Detecting the macroevolutionary signal of species interactions.

Species interactions lie at the heart of many theories of macroevolution, from adaptive radiation to the Red Queen. Although some theories describe the imprint that interactions will have over long timescales, we are still missing a comprehensive understanding of the effects of interactions on macroevolution. Current research shows strong evidence for the impact of interactions on macroevolutionary patterns of trait evolution and diversification, yet many macroevolutionary studies have only a tenuous relationship to ecological studies of interactions over shorter timescales. We review current research in this area, highlighting approaches that explicitly model species interactions and connect them to broad-scale macroevolutionary patterns. We also suggest that progress has been made by taking an integrative interdisciplinary look at individual clades. We focus on African cichlids as a case study of how this approach can be fruitful. Overall, although the evidence for species interactions shaping macroevolution is strong, further work using integrative and model-based approaches is needed to spur progress towards understanding the complex dynamics that structure communities over time and space.

Signatures of Microevolutionary Processes in Phylogenetic Patterns.

Phylogenetic trees are representations of evolutionary relationships among species and contain signatures of the processes responsible for the speciation events they display. Inferring processes from tree properties, however, is challenging. To address this problem, we analyzed a spatially-explicit model of speciation where genome size and mating range can be controlled. We simulated parapatric and sympatric (narrow and wide mating range, respectively) radiations and constructed their phylogenetic trees, computing structural properties such as tree balance and speed of diversification. We showed that parapatric and sympatric speciation are well separated by these structural tree properties. Balanced trees with constant rates of diversification only originate in sympatry and genome size affected both the balance and the speed of diversification of the simulated trees. Comparison with empirical data showed that most of the evolutionary radiations considered to have developed in parapatry or sympatry are in good agreement with model predictions. Even though additional forces other than spatial restriction of gene flow, genome size, and genetic incompatibilities, do play a role in the evolution of species formation, the microevolutionary processes modeled here capture signatures of the diversification pattern of evolutionary radiations, regarding the symmetry and speed of diversification of lineages.

Gene flow and metacommunity arrangement affects coevolutionary dynamics at the mutualism-antagonism interface.

Interspecific interactions are affected by community context and, as a consequence, show spatial variation in magnitude and sign. The selective forces imposed by interactions at the mutualism-antagonism interface are a consequence of the traits involved and their matching between species. If mutualistic and antagonistic communities are linked by gene flow, coevolution between a pair of interacting species is influenced by how selection varies in space. Here we investigate the effects of metacommunity arrangement, i.e. patterns of connection between communities and the number of communities, on the coevolutionary dynamics between two species for which the sign and magnitude of the interaction varies across the landscape. We quantify coevolutionary outcome as an index that can be decomposed into the contribution of intraspecific genetic diversity and interspecific interaction. We show that polymorphisms and mismatches are an expected outcome, which is influenced by spatial structure, interaction strength and the degree of gene flow. The index describes how variation is distributed within and between species, and provides information on the directionality of the mismatches and polymorphisms. Finally, we argue that depending on metacommunity arrangement, some communities have disproportionate roles in maintaining genetic diversity, with implications for the coevolution of interacting species in a fragmented landscape.

The mutation-drift balance in spatially structured populations.

In finite populations the action of neutral mutations is balanced by genetic drift, leading to a stationary distribution of alleles that displays a transition between two different behaviors. For small mutation rates most individuals will carry the same allele at equilibrium, whereas for high mutation rates of the alleles will be randomly distributed with frequencies close to one half for a biallelic gene. For well-mixed haploid populations the mutation threshold is µc=1/2N, where N is the population size. In this paper we study how spatial structure affects this mutation threshold. Specifically, we study the stationary allele distribution for populations placed on regular networks where connected nodes represent potential mating partners. We show that the mutation threshold is sensitive to spatial structure only if the number of potential mates is very small. In this limit, the mutation threshold decreases substantially, increasing the diversity of the population at considerably low mutation rates. Defining kc as the degree of the network for which the mutation threshold drops to half of its value in well-mixed populations we show that kc grows slowly as a function of the population size, following a power law. Our calculations and simulations are based on the Moran model and on a mapping between the Moran model with mutations and the voter model with opinion makers.

Error catastrophe in populations under similarity-essential recombination.

Organisms are often more likely to exchange genetic information with others that are similar to themselves. One of the most widely accepted mechanisms of RNA virus recombination requires substantial sequence similarity between the parental RNAs and is termed similarity-essential recombination. This mechanism may be considered analogous to assortative mating, an important form of non-random mating that can be found in animals and plants. Here we study the dynamics of haplotype frequencies in populations evolving under similarity-essential recombination. Haplotypes are represented by a genome of B biallelic loci and the Hamming distance between individuals is used as a criterion for recombination. We derive the evolution equations for the haplotype frequencies assuming that recombination does not occur if the genetic distance is larger than a critical value G and that mutation occurs at a rate µ per locus. Additionally, uniform crossover is considered. Although no fitness is directly associated to the haplotypes, we show that frequency-dependent selection emerges dynamically and governs the haplotype distribution. A critical mutation rate µc can be identified as the error threshold transition, beyond which this selective information cannot be stored. For µ<µc the distribution consists of a dominant sequence surrounded by a cloud of closely related sequences, characterizing a quasispecies. For µ>µc the distribution becomes uniform, with all haplotypes having the same frequency. In the case of extreme assortativeness, where individuals only recombine with others identical to themselves (G=0), the error threshold results µc=1/4, independently of the genome size. For weak assortativity (G=B-1)µc=2(-(B+1)) and for the case of no assortativity (G=B) µc=0. We compute the mutation threshold for 0

Evolution and stability of ring species.

Neutral models, in which genetic change arises through random variation without fitness differences, have proven remarkably successful in describing observed patterns of biodiversity, despite the manifest role of selection in evolution. Here we investigate the effect of barriers on biodiversity by simulating the expansion of a population around a barrier to form a ring species, in which the two ends of the population are reproductively isolated despite ongoing gene flow around the ring. We compare the spatial and genetic properties of a neutral agent-based population model to the greenish warblers' complex, a well-documented example of an actual ring species in nature. Our results match the distribution of subspecies, the principal components of genetic diversity, and the linear spatial-genetic correlation of the observed data, even though selection is expected to be important for traits of this species. We find that ring species are often unstable to speciation or mixing but can persist for extended times depending on species and landscape features. For the greenish warblers, our analysis implies that the expanded area near the point of secondary contact is important for extending the duration of the ring, and thus, for the opportunity to observe this ring species. Nevertheless it also suggests the ring will break up into multiple species in 10,000 to 50,000 y. These results imply that simulations can be used to accurately describe empirical data for complex spatial-genetic traits of an individual species.

Spiroplasma in Drosophila melanogaster populations: prevalence, male-killing, molecular identification, and no association with Wolbachia.

Spiroplasma endosymbionts are maternally transmitted bacteria that may kill infected sons resulting in the production of female-biased broods. The prevalence of male killers varies considerably both between and within species. Here, we evaluate the spatial and temporal status of male-killing and non-male-killing Spiroplasma infection in three Brazilian populations of Drosophila melanogaster, nearly a decade after the first occurrence report for this species. The incidence of the male-killing Spiroplasma ranged from close to 0 to 17.7 % (so far the highest estimate for a Drosophila species) with a suggestion of temporal decline in a population. We also found non-male-killing Spiroplasma coexisting in one population at lower prevalence (3-5 %), and we did not detect it in the other two. This may be taken as a suggestion of a spreading advantage conferred by the male-killing strategy. Sequencing two loci, we identified the phylogenetic position of Spiroplasma strains from the three localities, showing that all strains group closely in the poulsonii clade. Due to intensive sampling effort, we were able to test the association between Spiroplasma infections and another widespread endosymbiont, Wolbachia, whose prevalence ranged from 81.8 to 100 %. The prevalence of Wolbachia did not differ between Spiroplasma-infected and uninfected strains in our largest sample nor were the prevalences of the two endosymbionts associated across localities.