Speciation in peripheral populations: effects of drift load and mating systems.

Speciation in peripheral populations has long been considered one of the most plausible scenarios for speciation with gene flow. In this study, however we identify two additional problems of peripatric speciation, as compared to the parapatric case, that may impede the completion of the speciation process for most parameter regions. First, with (predominantly) unidirectional gene flow, there is no selection pressure to evolve assortative mating on the continent. We discuss the implications of this for different mating schemes. Second, genetic load can build up in small populations. This can lead to extinction of the peripheral species, or generate selection pressure for lower assortative mating to avoid inbreeding. In this case, either a stable equilibrium with intermediate assortment evolves or there is cycling between phases of hybridization and phases of complete isolation.

The interpretation of selection coefficients.

Evolutionary biologists have an array of powerful theoretical techniques that can accurately predict changes in the genetic composition of populations. Changes in gene frequencies and genetic associations between loci can be tracked as they respond to a wide variety of evolutionary forces. However, it is often less clear how to decompose these various forces into components that accurately reflect the underlying biology. Here, we present several issues that arise in the definition and interpretation of selection and selection coefficients, focusing on insights gained through the examination of selection coefficients in multilocus notation. Using this notation, we discuss how its flexibility-which allows different biological units to be identified as targets of selection-is reflected in the interpretation of the coefficients that the notation generates. In many situations, it can be difficult to agree on whether loci can be considered to be under "direct" versus "indirect" selection, or to quantify this selection. We present arguments for what the terms direct and indirect selection might best encompass, considering a range of issues, from viability and sexual selection to kin selection. We show how multilocus notation can discriminate between direct and indirect selection, and describe when it can do so.

The role of linkage disequilibrium in the evolution of premating isolation.

The suggestion that speciation may often occur, or be completed, in the presence of gene flow has long been contentious, due to an appreciation of the challenges to maintaining population- or species-specific gene combinations when gene flow is occurring. Linkage disequilibrium between loci involved in postzygotic and premating isolation must often be built and maintained as the source of these species-specific genotypes. Here, I discuss proposed solutions to facilitate the establishment and maintenance of this linkage disequilibrium. I concentrate primarily on two such factors: one-allele versus two-allele mechanisms of premating isolation, and the form of selection against hybrids as it relates to its effect on the pathway between postzygotic and prezygotic isolation. The goal of this discussion is not to thoroughly review these factors, but instead to concentrate on aspects and implications of these solutions that are currently underemphasized in the speciation literature.

The evolution of conspecific gamete precedence and its effect on reinforcement.

Conspecific gamete precedence, the usage of conspecific sperm by a female that mates with both a conspecific and a heterospecific male, has been found in many taxa. We construct a population genetic model to examine the evolution of conspecific gamete precedence and its coevolution with premating isolation in the process of reinforcement. Our findings suggest that conspecific gamete precedence can evolve via a process very similar to reinforcement. We explore the nature of the selection against hybridization necessary to drive this evolution. Moreover, our results confirm the prediction of Marshall et al. (Trends Ecol. Evol. 2002;17:558-563) that conspecific gamete precedence will inhibit the evolution of reinforcement between two species. We further find that reinforcement will inhibit the evolution of conspecific gamete precedence. Both reinforcement and conspecific gamete precedence increase reproductive isolation and contribute to the process of speciation. We discuss factors that may affect which of these phenomena are likely to become predominant between incipient species.

To eject or to abandon? Life history traits of hosts and parasites interact to influence the fitness payoffs of alternative anti-parasite strategies.

Hosts either tolerate avian brood parasitism or reject it by ejecting parasitic eggs, as seen in most rejecter hosts of common cuckoos, Cuculus canorus, or by abandoning parasitized clutches, as seen in most rejecter hosts of brown-headed cowbirds, Molothrus ater. What explains consistent variation between alternative rejection behaviours of hosts within the same species and across species when exposed to different types of parasites? Life history theory predicts that when parasites decrease the fitness of host offspring, but not the future reproductive success of host adults, optimal clutch size should decrease. Consistent with this prediction, evolutionarily old cowbird hosts, but not cuckoo hosts, have lower clutch sizes than related rarely- or newly parasitized species. We constructed a mathematical model to calculate the fitness payoffs of egg ejector vs. nest abandoner hosts to determine if various aspects of host life history traits and brood parasites' virulence on adult and young host fitness differentially influence the payoffs of alternative host defences. These calculations showed that in general egg ejection was a superior anti-parasite strategy to nest abandonment. Yet, increasing parasitism rates and increasing fitness values of hosts' eggs in both currently parasitized and future replacement nests led to switch points in fitness payoffs in favour of nest abandonment. Nonetheless, nest abandonment became selectively more favourable only at lower clutch sizes and only when hosts faced parasitism by a cowbird- rather than a cuckoo-type brood parasite. We suggest that, in addition to evolutionary lag and gape-size limitation, our estimated fitness differences based on life history trait variation provide new insights for the consistent differences observed in the anti-parasite rejection strategies between many cuckoo- and cowbird-hosts.

Song learning accelerates allopatric speciation.

The songs of many birds are unusual in that they serve a role in identifying conspecific mates, yet they are also culturally transmitted. Noting the apparently high rate of diversity in one avian taxon, the songbirds, in which song learning appears ubiquitous, it has often been speculated that cultural transmission may increase the rate of speciation. Here we examine the possibility that song learning affects the rate of allopatric speciation. We construct a population-genetic model of allopatric divergence that explores the evolution of genes that underlie learning preferences (predispositions to learn some songs over others). We compare this with a model in which mating signals are inherited only genetically. Models are constructed for the cases where songs and preferences are affected by the same or different loci, and we analyze them using analytical local stability analysis combined with simulations of drift and directional sexual selection. Under nearly all conditions examined, song divergence occurs more readily in the learning model than in the nonlearning model. This is a result of reduced frequency-dependent selection in the learning models. Cultural evolution causes males with unusual genotypes to tend to learn from the majority of males around them, and thus develop songs compatible with the majority of the females in the population. Unusual genotypes can therefore be masked by learning. Over a wide range of conditions, learning therefore reduces the waiting time for speciation to occur and can be predicted to accelerate the rate of speciation.

Beyond reinforcement: the evolution of premating isolation by direct selection on preferences and postmating, prezygotic incompatibilities.

The evolution of premating isolation after secondary contact is primarily considered in the guise of reinforcement, which relies on low hybrid fitness as the driving force for mating preference divergence. Here I consider two additional forces that may play a substantial role in the adaptive evolution of premating isolation, direct selection on preferences and indirect selection against postmating, prezygotic incompatibilities. First, I argue that a combination of ecological character displacement and sensory bias can cause direct selection on preferences that results in the pattern of reproductive character displacement. Both analytical and numerical methods are then used to demonstrate that, as expected from work in single populations, such direct selection will easily overwhelm indirect selection due to low hybrid fitness as the primary determinant of preference evolution. Second, postmating, prezygotic incompatibilities are presented as a driving force in the evolution of premating isolation. Two classes of these mechanisms, those increasing female mortality after mating but before producing offspring and those reducing female fertility, are shown to be identical in their effects on preference divergence. Analytical and numerical techniques are then used to demonstrate that postmating, prezygotic factors may place strong selection on preference divergence. These selective forces are shown to be comparable if not greater than those produced by the low fitness of hybrids.

Reinforcement and the genetics of nonrandom mating.

The occurrence of reinforcement is compared when premating isolation is caused by the spread of a gene causing females to prefer to mate with males carrying a population-specific trait (a "preference" model) and by a gene that causes females to prefer to mate with males that share their own trait phenotype (an "assortative mating" model). Both two-island models, which have symmetric gene flow, and continent-island models, which have one-way gene flow, are explored. Reinforcement is found to occur much more easily in a two-island assortative mating model than in any of the other three models. This is due primarily to the fact that in this model the assortative mating allele will automatically become genetically associated in each population with the trait allele that is favored by natural selection on that island. In contrast, natural selection on the trait both favors and opposes the evolution of premating isolation in the two-island preference model, depending on the particular population. These results imply that species recognition in the context of mating may evolve particularly easily when it targets cues that are favored by natural selection in each population. In the continent-island models, reinforcement is found to occur more often under the preference model than the assortative mating model, thus reversing the trend from the two-island models. Patterns of population subdivision may therefore play a role in determining what types of premating isolation may evolve.

The effects of predator learning, forgetting, and recognition errors on the evolution of warning coloration.

This paper demonstrates that the specifics of predator avoidance learning, information loss, and recognition errors may heavily influence the evolution of aposematism. I establish a mathematical model of the change in frequency over time of bright individuals of a distasteful prey species. Warning color spreads through green beard selection as reformulated by Guilford (1990); bright colored forms gain an advantage due to their phenotypic resemblance to other bright forms, which have been sampled by the predator. I use a general classical conditioning model to examine gradual predator learning and forgetting, and then consider the extreme of one-trial learning and no forgetting over time that may occur with very toxic prey. The advantage of conspicuous coloration under these latter conditions depends upon its role in lowering a constant probability of the prey being misidentified and thus mistakenly attacked by a predator, a rarely emphasized factor in the evolution of warning coloration. This constant probability of mistaken attacks can also be interpreted as a constant probability that forgetting has occurred (forgetting does not increase with time) or a periodic decision by the predator to resample avoided prey. I show that when predators learn and forget gradually, as under the general classical conditioning model, it is very difficult for aposematic coloration to become established unless bright individuals cross an often high threshold frequency through chance factors. In contrast, the conditions expected with highly toxic prey promote the evolution of warning coloration more easily, by means from the fixation of very bright mutations to the fixation of successive mutations each of which causes a small increase in a prey's conspicuousness. The results therefore predict that aposematic coloration may have evolved in a different manner in different predator and prey systems. They also suggest that it may be extremely difficult for warning coloration to evolve in more mildly toxic or distasteful prey outside of a mimicry system.

Species delimitation in systematics: inferring diagnostic differences between species.

Species are fundamental units in studies of systematics, biodiversity and ecology, but their delimitation has been relatively neglected methodologically. Species are typically circumscribed based on the presence of fixed (intraspecifically invariant or non-overlapping) diagnostic morphological characters which distinguish them from other species. In this paper, we argue that determining whether diagnostic characters are truly fixed with certainty is generally impossible with finite sample sizes and we show that sample sizes of hundreds or thousands of individuals may be necessary to have a reasonable probability of detecting polymorphisms in diagnostic characters at frequencies approaching zero. Instead, we suggest that using a non-zero frequency cut-off may be a more realistic and practical criterion for character-based species delimitation (for example, allowing polymorphisms in the diagnostic characters at frequencies of 5% or less). Given this argument, we then present a simple statistical method to evaluate whether at least one of a set of apparently diagnostic characters is below the frequency cut-off. This method allows testing of the strength of the evidence for species distinctness and is readily applicable to empirical studies.

The reinforcement of mating preferences on an island.

We develop a haploid model for the reinforcement of female mating preferences on an island that receives migrants from a continent. We find that preferences will evolve to favor island males under a broad range of conditions: when the average male display trait on the island and continent differ, when the preference acts on that difference, and when there is standing genetic variance for the preference. A difference between the mean display trait on the continent and on the island is sufficient to drive reinforcement of preferences. Additional postzygotic isolation, caused, for example, by either epistatic incompatibility or ecological selection against hybrids, will amplify reinforcement but is not necessary. Under some conditions, the degree of preference reinforcement is a simple function of quantities that can be estimated entirely from phenotypic data. We go on to study how postzygotic isolation caused by epistatic incompatibilities affects reinforcement of the preference. With only one pair of epistatic loci, reinforcement is enhanced by tighter linkage between the preference genes and the genes causing hybrid incompatibility. Reinforcement of the preference is also affected by the number of epistatically interacting genes involved in incompatibility, independent of the overall intensity of selection against hybrids.

Phylogenetic analysis and intraspecific variation: performance of parsimony, likelihood, and distance methods.

Intraspecific variation is abundant in all types of systematic characters but is rarely addressed in simulation studies of phylogenetic method performance. We compared the accuracy of 15 phylogenetic methods using simulations to (1) determine the most accurate method(s) for analyzing polymorphic data (under simplified conditions) and (2) test if generalizations about the performance of phylogenetic methods based on previous simulations of fixed (nonpolymorphic) characters are robust to a very different evolutionary model that explicitly includes intraspecific variation. Simulated data sets consisted of allele frequencies that evolved by genetic drift. The phylogenetic methods included eight parsimony coding methods, continuous maximum likelihood, and three distance methods (UPGMA, neighbor joining, and Fitch-Margoliash) applied to two genetic distance measures (Nei's and the modified Cavalli-Sforza and Edwards chord distance). Two sets of simulations were performed. The first examined the effects of different branch lengths, sample sizes (individuals sampled per species), numbers of characters, and numbers of alleles per locus in the eight-taxon case. The second examined more extensively the effects of branch length in the four-taxon, two-allele case. Overall, the most accurate methods were likelihood, the additive distance methods (neighbor joining and Fitch-Margoliash), and the frequency parsimony method. Despite the use of a very different evolutionary model in the present article, many of the results are similar to those from simulations of fixed characters. Similarities include the presence of the "Felsenstein zone," where methods often fail, which suggests that long-branch attraction may occur among closely related species through genetic drift. Differences between the results of fixed and polymorphic data simulations include the following: (1) UPGMA is as accurate or more accurate than nonfrequency parsimony methods across nearly all combinations of branch lengths, and (2) likelihood and the additive distance methods are not positively misled under any combination of branch lengths tested (even when the assumptions of the methods are violated and few characters are sampled). We found that sample size is an important determinant of accuracy and affects the relative success of methods (i.e., distance and likelihood methods outperform parsimony at small sample sizes). Attempts to generalize about the behavior of phylogenetic methods should consider the extreme examples offered by fixed-mutation models of DNA sequence data and genetic-drift models of allele frequencies.