Niles Lehman

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.

Spontaneous network formation among cooperative RNA replicators

The origins of life on Earth required the establishment of self-replicating chemical systems capable of maintaining and evolving biological information. In an RNA world, single self-replicating RNAs would have faced the extreme challenge of possessing a mutation rate low enough both to sustain their own information and to compete successfully against molecular parasites with limited evolvability. Thus theoretical analyses suggest that networks of interacting molecules were more likely to develop and sustain life-like behaviour. Here we show that mixtures of RNA fragments that self-assemble into self-replicating ribozymes spontaneously form cooperative catalytic cycles and networks. We find that a specific three-membered network has highly cooperative growth dynamics. When such cooperative networks are competed directly against selfish autocatalytic cycles, the former grow faster, indicating an intrinsic ability of RNA populations to evolve greater complexity through cooperation. We can observe the evolvability of networks through in vitro selection. Our experiments highlight the advantages of cooperative behaviour even at the molecular stages of nascent life.

The RNA World: molecular cooperation at the origins of life

The RNA World concept posits that there was a period of time in primitive Earths history — about 4 billion years ago — when the primary living substance was RNA or something chemically similar. In the past 50 years, this idea has gone from speculation to a prevailing idea. In this Review, we summarize the key logic behind the RNA World and describe some of the most important recent advances that have been made to support and expand this logic. We also discuss the ways in which molecular cooperation involving RNAs would facilitate the emergence and early evolution of life. The immediate future of RNA World research should be a very dynamic one.

A morphologic and genetic study of the Island fox, Urocyon littoralis

The Island Fox, Urocyon littoralis, is a dwarf form found on six of the Channel Islands located 30–98 km off the coast of southern California. The island populations differ in two variables that affect genetic variation: effective population size and duration of isolation. We estimate that the effective population size of foxes on the islands varies from approximately 150 to 1,000 individuals. Archeological and geological evidence suggests that foxes likely arrived on the three northern islands minimally 10,400–16,000 years ago and dispersed to the three southern islands 2,200–4,300 years ago. We use morphometrics, allozyme electrophoresis, mitochondrial DNA (mtDNA) restriction‐site analysis, and analysis of hypervariable minisatellite DNA to measure variability within and distances among island fox populations. The amount of within‐population variation is lowest for the smallest island populations and highest for the mainland population. However, the larger populations are sometimes less variable, with respect to some genetic measures, than expected. No distinct trends of variability with founding time are observed. Genetic distances among the island populations, as estimated by the four techniques, are not well correlated. The apparent lack of correspondence among techniques may reflect the effects of mutation rate and colonization history on the values of each genetic measure.

Major histocompatibility complex variation at three class II loci in the northern elephant seal

Northern elephant seals were hunted to near extinction in the 19th century, yet have recovered remarkably and now number around 175 000. We surveyed 110 seals for single‐strand conformation polymorphism (SSCP) and sequence variation at three major histocompatibility (MHC) class II loci (DQA, DQB and DRB) to evaluate the genetic consequences of the population bottleneck at these loci vs. other well‐studied genes. We found very few alleles at each MHC locus, significant variation among breeding sites for the DQA locus, and linkage disequilibrium between the DQB and DRB loci. Northern elephant seals are evidently inbred, although there is as yet no evidence of correlative reductions in fitness.

Allozyme and mtDNA variation in populations of the Daphnia pulex complex from both sides of the Rocky Mountains

Long-distance dispersal of diapausing eggs by migratory waterfowl is one factor thought to be responsible for the macrogeographical homogeneity of allozyme frequencies in species of the Daphnia pulex complex. If so, populations on either side of the Rocky Mountains are expected to be divergent because few major flyways cross them. To test this prediction, Daphnia populations from lakes and ponds across eastern Oregon were surveyed for mtDNA and allozyme variation. The data were analysed with previously collected data from populations in the midwest U.S. Phenetic analysis of the allozyme data clustered the populations into four discrete groups, which correspond to habitat: permanent lakes, ponds in the midwest, coastal and valley ponds in Oregon and sand dune ponds in Oregon. A recent taxonomic revision by Hebert suggests that these groups correspond to D. pulicaria, D. pulex, D. arenata and D. melanica, respectively. Cladistic analysis of mtDNA variation revealed the same groups except that mtDNA haplotypes from the D. pulex and D. pulicaria populations formed a single clade. All four species were significantly subdivided with respect to allozyme markers, but there were no clear differences between D. pulicaria populations on either side of the Rocky Mountains, suggesting that they are not a barrier to gene flow in this species. Whereas mtDNA differentiation among D. pulicaria populations was not significant, the pond-dwelling species, D. pulex and D. arenata, showed even greater differentiation for mtDNA than for allozymes. It is suggested that extinction/recolonization events occur more frequently in pond vs. lake habitats and have a greater impact on the subdivision of mtDNA variation because of the haploid, maternal inheritance of the mitochondrial genome.

A case for the extreme antiquity of recombination.

Recombination is usually assumed to be a mode of reproduction that evolved long after asexual reproduction in response to specific genetic and environmental circumstances. Here the argument is made that recombination was an evolutionary development as ancient as the origins of life. To support this proposition four lines of evidence are given, in particular, the need for primordial genomes to acquire substantial length and to escape from Muller’s Ratchet.

Multi-locus genetic evidence for rapid ecologically based speciation in Daphnia

The process of speciation involves the divergence of two or more subpopulations of a parent species into independent evolutionary trajectories. To study this process in natural populations requires a detailed knowledge of the genetic and ecological characteristics of the parent species and an understanding of how its populations can lose evolutionary cohesion. The cosmopolitan and speciose genus Daphnia provides many of these features by existing in multiple freshwater habitat types, particularly permanent lakes and temporary ponds, each of which presents distinct ecological challenges. We assayed the genetic composition of 20 temporary pond populations of members of the Daphnia pulex species complex in north‐western Oregon and compared them to published data on related lake and pond populations. We collected molecular genetic data from 13 allozyme loci, from six microsatellite loci, and from the control region of the mitochondrial DNA. By assaying over 400 individual Daphnia for these data, we were able to compile composite genotypes not only of individual Daphnia but of each pond population as a whole. In these ponds, we discovered two distinct genotypic constellations, one which bears resemblance to the lake‐dwelling taxon D. pulicaria, and one which bears resemblance to the pond‐dwelling taxon, D. pulex. Using published genetic data from these and other species as a frame of reference, we characterized 13 of these ponds as being ‘pond‐like’, three as being ‘lake‐like’, and four as being ‘mixed’. Unlike studies performed elsewhere, however, these ponds do not exhibit high probabilities of interspecific hybridization. Over 95% of all individuals have either a lake‐like or a pond‐like genotype at all three genetic systems, suggesting the two forms do not represent hybridized vs. nonhybridized genotypes. Because both types can be found in the same ponds at the same time in gametic disequilibrium, we also discount the possibility that they are two extremes of a single species that is highly genetically subdivided. With these genetic data, and with supporting life‐history and ecological data previously gathered on these pond populations, we conclude that the most likely description of this system is of a taxon caught in the act of speciating, with new pond‐adapted populations periodically stemming from lake‐adapted sources during river flooding events.

A recombination-based model for the origin and early evolution of genetic information.

Recombination is the exchange of groups of subunits between two entities. It is argued here that this process was central to the origin of life, because it allowed for the creation of useful information from a random pool of linear polymers. The length distribution of such a pool could be broadened if these polymers, such as RNA strands, have the capability of interacting and performing a cross‐strand nucleophilic attack of a hydroxy group on a phosphate. Both the formation of stable secondary structures such as stem‐loops and selection for self‐replication can operate to push the equilibrium length distribution of the pool to longer and more catalytically proficient oligomers. There is empirical and theoretical support for these operations. Finally, in a collection of recombining linear oligomers, the advent of short recognition sequences that favor certain interactions over others, the property of a genotypic ‘self’ could develop, which later can shed its collective nature and be subject to Darwinian evolution. This could have given rise to true replicase enzymes, for example.

Assessing the likelihood of recurrence during RNA evolution in vitro

Recurrence is the possibility of resulting in the same endpoint multiple times when a living system is allowed to evolve repeatedly starting from a given initial point. This concept is of concern to both evolutionary theoreticians and molecular biologists who use nucleic acid selection techniques to mimic biotic and computorial processes in the test tube. Using the continuous in vitro evolution methodology, many replicate experimental evolutionary lineages with populations of catalytic RNA were performed to gain insight into the parameters that could affect recurrence. The likelihood that the same genotype will result in parallel trials of an evolution experiment in vitro depends on several factors, including the phenotype under selection, the size and composition of the initial diverse pool of nucleic acids used in the experiment, the degree of mutation possible during the experiment, the shape of the fitness landscape through which the population evolves, and the strategies used to invoke selection and to search the landscape, among others. By considering these factors, it can be predicted that recurrence is more likely when a small, wild-type-based starting pool is used with efficient selection and search strategies involving little online mutagenesis within a rugged adaptive landscape with a strong local optimum. The recurrence experiments performed here on the 150-nucleotide ligase ribozyme demonstrate that it repeatedly jumps from one peak in a fitness landscape to another, apparently hurdling a deep fitness valley. These predictions can and should be tested by additional multiple replicates of actual evolution experiments in the laboratory.