthesis of long‐chain polyunsaturated fatty acids (LC‐PUFA) will in most land plants commence with either a Δ6‐desaturation or a Δ9‐elongation. Numerous Δ6‐desaturases have been characterized, but only one Δ9‐elongase has been reported in peer‐reviewed literature. In the present study, we describe the isolation of three additional Δ9‐elongases from the class Haptophyceae and demonstrate that the Δ9‐elongase group contains highly conserved regions, which differentiate them from other ELO‐type elongases. One such important difference is the presence of an LQxFHH motif instead of the usual LHxYHH motif, a feature that should simplify further gene discovery efforts in this group of enzymes. Moreover, the identification of the Pavlova salina (N. Carter) J. C. Green Δ9‐elongase completes the isolation of the entire P. salina docosahexaenoic acid (DHA) pathway, and we describe the assembly of this pathway in Nicotiana benthamiana. Finally, we comment on possible explanations for the widespread presence of the Δ6‐desaturated fatty acid stearidonic acid (SDA, 18:4^Δ6,9,12,15) in the plastidial lipids of organisms using the Δ9‐elongase pathway.     

SHORT‐ AND LONG‐TERM EFFECTS OF ELEVATED CO2 ON PHOTOSYNTHESIS AND RESPIRATION IN THE MARINE MACROALGA HIZIKIA FUSIFORMIS (SARGASSACEAE,PHAEOPHYTA) GROWN AT LOW AND HIGH N SUPPLIES1

The short‐term and long‐term effects of elevated CO₂ on photosynthesis and respiration were examined in cultures of the marine brown macroalga Hizikia fusiformis (Harv.) Okamura grown under ambient (375 μL · L^?1) and elevated (700 μL · L^?1) CO₂ concentrations and at low and high N availability. Short‐term exposure to CO₂ enrichment stimulated photosynthesis, and this stimulation was maintained with prolonged growth at elevated CO₂, regardless of the N levels in culture, indicating no down‐regulation of photosynthesis with prolonged growth at elevated CO₂. However, the photosynthetic rate of low‐N‐grown H. fusiformis was more responsive to CO₂ enrichment than that of high‐N‐grown algae. Elevation of CO₂ concentration increased the value of K_1/2(Ci) (the half‐saturation constant) for photosynthesis, whereas high N supply lowered it. Neither short‐term nor long‐term CO₂ enrichment had inhibitory effects on respiration rate, irrespective of the N supply, under which the algae were grown. Under high‐N growth, the Q₁₀ value of respiration was higher in the elevated‐CO₂‐grown algae than the ambient‐CO₂‐grown algae. Either short‐ or long‐term exposure to CO₂ enrichment decreased respiration as a proportion of gross photosynthesis (Pg) in low‐N‐grown H. fusiformis. It was proposed that in a future world of higher atmospheric CO₂ concentration and simultaneous coastal eutrophication, the respiratory carbon flux would be more sensitive to changing temperature.     

A DEMOGRAPHIC TRANSITION ALTERED THE STRENGTH OF SELECTION FOR FITNESS AND AGE‐SPECIFIC SURVIVAL AND FERTILITY IN A 19TH CENTURY AMERICAN POPULATION

Modernization has increased longevity and decreased fertility in many human populations, but it is not well understood how or to what extent these demographic transitions have altered patterns of natural selection. I integrate individual‐based multivariate phenotypic selection approaches with evolutionary demographic methods to demonstrate how a demographic transition in 19th century female populations of Utah altered relationships between fitness and age‐specific survival and fertility. Coincident with this demographic transition, natural selection for fitness, as measured by the opportunity for selection, increased by 13% to 20% over 65 years. Proportional contributions of age‐specific survival to total selection (the complement to age‐specific fertility) diminished from approximately one third to one seventh following a marked increase in infant survival. Despite dramatic reductions in age‐specific fertility variance at all ages, the absolute magnitude of selection for fitness explained by age‐specific fertility increased by approximately 45%. I show that increases in the adaptive potential of fertility traits followed directly from decreased population growth rates. These results suggest that this demographic transition has increased the adaptive potential of the Utah population, intensified selection for reproductive traits, and de‐emphasized selection for survival‐related traits.     

SIGN EPISTASIS LIMITS EVOLUTIONARY TRADE‐OFFS AT THE CONFLUENCE OF SINGLE‐ AND MULTI‐CARBON METABOLISM IN METHYLOBACTERIUM EXTORQUENS AM1

Adaptation of one set of traits is often accompanied by attenuation of traits important in other selective environments, leading to fitness trade‐offs. The mechanisms that either promote or prevent the emergence of trade‐offs remain largely unknown, and are difficult to discern in most systems. Here, we investigate the basis of trade‐offs that emerged during experimental evolution of Methylobacterium extorquens AM1 to distinct growth substrates. After 1500 generations of adaptation to a multi‐carbon substrate, succinate (S), many lineages had lost the ability to use one‐carbon compounds such as methanol (M), generating a mixture of M⁺ and M^? evolved phenotypes. We show that trade‐offs in M^? strains consistently arise via antagonistic pleiotropy through recurrent selection for loss‐of‐function mutations to ftfL (formate‐tetrahydrofolate ligase), which improved growth on S while simultaneously eliminating growth on M. But if loss of FtfL was beneficial, why were M trade‐offs not found in all populations? We discovered that eliminating FtfL was not universally beneficial on S, as it was neutral or even deleterious in certain evolved lineages that remained M⁺. This suggests that sign epistasis with earlier arising mutations prevented the emergence of mutations that drove trade‐offs through antagonistic pleiotropy, limiting the evolution of metabolic specialists in some populations.