Most conspicuous organisms are multicellular and most multicellular organisms develop somatic cells to perform specific, nonre-productive tasks. The ubiquity of this division of labor suggests that it is highly advantageous. In this article I present a model to study the evolution of specialized cells. The model allows for unicellular and multicellular organisms that may contain somatic (terminally differentiated) cells. Cells contribute additively to a quantitative trait. The fitness of the organism depends on this quantitative trait (via a benefit function), the size of the organism, and the number of somatic cells. The model allows one to determine when somatic cells are advantageous and to calculate the optimum number (or fraction) of reproductive cells. I show that the fraction of reproductive cells is always surprisingly high. If somatic cells are very small, they can outnumber reproductive cells but their biomass is still less than the biomass of reproductive cells. I discuss the biology of primitive multicellular organisms with respect to the model predictions. I find a good agreement and outline how this work can be used to guide further quantitative studies of multicellularity.

Although theory indicates that indirect genetic benefits through mate choice should be widespread, empirical work has often either failed to detect the operation of such benefits or shown a net cost to the presence of sexual selection. We tested whether sexual selection can increase the speed with which a conditionally deleterious allele is removed from a laboratory population of Drosophila melanogaster. The alcohol dehydrogenase null allele (Adh-) confers slightly lower viability than wild-type alleles in the absence of ethanol but is lethal in homozygotes when ethanol comprises 6% of the medium. We tracked the frequency of this allele in artificially constructed populations reared at three different levels of ethanol (0%, 2%, and 4%) that either experienced sexual selection or did not. Loss of the deleterious Adh- allele was more rapid when sexual selection was allowed to act, especially in the presence of ethanol. We also quantified the strength of both nonsexual and sexual selection against the Adh- allele using maximum-likelihood estimation. In contrast to recent experiments employing monogamy/polygamy designs, our results demonstrate a fitness benefit to sexual selection. This is consistent with the operation of good-genes female choice.

In genetic polymorphisms of two alleles, heterozygous individuals may contribute to the next generation on average more or fewer descendants than the homozygotes. Two different evolutionary responses that remove a disadvantageous heterozygote phenotype from the population are the evolution of strictly assortative mate choice, and that of a modifier making one of the two alleles completely dominant. We derive invasion fitness of mutants introducing dominance or assortative mate choice in a randomly mating population with a genetic polymorphism for an ecological trait. Mutations with small effects as well as mutants introducing complete dominance or perfect assorting are considered. Using adaptive dynamics techniques, we are able to calculate the ratio of fitness gradients for the effects of a dominance modifier and a mate choice locus, near evolutionary branching points. With equal resident allele frequencies, selection for mate choice is always stronger. Dominance is more strongly selected than assortative mating when the resident (common) alleles have very unequal frequencies at equilibrium. With female mate choice the difference in frequencies where dominance is more strongly selected is smaller than when mutants of both sexes can choose without costs. A symmetric resource-competition model illustrates the results.

Sexual isolation is often assumed to arise because choosy females recognize and reject heterospecific males as mates. Yet in taxa in which both males and females are choosy, males might also recognize and reject heterospecific females. Here, we asked about the relative contribution of the sexes to the strong sexual isolation found in limnetic-benthic species pairs of threespine sticklebacks, which show mutual mate choice. We asked whether males and females of the two species recognize conspecifics and also prefer to mate with them. We found evidence for mate recognition by both sexes but only females prefer conspecifics. The nature of male courtship depended on which species of female they were courting, indicating that males recognized conspecific females and differentiated them from heterospecifics. However, males courted both species of females with equal vigor and changed courtship in a manner that would increase the chance of mating with heterospecifics. Females both recognized conspecifics and strongly preferred them. They responded very little to heterospecific male courtship and almost never mated with them. Therefore, males are likely to undermine sexual isolation, but females uphold it. Despite mutual mate choice and mate recognition in both sexes, females are primarily responsible for sexual isolation in these taxa.

An intersexual conflict arises when males and females differ in their reproductive interests. Although experimental studies have shown that females often mate with dominant males, it may not always be in the interest of a female to do so. Here we investigated the impact of male dominance on female mate choice and offspring growth and survival in the rose bitterling (Rhodeus ocellatus), a freshwater fish with a resource-based mating system. Three experimental mating trials were conducted using males of known dominance rank, but with different levels of constraint on male behavior. Thus, females were able to choose among; (1) males that were isolated from each other; (2) males that could see and smell each other, but could not directly interact; (3) males that could interact fully. Using a combination of behavioral observation and parentage analyses it was shown that female preferences did not correspond with male dominance and that male aggression and dominance constrained female mate choice, resulting in a potential intersexual conflict. The survival of offspring to independence was significantly correlated with female mate preferences, but not with male dominance. A lack of strong congruence in female preference for males suggested a role for parental haplotype compatibility in mate choice.

The spatial distribution of breeding resources can have pronounced demographic and evolutionary consequences. We used 20 experimental groups of the bitterling (Rhodeus amarus), an annual fish with a promiscuous, resource-based mating system, and extended breeding season to investigate how the spatial distribution (clumped or regular) of bitterling oviposition sites (live freshwater mussels) affected offspring production, variation in reproductive success, and directional selection on phenotypic traits over their entire reproductive lifetime. We did not detect any effect of resource distribution on offspring production or variation in reproductive success among individual fish, although variation between replicates was higher with a clumped distribution. This finding is discussed with regard to the incidence of alternative mating behaviors (sneaking) within the limitations imposed by our experimental design. Breeding resource distribution had a significant effect on selection on male phenotypic traits. Stronger directional selection on traits associated with intrasexual competition for fertilizations, gonad mass (an indicator of sperm competition), and the extent of red, carotenoid-based pigment in the iris (an index of dominance status), was detected with a clumped resource distribution. With a regular resource distribution, a stronger positive selection on male body size was detected. We discuss the implications of our results for natural populations.

Sperm morphology varies considerably across taxa, and postcopulatory sexual selection is thought to be one of the main forces responsible for this diversity. Several studies have investigated the effects of the variation in sperm design on sperm function, but the consequences of variation in sperm design on testis morphology have been overlooked. Testes size or architecture may determine the size of the sperm they produce, and selection for longer sperm may require concomitant adaptations in the testes. Relative testes size differs greatly between species and is often used as an index of sperm competition, but little is known about whether larger testes have more sperm-producing tissue or produce sperm at a faster rate. Using a comparative approach in New World Blackbirds (Icteridae), we found (1) a strong link between testis histology and sperm length, suggesting selection on testis architecture through selection on sperm size, and (2) that species under intense sperm competition had a greater proportion of sperm-producing tissue within their testes. These results support the prediction that sperm competition fosters adaptations in reproductive organs that extend beyond testes size, and raise questions about the trade-offs influencing reproductive investment.

Heterozygosity-fitness correlations (HFCs) are increasingly reported but the underlying mechanisms causing HFCs are generally poorly understood. Here, we test for HFCs in roe deer (Capreolus capreolus) using 22 neutral microsatellites widely distributed in the genome and four microsatellites in genes that are potentially under selection. Juvenile survival was used as a proxy for individual fitness in a population that has been intensively studied for 30 years in northeastern France. For 222 juveniles, we computed two measures of genetic diversity: individual heterozygosity (H), and mean d² (relatedness of parental genomes). We found a relationship between genetic diversity and fitness both for the 22 neutral markers and two candidate genes: IGF1 (Insulin-like Growth Factor I) and NRAMP (natural resistance-associated macrophage protein). Statistical evidence and the size of genetic effects on juvenile survival were comparable to those reported for early development and cohort variation, suggesting a substantial influence of genetic components on fitness in this roe deer population. For the 22 neutral microsatellites, a correlation with fitness was revealed for mean d², but not for H, suggesting a possible outbreeding advantage. This heterosis effect could have been favored by introduction of genetically distant (Hungarian) roe deer to the population in recent times and, possibly, by the structuring of the population into distinct clans. The locus-specific correlations with fitness may be driven by growth rate advantages and resistance to diseases known to exist in the studied population. Our analyses of neutral and candidate gene markers both suggest that the observed HFCs are likely mainly due to linkage with dominant or overdominant loci that affect fitness (“local” effect) rather than to a genome-wide relationship with homozygosity due to inbreeding (“general” effect).

After an ancestral population splits into two allopatric populations, different mutations may fix in each. When pairs of mutations are brought together in a hybrid offspring, epistasis may cause reduced fitness. Such pairs are known as Bateson-Dobzhansky-Muller (BDM) incompatibilities. A well-known model of BDM incompatibility due to Orr suggests that the fitness load on hybrids should initially accelerate, and continue to increase as the number of potentially incompatible substitutions increases (the “snowball effect”). In the gene networks model, which violates a key assumption of Orr's model (independence of fixation probabilities), the snowball effect often does not occur. Instead, we describe three possible dynamics in a constant environment: (1) Stabilizing selection can constrain two allopatric populations to remain near-perfectly compatible. (2) Despite constancy of environment, punctuated evolution may obtain; populations may experience rare adaptations asynchronously, permitting incompatibility. (3) Despite stabilizing selection, developmental system drift may permit genetic change, allowing two populations to drift in and out of compatibility. We reinterpret Orr's model in terms of genetic distance. We extend Orr's model to the finite loci case, which can limit incompatibility. Finally, we suggest that neutral evolution of gene regulation in nature, to the point of speciation, is a distinct possibility.

Many insects, other arthropods, and nematodes harbor maternally inherited bacteria inducing “cytoplasmic incompatibility” (CI), reduced egg hatch when infected males mate with uninfected females. Although CI drives the spread of these microbes, selection on alternative, mutually compatible strains in panmictic host populations does not act directly on CI intensity but favors higher “effective fecundity,” the number of infected progeny an infected female produces. We analyze the consequences of host population subdivision using deterministic and stochastic models. In subdivided populations, effective fecundity remains the primary target of selection. For strains of equal effective fecundity, if population density is regulated locally (i.e., “soft selection”), variation among patches in infection frequencies may induce change in the relative frequencies of the strains. However, whether this change favors stronger incompatibility depends on initial frequencies. Demographic fluctuations maintain frequency variation that tends to favor stronger incompatibility. However, this effect is weak; even with small patches, minute increases in effective fecundity can offset substantial decreases in CI intensity. These results are insensitive to many details of host life cycle and migration and to systematic outbreeding or inbreeding within patches. Selection acting through transfer between host species may be required to explain the prevalence of CI.

We investigate evolution of two categories of adaptive host manipulation by trophically transmitted helminths: (1) predation suppression decreases the host's mortality before the helminth is capable of establishing in its next host; (2) predation enhancement increases the existing host's mortality after it can establish in its next host. If all parasite mortality is purely random (time-independent), enhancement must increase predation by the next host sufficiently more (depending on manipulative costs) than it increases the average for all forms of host mortality; thus if host and parasite die only through random predation, manipulation must increase the “right” predation more than the “wrong” predation. But if almost all parasites die in their intermediate host through reaching the end of a fixed life span, enhancement can evolve if it increases the right predation, regardless of how much it attracts wrong predators. Although enhancement is always most favorable when it targets the right host, suppression aids survival to the time when establishment in the next host is possible: it is most favorable if it reduces all aspects of host (and hence parasite) mortality. If constrained to have selective effects, suppression should reduce the commonest form of mortality.

Two hypotheses address the evolution of polyphenic traits in insects. Under the developmental reprogramming model, individuals exceeding a threshold follow a different developmental pathway from individuals below the threshold. This decoupling is thought to free selection to independently hone alternative morphologies, increasing phenotypic plasticity and morphological diversity. Under the alternative model, extreme positive allometry explains the existence of alternative phenotypes and divergent phenotypes are developmentally coupled by a continuous reaction norm, such that selection on either morph acts on both. We test the hypothesis that continuous reaction norm polyphenisms, evolve through changes in the allometric parameters of even the smallest males with minimal trait expression, whereas threshold polyphenisms evolve independent of the allometric parameters of individuals below the threshold. We compare two polyphenic species; the dung beetle Onthophagus taurus, whose allometry has been modeled both as a threshold polyphenism and a continuous reaction norm and the earwig Forficula auricularia, whose allometry is best modeled with a discontinuous threshold. We find that across populations of both species, variation in forceps or horn allometry in minor males are correlated to the population's threshold. These findings suggest that regardless of developmental mode, alternative morphs do not evolve independently of one another.

Evolution of conspicuous signals may be constrained if animal coloration has nonsignaling as well as signaling functions. In aposematic wood tiger moth (Parasemia plantaginis) larvae, the size of a warning signal (orange patch on black body) varies phenotypically and genetically. Although a large warning signal is favored as an antipredator defense, we hypothesized that thermoregulation may constrain the signal size in colder habitats. To test this hypothesis, we conducted a factorial rearing experiment with two selection lines for larval coloration (small and large signal) and with two temperature manipulations (high and low temperature environment). Temperature constrained the size and brightness of the warning signal. Larvae with a small signal had an advantage in the colder environment, which was demonstrated by a faster development time and growth rate in the low temperature treatment, compared to larvae with a large signal. Interestingly, the larvae with a small signal were found more often on the plant than the ones with a large signal, suggesting higher basking activity of the melanic (small signal) individuals in the low temperature. We conclude that the expression of aposematic display is not only defined by its efficacy against predators; variation in temperature may constrain evolution of a conspicuous warning signal and maintain variation in it.

Leaf shapes reflect complex assemblages of shape-determining elements, yet evolutionary studies tend to treat leaf shape as a single attribute, for example cordate or linear. As with all complex structures, individual elements of a leaf could theoretically evolve independently and at different rates to the extent permitted by genetic and functional limitations. We examined relative evolutionary lability of shape-determining elements in the highly diverse South African plant genus Pelargonium (Geraniaceae). We used SIMMAP to calculate Bayesian posterior probabilities for ancestral states of leaf-shape characters for major nodes across multiple phylogenetic trees. Trees were derived from a Bayesian analysis of DNA sequence data from four partitions. We found that shape elements differed in rates of character-state transformations across the tree. Leaf base, apex, and overall outline had low rates. Transformations in venation occurred at slightly higher rates and were associated with shifts in venation among major clades. Leaf margin type and overall leaf size showed intermediate rates, whereas high rates were observed in the extent of lamina lobing and functional leaf size. The results indicate that suites of elements characteristic of the recently evolved xerophytic lineage, for example pinnate venation, dissected lamina, and entire margins, were acquired piecemeal over nested levels of the phylogeny.

Using an explicit phylogenetic framework, ontogenetic patterns of leaf form are compared among the three genera of marsileaceous ferns (Marsilea, Regnellidium, and Pilularia) with the outgroup Asplenium to address the hypothesis that heterochrony played a role in their evolution. We performed a Fourier analysis on a developmental sequence of leaves from individuals of these genera. Principal components analysis of the harmonic coefficients was used to characterize the ontogenetic trajectories of leaf form in a smaller dimensional space. Results of this study suggest that the “evolutionary juvenilization” observed in these leaf sequences is best described using a mixed model of heterochrony (accelerated growth rate and early termination at a simplified leaf form). The later stages of the ancestral, more complex, ontogenetic pattern were lost in Marsileaceae, giving rise to the simplified adult leaves of Marsilea, Regnellidium, and Pilularia. Life-history traits such as ephemeral and uncertain habitats, high reproductive rates, and accelerated maturation, which are typical for marsileaceous ferns, suggest that they may be “r strategists.” The evidence for heterochrony presented here illustrates that it has resulted in profound ecological and morphological consequences for the entire life history of Marsileaceae.

The completion of the Panamanian Isthmus is one of the greatest natural experiments in evolution, sending multiple species pairs from a broad range of taxonomic groups on independent evolutionary trajectories. The resulting transisthmian sister species have been used as model systems for examining consequences that accompany cessation of gene flow in formerly panmictic populations. However, variance in pairwise genetic distances of these “geminates” often exceeds expectations, seemingly conflicting with the assumption that separation of populations was contemporaneous with the final closure of the Isthmus. Multilocus datasets and coalescent-based analytical methods can be used to estimate divergence times while accounting for variance in gene divergence that predates isolation, thus removing the need to invoke unequal divergence times. Here we present results from Bayesian analyses of sequence data from seven nuclear and one mitochondrial marker in eight transisthmian species pairs in the snapping shrimp genus Alpheus. Divergence times in two species pairs were shown to occur much earlier than the Isthmus final closure, but much of the variance in pairwise genetic distances from cytochrome oxidase I (COI) was explained when ancestral polymorphisms were accounted for. Results illustrate how coalescent approaches may be more appropriate for dating recent divergences than for estimating ancient speciation events.

The Price equation is recognized as a general statistical description of evolutionary change with the potential to represent diverse processes. Here we present a new structurally symmetric equation for change that allows for arbitrary causal connectivity between ancestors and descendants, accounts for previously unaddressed processes (such as migration), and yields the Price equation as a special case.

Adaptation to temporal variation in environmental conditions is widespread. Whether evolution in a constant environment alters adaptation to temporal variation is relatively unexplored. We examine how constant and diurnally fluctuating temperature conditions affect life-history traits in two populations of the tobacco hornworm, Manduca sexta: a field population that routinely experiences fluctuating temperatures; and a laboratory population (derived from this field population in the 1960s) maintained at a constant temperature for more than 250 generations. Our experiments demonstrate that diurnal fluctuations significantly alter body size and development time in both populations, and confirm that these populations differ in their responses to a mean temperature. However, we found no evidence for population divergence in responses to diurnal temperature fluctuations. We suggest that mean and extreme temperatures may act as more potent selective forces on thermal reaction norms than temperature variation per se.

Little is known about the population structure of social microorganisms, yet such studies are particularly interesting for the ways that genetic variation impacts their social evolution. Dictyostelium, a eukaryotic microbe widely used as a developmental model, has a social fruiting stage in which some formerly independent individuals die to help others. To assess genetic variation within the social amoeba Dictyostelium purpureum, we sequenced ∼4000 base pairs of ribosomal DNA (rDNA) from 37 isolates collected in Texas, Virginia, and Japan. Our analysis showed extensive genetic variation between populations and clear evidence of phylogenetic structure. We identified three major phylogenetic groups that were more different than other accepted species pairs. Tests using pairs of clones showed that both sexual macrocyst and asexual fruiting body formation were influenced by genetic divergence. Macrocysts were less likely to form between pairs of clones from different groups than from the same group. There was also a correlation between the genetic divergence of a pair of clones and their degree of mixing within fruiting bodies. These observations suggest that cryptic species might occur within D. purpureum and, more importantly, reveal how genetic variation impacts social interactions.

The development of isolation by distance (IBD) and isolation by time (IBT) was contrasted among demes of European grayling (Thymallus thymallus) that have diverged within the last 25 generations following colonization of a lake (Lesjaskogsvatnet). We find low but significant levels of genetic differentiation among spawning tributaries and a pattern of IBD among them. We do not, however, find evidence for IBT despite an up to four-week difference in spawning date between “warm/early” and “cold/late” spawning demes and differences in the incubation temperatures experienced by offspring. It appears that IBD has developed more rapidly than IBT in this system and that adaptive divergence has been initiated in the absence of IBT. Although analysis of selected loci could reveal reduced recombination in parts of the genome associated with temporal divergence, our analysis of neutral genetic data suggests that IBD is a more important isolating mechanism in the early stages of adaptive divergence in European grayling.