Leigh C. Latta

THE QUANTITATIVE AND MOLECULAR GENETIC ARCHITECTURE OF A SUBDIVIDED SPECIES

In an effort to elucidate the evolutionary mechanisms that determine the genetic architecture of a species, we have analyzed 17 populations of the microcrustacean Daphnia pulex for levels of genetic variation at the level of life‐history characters and molecular markers in the nuclear and mitochondrial genomes. This species is highly subdivided, with approximately 30% of the variation for nuclear molecular markers and 50% of the variation for mitochondrial markers being distributed among populations. The average level of genetic subdivision for quantitative traits is essentially the same as that for nuclear markers, which superficially suggests that the life‐history characters are diverging at the neutral rate. However, the existence of a strong correlation between the levels of population subdivision and broadsense heritabilities of individual traits argues against this interpretation, suggesting instead that the among‐population divergence of some quantitative traits (most notably body size) is being driven by local adaptation to different environments. The fact that the mean phenotypes of the individual populations are also strongly correlated with local levels of homozygosity indicates that variation in local inbreeding plays a role in population differentiation. Rather than being a passive consequence of local founder effects, levels of homozygosity may be selected for directly for their effects on the phenotype (adaptive inbreeding depression). There is no relationship between the levels of variation within populations for molecular markers and quantitative characters, and this is explained by the fact that the average standing genetic variation for life‐history characters in this species is equivalent to only 33 generations of variation generated by mutation.

MUTATION, SELECTION, AND THE MAINTENANCE OF LIFE-HISTORY VARIATION IN A NATURAL POPULATION

In an effort to provide insight into the role of mutation in the maintenance of genetic variance for life‐history traits, we accumulated spontaneous mutations in 10 sets of clonal replicates of Daphnia pulex for approximately 30 generations and compared the variance generated by mutation with the standing level of variation in the wild population. Mutations for quantitative traits appear to arise at a fairly high rate in this species, on the order of at least 0.6 per character per generation, but have relatively small heterozygous effects, changing the phenotype by less than 2.5% of the mean. The mean persistence time of a new mutation affecting life‐history/body‐size traits is approximately 40 generations in the natural population, which requires an average selection coefficient against new mutations of approximately 3% in the heterozygous state. These data are consistent with the idea that the vast majority of standing genetic variance for life‐history characters may be largely a consequence of the recurrent introduction of transient cohorts of mutations that are at least conditionally deleterious and raise issues about the meaning of conventional measures of standing levels of variation for fitness‐related traits.

PATTERNS OF GENETIC ARCHITECTURE FOR LIFE-HISTORY TRAITS AND MOLECULAR MARKERS IN A SUBDIVIDED SPECIES

Abstract Understanding the utility and limitations of molecular markers for predicting the evolutionary potential of natural populations is important for both evolutionary and conservation genetics. To address this issue, the distribution of genetic variation for quantitative traits and molecular markers is estimated within and among 14 permanent lake populations of Daphnia pulicaria representing two regional groups from Oregon. Estimates of population subdivision for molecular and quantitative traits are concordant, with QST generally exceeding GST. There is no evidence that microsatellites loci are less informative about subdivision for quantitative traits than are allozyme loci. Character‐specific comparison of QST and GST support divergent selection pressures among populations for the majority of life‐history traits in both coast and mountain regions. The level of within‐population variation for molecular markers is uninformative as to the genetic variation maintained for quantitative traits. In D. pulicaria, regional differences in the frequency of sex may contribute to variation in the maintenance of expressed within‐population quantitative‐genetic variation without substantially impacting diversity at the genic level. These data are compared to an identical dataset for 17 populations of the temporary‐pond species, D. pulex.

Lack of concordance between genetic diversity estimates at the molecular and quantitative-trait levels

In many applications of population genetics, particularly in the field of conservation biology, estimates of molecular diversity are used as surrogate indicators of less easily acquired measures of genetic variation for quantitative traits. The general validity of this approach to inferring levels of quantitative genetic variation within populations is called into question by the demonstration that estimates of molecular and quantitative-genetic variation are essentially uncorrelated in natural populations of Daphnia, one of the few organisms for which multiple estimates of both quantities are available. On the other hand, molecular measures of population subdivision seem to give conservatively low estimates of the degree of genetic subdivision at the level of quantitative traits. This suggests that although molecular markers provide little information on the level of genetic variation for quantitative traits within populations, they may be valid indicators of population subdivision for such characters.

Rapid evolution in response to introduced predators I: rates and patterns of morphological and life-history trait divergence

BackgroundIntroduced species can have profound effects on native species, communities, and ecosystems, and have caused extinctions or declines in native species globally. We examined the evolutionary response of native zooplankton populations to the introduction of non-native salmonids in alpine lakes in the Sierra Nevada of California, USA. We compared morphological and life-history traits in populations of Daphnia with a known history of introduced salmonids and populations that have no history of salmonid introductions.ResultsOur results show that Daphnia populations co-existing with fish have undergone rapid adaptive reductions in body size and in the timing of reproduction. Size-related traits decreased by up to 13 percent in response to introduced fish. Rates of evolutionary change are as high as 4,238 darwins (0.036 haldanes).ConclusionSpecies introductions into aquatic habitats can dramatically alter the selective environment of native species leading to a rapid evolutionary response. Knowledge of the rates and limits of adaptation is an important component of understanding the long-term effects of alterations in the species composition of communities. We discuss the evolutionary consequences of species introductions and compare the rate of evolution observed in the Sierra Nevada Daphnia to published estimates of evolutionary change in ecological timescales.

The evolution of salinity tolerance in Daphnia: a functional genomics approach.

One route to genetic adaptation in a novel environment is the evolution of ecological generalisation. Yet, identifying the cost that a generalist pays for the increased breadth of tolerance has proven elusive. We integrate phenotypic assays with functional genomics to understand how tolerance to a salinity gradient evolves, and we test the relationship between the fitness cost of this generalisation and the cost of transcription that arises from evolved differences in patterns of gene expression. Our results suggest that a salt-tolerant genotype of Daphnia is characterised by constitutively expressed genes, which does not incur a loss of fitness or a cost of transcription relative to a salt-intolerant genotype in low saline environments. We find that many genes whose expression pattern evolved in response to salinity are also involved in the response to predators, suggesting that the cost of generalisation may be due to trade-offs along other environmental axes.

Functional Biogeography as Evidence of Gene Transfer in Hypersaline Microbial Communities

Background Horizontal gene transfer (HGT) plays a major role in speciation and evolution of bacteria and archaea by controlling gene distribution within an environment. However, information that links HGT to a natural community using relevant population-genetics parameters and spatial considerations is scarce. The Great Salt Lake (Utah, USA) provides an excellent model for studying HGT in the context of biogeography because it is a contiguous system with dispersal limitations due to a strong selective salinity gradient. We hypothesize that in spite of the barrier to phylogenetic dispersal, functional characteristics—in the form of HGT—expand beyond phylogenetic limitations due to selective pressure. Methodology and Results To assay the functional genes and microorganisms throughout the GSL, we used a 16S rRNA oligonucleotide microarray (Phylochip) and a functional gene array (GeoChip) to measure biogeographic patterns of nine microbial communities. We found a significant difference in biogeography based on microarray analyses when comparing Sørensen similarity values for presence/absence of function and phylogeny (Students t-test; p = 0.005). Conclusion and Significance Biogeographic patterns exhibit behavior associated with horizontal gene transfer in that informational genes (16S rRNA) have a lower similarity than functional genes, and functional similarity is positively correlated with lake-wide selective pressure. Specifically, high concentrations of chromium throughout GSL correspond to an average similarity of chromium resistance genes that is 22% higher than taxonomic similarity. This suggests active HGT may be measured at the population level in microbial communities and these biogeographic patterns may serve as a model to study bacteria adaptation and speciation.

The Phenotypic Effects of Spontaneous Mutations in Different Environments

Understanding the context dependence of mutation represents the current frontier of mutation research. In particular, understanding how traits vary in their abilities to accrue mutational variation and how the environment influences expression of mutant phenotypes yields insight into evolutionary processes. We conducted phenotypic assays in four environments using a set of Daphnia pulex mutation accumulation lines to examine the context dependence of mutation. Life-history traits accrued mutational variance faster than morphological traits when considered in individual environments. Across environments, the mutational variance in plasticity was also greater for life-history traits than for morphological traits, although this pattern was less robust. In addition, the expression of mutational variance depended on the environment, which resulted in changes in the rank order of genotype performance across environments in some cases. Such cryptic genetic variation resulting from mutation may maintain genetic diversity and allow for rapid adaptation in spatially or temporally variable environments.

The effect of spontaneous mutations on competitive ability

Understanding the impact of spontaneous mutations on fitness has many theoretical and practical applications in biology. Although mutational effects on individual morphological or life‐history characters have been measured in several classic genetic model systems, there are few estimates of the rate of decline due to mutation for complex fitness traits. Here, we estimate the effects of mutation on competitive ability, an important complex fitness trait, in a model system for ecological and evolutionary genomics, Daphnia. Competition assays were performed to compare fitness between mutation‐accumulation (MA) lines and control lines from eight different genotypes from two populations of Daphnia pulicaria after 30 and 65 generations of mutation accumulation. Our results show a fitness decline among MA lines relative to controls as expected, but highlight the influence of genomic background on this effect. In addition, in some assays, MA lines outperform controls providing insight into the frequency of beneficial mutations.

Species and genotype diversity drive community and ecosystem properties in experimental microcosms

Species diversity is important to ecosystems because of the increased probability of including species that are strong interactors and/or because multiple-species communities are more efficient at using resources due to synergisms and resource partitioning. Genetic diversity also contributes to ecosystem function through effects on primary productivity, community structure and resilience, and modulating energy and nutrient fluxes. Lacking are studies investigating the relationship between ecosystem function and diversity where hierarchical levels of biological diversity are systematically varied during experimentation. In this experiment, we manipulated both species and genotypic diversity of two Daphnia species in microcosms initially seeded with Chlamydomonas and measured community- and ecosystem-level properties to determine which level of diversity was most important for explaining variation in the property. Our results show that species diversity alters bacterial community composition while high genotypic diversity reduces bacterial richness and primary productivity. In addition, the highest levels of genotypic and species richness appear to increase community and ecosystem stability. These findings reveal that species and genotypic diversity are significant drivers of community and ecosystem properties and stability.