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Patel MN, Knight CG, Karageorgi C, et al., 2002, Evolution of germ-line signals that regulate growth and aging in nematodes, PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICA, Vol: 99, Pages: 769-774, ISSN: 0027-8424
We show that a signal from the germ line represses growth in the nematode Caenorhabditis elegans. Laser-microbeam ablation of cells that give rise to the germ line causes adults to become giant. Ablation of these cells in self-sterile mutant worms also causes gigantism, suggesting that the germ line represses growth because it is the source of a growth-antagonizing signal rather than because of a sink of resources required for reproduction. The C. elegans germ line also emits a signal that represses longevity. This longevity-repressing signal requires the activity of DAF-16, a forkhead/winged-helix transcription factor, but we find that that the growth-repressing signal does not. The growth-repressing signal also does not require the activity of DBL-1, a transforming growth factor beta-related protein that promotes growth in worms. By ablating the germ-line precursors of other species of free-living nematodes, we also found that both the growth-repressing and longevity-repressing signals are evolutionarily variable. Some species have both signals; others have just one or the other. We suggest that variation in germ-line signaling contributes to body size and life-history diversity in the nematodes.
Darwin observed that multiple, lowly organized, rudimentary, or exaggerated structures show increased relative variability. However, the cellular basis for these laws has never been investigated. Some animals, such as the nematode Caenorhabditis elegans, are famous for having organs that possess the same number of cells in all individuals, a property known as eutely. But for most multicellular creatures, the extent of cell number variability is unknown. Here we estimate variability in organ cell number for a variety of animals, plants, slime moulds, and volvocine algae. We find that the mean and variance in cell number obey a power law with an exponent of 2, comparable to Taylor's law in ecological processes. Relative cell number variability, as measured by the coefficient of variation, differs widely across taxa and tissues, but is generally independent of mean cell number among homologous tissues of closely related species. We show that the power law for cell number variability can be explained by stochastic branching process models based on the properties of cell lineages. We also identify taxa in which the precision of developmental control appears to have evolved. We propose that the scale independence of relative cell number variability is maintained by natural selection.
Knight CG, Azevedo RBR, Leroi AM, et al., 2001, Testing life-history pleiotropy in Caenorhabditis elegans, EVOLUTION, Vol: 55, Pages: 1795-1804, ISSN: 0014-3820
Much life-history theory assumes that alleles segregating in natural populations pleiotropically affect life-history traits. This assumption, while plausible, has rarely been tested directly. Here we investigate the genetic relationship between two traits often suggested to be connected by pleiotropy: maternal body size and fertility. We carry out a quantitative trait locus (QTL) analysis on two isolates of the free-living nematode Caenorhabditis elegans, and identify two body size and three fertility QTLs. We find that one of the fertility QTLs colocalizes with the two body size QTLs on Chromosome IV. Further analysis, however, shows that these QTLs are genetically separable. Thus, none of the five body size or fertility QTLs identified here shows detectable pleiotropy for the assayed traits. The evolutionary origin of these QTLs, possible candidate loci, and the significance for life-history evolution are discussed.
Life history tradeoffs are often thought to be caused by the allocation of limited resources among competing traits such as reproduction, somatic growth and maintenance. One line of evidence supporting this comes from eliminating reproduction, for example, by surgically removing gonads. However, recent evidence from the nematode Caenorhabditis elegans suggests that the apparent tradeoffs it shows might not be due to resource allocation at all but rather to the effects of a molecular signal originating in the germ line that represses longevity. These results should cause us to rethink the interpretation of many classic experiments in life history evolution.
Nematodes are generally considered to have an adult cell number that does not vary among wildtype individuals as a consequence of invariant cell lineages (eutely). However, there is extensive evidence that at least some cell lineages can be variable in nematodes. In a comparative study of 13 free-living nematode species, we have shown that the adult epidermis of most species contained variable numbers of nuclei and that this variance was positively correlated with mean epidermal nuclear number. Here we present simulations of the lateral seam cell lineages of four species and show that variance in cell number is influenced by lineage topology, as well as by the frequency of lineage variants. We show that the epidermal variability of Panagrellus redivivus cannot be accounted for by the complexity of its lineage, but requires higher levels of lineage variability than are found in Caenorhabditis elegans, Oscheius myriophila and Rhabditella octopleura. Our findings suggest that many nematodes may have tissues composed of indeterminate numbers of cells formed from variable lineages and, as such, resemble other metazoans.
Flemming AJ, Shen ZZ, Cunha A, et al., 2000, Somatic polyploidization and cellular proliferation drive body size evolution in nematodes, PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICA, Vol: 97, Pages: 5285-5290, ISSN: 0027-8424
Most of the hypodermis of a rhabditid nematode such as Caenorhabditis elegans is a single syncytium. The size of this syncytium (as measured by body size) has evolved repeatedly in the rhabditid nematodes. Two cellular mechanisms are important in the evolution of body size: changes in the numbers of cells that fuse with the syncytium, and the extent of its acellular growth. Thus nematodes differ from mammals and other invertebrates in which body size evolution is caused by changes in cell number alone. The evolution of acellular syncytial growth in nematodes is also associated with changes in the ploidy of hypodermal nuclei. These nuclei are polyploid as a consequence of iterative rounds of endoreduplication, and this endocycle has evolved repeatedly. The association between acellular growth and endoreduplication is also seen in C. elegans mutations that interrupt transforming growth factor-beta signaling and that result in dwarfism and deficiencies in hypodermal ploidy. The transforming growth factor-beta pathway is a candidate for being involved in nematode body size evolution.
In this paper, I argue that the ultimate causes of morphological, and hence developmental, evolution are scale independent. In other words, micro- and macroevolutionary patterns show fundamental similarities and therefore are most simply explained as being caused by the same kinds of evolutionary forces. I begin by examining the evolution of single lineages and argue that dynamics of adaptive evolution are the same for bacteria in test-tube evolution experiments and fossil lineages. Similarly, I argue that the essential features of adaptive radiations large and small can be attributed to conventional forces such as mutation and diversifying natural selection due to competition. I then address recent claims that the molecular features of metazoan development are the result of clade-level selection for evolvability, and suggest that these features can be more easily explained by conventional individual-level selection for the suppression of deleterious pleiotropic effects. Finally, I ask what must be known if we are to understand the ultimate causes of molecular and developmental diversity.
Leroi AM, 1999, Leonardo's mountain of clams and the diet of worms, TLS-THE TIMES LITERARY SUPPLEMENT, Pages: 28-28, ISSN: 0307-661X
Leroi AM, Leroi AM, Leroi AM, 1998, The origin of animal body plans: a study in evolutionary developmental biology, by w. Arthur, and cells, embryos and evolution, by j. Gerhart and m. Kirschner., Trends Ecol Evol, Vol: 13, Pages: 82-83, ISSN: 0169-5347
Cambridge University Press, 1997. $64.95/£45.00hbk (xii +338 pages) ISBN 0 521 55014 9 Blackwell Science, 1997. $49.50/£29.50pbk (xi +642 pages) ISBN 0 865 42574 4.
Chippindale AK, Leroi AM, Saing H, et al., 1997, Phenotypic plasticity and selection in Drosophila life history evolution .2. Diet, mates and the cost of reproduction, JOURNAL OF EVOLUTIONARY BIOLOGY, Vol: 10, Pages: 269-293, ISSN: 1010-061X
Shiotsugu J, Leroi AM, Yashiro H, et al., 1997, The symmetry of correlated selection responses in adaptive evolution: An experimental study using Drosophila, EVOLUTION, Vol: 51, Pages: 163-172, ISSN: 0014-3820
The relationship between the processes of density-dependent and age-specific selection has been investigated by examining a common phenotype, urea resistance, which has apparently evolved in response to each of these selection mechanisms. Twenty populations that have experienced differing levels of age-specific selection show differences in egg-to-adult viability in environments with high levels of urea. Among this group of populations, it appears that resistance to urea is correlated with longevity, but not development time. Ten populations kept at extreme larval densities for many generations also show responses to urea: those kept at high larval densities appear to be most resistant to urea. However, these populations show no differences in adult longevity. An additional five populations were selected directly for urea resistance by adding this compound to the larval food environment. Again, there was a strong response to this artificial selection, with urea resistance increasing dramatically, but these populations showed no response in adult longevity or resistance to crowding when compared to five control populations. There is clearly no simple relationship between longevity and larval urea resistance. It may be that age-specific and density-dependent selection induce similar changes in this phenotype, but do so through different genetic and physiological pathways. We suggest that these data are not consistent with the view of constant and symmetric genetic variance-covariance matrices. These data support a more prominent role for observations of evolutionary trajectories rather than static measurements of genetic components of variance.
LEROI AM, BENNETT AF, LENSKI RE, et al., 1994, TEMPERATURE-ACCLIMATION AND COMPETITIVE FITNESS - AN EXPERIMENTAL TEST OF THE BENEFICIAL ACCLIMATION ASSUMPTION, PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICA, Vol: 91, Pages: 1917-1921, ISSN: 0027-8424
Phenotypic acclimation is generally assumed to confer an advantage in the environment that stimulates the response. To test this beneficial acclimation assumption explicitly, we investigated the consequences of temperature acclimation for the fitness of Escherichia coli at two temperatures, 32 degrees C and 41.5 degrees C. Both temperatures permit growth and long-term persistence of the genotypes in serial culture. We found that prior acclimation to 32 degrees C, relative to acclimation to 41.5 degrees C, enhanced fitness at 32 degrees C, consistent with the assumption. But prior acclimation to 41.5 degrees C actually reduced fitness at 41.5 degrees C, relative to acclimation to 32 degrees C. Hence, the assumption that acclimation always confers an advantage is demonstrated to be false. Acclimation to 41.5 degrees C did, however, improve survival at 50 degrees C, a lethal temperature. This protective response has been shown to be associated with the induction of stress proteins. The reduced competitive fitness caused by acclimation at 41.5 degrees C may reflect a physiological burden associated with expression of stress proteins when they are not needed to prevent lethal damage. Whatever the cause, acclimation to the higher temperature decreased competitive fitness at that temperature.
LEROI AM, CHEN WR, ROSE MR, et al., 1994, LONG-TERM LABORATORY EVOLUTION OF A GENETIC LIFE-HISTORY TRADE-OFF IN DROSOPHILA-MELANOGASTER .2. STABILITY OF GENETIC CORRELATIONS, EVOLUTION, Vol: 48, Pages: 1258-1268, ISSN: 0014-3820
Experiments in laboratory populations of Drosophila melanogaster have shown a negative genetic correlation between early-life fecundity on the one hand and starvation resistance and longevity on the other. Selection for late-life reproductive success resulted in long-lived populations that had increased starvation resistance but diminished early-life fecundity relative to short-lived controls. This pattern of differentiation proved, however, to be unstable. When assayed in a standard high-fecundity environment, the relative early fecundity of the long- and short-lived stocks reversed over a decade. That is, the long-lived populations came to have greater relative early-life fecundity, late-life fecundity, longevity and starvation resistance. Nevertheless, when these populations were assayed in other assay environments, the original trade-off was still present. We investigated the genetic structure of the short- and long-lived populations, to ask whether the inconstancy of the trade-off, as inferred from among population comparisons, is reflected in the pattern of genetic correlations within populations. For this purpose, lines from each of the short- and long-lived populations that had been selected for starvation resistance were compared with unselected controls. The direct and correlated responses of these starvation selected populations suggest that (1) the original genetic trade-off was still present in the ancestral short- and long-lived populations, even when it was no longer apparent from their comparison; (2) the trade-off was present in both assay environments; and (3) selectable genotype × environment variation exists for early fecundity. We suggest that a failure of the pattern of differentiation among populations to reflect the pattern of genetic correlations, if common in natural populations, will prevent the reliable inference of genetic trade-offs from comparisons of most natural populations.
LEROI AM, CHIPPINDALE AK, ROSE MR, et al., 1994, LONG-TERM LABORATORY EVOLUTION OF A GENETIC LIFE-HISTORY TRADE-OFF IN DROSOPHILA-MELANOGASTER .1. THE ROLE OF GENOTYPE-BY-ENVIRONMENT INTERACTION, EVOLUTION, Vol: 48, Pages: 1244-1257, ISSN: 0014-3820
Trade-offs among life-history traits are often thought to constrain the evolution of populations. Here we report the disappearance of a trade-off between early fecundity on the one hand, and late-life fecundity, starvation resistance, and longevity on the other, over 10 yr of laboratory selection for late-life reproduction. Whereas the selected populations showed an initial depression in early-life fecundity, they later converged upon the controls and then surpassed them. The evolutionary loss of the trade-off among life-history traits is considered attributable to the following factors: (1) the existence of differences in the culture regimes of the short- and long-generation populations other than the demographic differences deliberately imposed; (2) adaptation of one or both of these sets of populations to the unique aspects of their culture regimes; (3) the existence of an among-environment trade-off in the expression of early fecundity in the two culture regimes, as reflected in assays that mimic those regimes. The trade-off between early and late-life reproductive success, as manifest among divergently selected populations, is apparent or not depending on the assay environment. This demonstration that strong genotype-by-environment interactions can obscure a fundamental trade-off points to the importance of controlling all aspects of the culture regime of experimental populations and the difficulty of doing so even in the laboratory.
LEROI AM, KIM SB, ROSE MR, et al., 1994, THE EVOLUTION OF PHENOTYPIC LIFE-HISTORY TRADE-OFFS - AN EXPERIMENTAL-STUDY USING DROSOPHILA-MELANOGASTER, AMERICAN NATURALIST, Vol: 144, Pages: 661-676, ISSN: 0003-0147
LEROI AM, LENSKI RE, BENNETT AF, et al., 1994, EVOLUTIONARY ADAPTATION TO TEMPERATURE .3. ADAPTATION OF ESCHERICHIA-COLI TO A TEMPORALLY VARYING ENVIRONMENT, EVOLUTION, Vol: 48, Pages: 1222-1229, ISSN: 0014-3820
Six lines of the bacterium Escherichia coli were propagated for 2,000 generations in a temporally varying environment. The imposed environmental regime consisted of alternating days at 32°C and 42°C, with rapid transitions between them. These derived lines are competitively superior to their ancestor in this variable temperature regime. We also measured changes in the fitness of these lines, relative to their common ancestor, in both the constant (32°C and 42°C) and transition (from 32°C to 42°C and from 42°C to 32°C) components of this temporally varying environment, to determine whether the bacteria had adapted to the particular constant temperatures or the transitions between them, or both. The experimentally evolved lines had significantly improved fitness in each of the constant environmental components (32°C and 42°C). However, the experimental lines had not improved in making the sudden temperature transitions that were a potentially important aspect of the temporally variable environment. In fact, fitness in making at least one of the transitions (between 32°C and 42°C) unexpectedly decreased. This reduced adaptation to the abrupt transitions between these temperatures is probably a pleiotropic effect of mutations that were responsible for the increased fitness at the component temperatures. Among the six experimental lines, significant heterogeneity occurred in their adaptation to the constant and transition components of the variable environment.
LEROI AM, ROSE MR, LAUDER GV, et al., 1994, WHAT DOES THE COMPARATIVE METHOD REVEAL ABOUT ADAPTATION, AMERICAN NATURALIST, Vol: 143, Pages: 381-402, ISSN: 0003-0147
CHIPPINDALE AK, LEROI AM, KIM SB, et al., 1993, PHENOTYPIC PLASTICITY AND SELECTION IN DROSOPHILA LIFE-HISTORY EVOLUTION .1. NUTRITION AND THE COST OF REPRODUCTION, JOURNAL OF EVOLUTIONARY BIOLOGY, Vol: 6, Pages: 171-193, ISSN: 1010-061X
The historical definition of adaptations has come into wide use as comparative biologists have applied methods of phylogenetic analysis to a variety of evolutionary problems. Here we point out a number of difficulties in applying historical methods to the study of adaptation, especially in cases where a trait has arisen but once. In particular, the potential complexity of the genetic correlations among phenotypic traits, performance variables and fitness makes inferring past patterns of selection from comparative data difficult. A given pattern of character distribution may support many alternative hypotheses of mechanism. While phylogenetic data are limited in their ability to reveal evolutionary mechanisms, they have always been an important source of adaptive hypotheses and will continue to be so.
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