Patch biogeography under intermittent barriers: macroevolutionary consequences of microevolutionary processes.

The processes that generate biodiversity start on a microevolutionary scale, where each individual's history can impact the species' history. This manuscript presents a theoretical study that examines the macroevolutionary patterns that emerge from the microevolutionary dynamics of populations inhabiting two patches. The model is neutral, meaning that neither survival nor reproduction depends on a fixed genotype, yet individuals must have minimal genetic similarity to reproduce. We used historical sea level oscillation over the past 800 thousand years to hypothesize periods when individuals could migrate from one patch to another. In our study, we keep track of each speciation and extinction event, build the complete and extant phylogenies, and characterize the macroevolutionary patterns regarding phylogeny balance, acceleration of speciation, and crown age. We also evaluate ecological patterns: richness, beta diversity, and species distribution symmetry. The balance of the complete phylogeny can be a sign of the speciation mode, contrasting speciation induced by migration and isolation (vicariance). The acceleration of the speciation process is also affected by the geographical barriers and the duration of the isolation period, with high isolation times leading to accelerated speciation. We report the correlation between ecological and macroevolutionary patterns and show it decreases with the time spent in isolation. We discuss, in light of our results, the challenge of integrating present-time community ecology with macroevolutionary patterns.

Intermittent migration can induce pulses of speciation in a two-island system.

Geographic barriers can come and go depending on natural conditions. These fluctuations cause population cycles of expansion and contraction, introducing intermittent migrations that may not hinder speciation but rather promote diversification. Here, we study a neutral 2-island speciation model with intermittent migration driven by sea-level fluctuations. Seabed depth modulates isolation and connection periods between the islands, with migration occurring during connection periods with a certain probability. Mating is restricted to genetically compatible individuals on the same island and offspring inherit genomes from both parents through recombination. We observe speciation pulses that would not occur under strict isolation or continuous migration, with infrequent, temporary increases in species richness happening at different times depending on the combination of geographic settings and migration probability. The resulting dynamic patterns of richness exhibit contrasting behavior between connected and isolated scenarios, often including species that do not persist. Prolonged isolation can reduce richness to 1 species per island, resembling patterns commonly associated with archipelagos under sea-level fluctuations. Together with other studies, our results in out-of-equilibrium populations support the relevance of investigating the impact of variable migration on diversification, particularly in regions of high diversity.

Effect of Host-Switching on the Ecological and Evolutionary Patterns of Parasites.

Speciation via host-switching is a macroevolutionary process that emerges from a microevolutionary dynamic where individual parasites switch hosts, establish a new association, and reduce reproductive contact with the original parasite lineage. Phylogenetic distance and geographic distribution of the hosts have been shown to be determinants of the capacity and opportunity of the parasite to change hosts. Although speciation via host-switching has been reported in many host-parasite systems, its dynamic on the individual, population and community levels is poorly understood. Here we propose a theoretical model to simulate parasite evolution considering host-switching events on the microevolutionary scale, taking into account the macroevolutionary history of the hosts, to evaluate how host-switching can affect ecological and evolutionary patterns of parasites in empirical communities at regional and local scales. In the model, parasite individuals can switch hosts under variable intensity and have their evolution driven by mutation and genetic drift. Mating is sexual and only individuals that are sufficiently similar can produce offspring. We assumed that parasite evolution occurs at the same evolutionary time scale as their hosts, and that the intensity of host-switching decreases as the host species differentiate. Ecological and evolutionary patterns were characterized by the turnover of parasite species among host species, and parasite evolutionary tree imbalance respectively. We found a range of host-switching intensity that reproduces ecological and evolutionary patterns observed in empirical communities. Our results showed that turnover decreased as host-switching intensity increased, with low variation among the model replications. On the other hand, tree imbalance showed wide variation and non-monotonic tendency. We concluded that tree imbalance was sensitive to stochastic events, whereas turnover may be a good indicator of host-switching. We found that local communities corresponded to higher host-switching intensity when compared to regional communities, highlighting that spatial scale is a limitation for host-switching. [Dispersal of parasites, opportunity and capacity of interaction, phylogenetic conservatism, and community structure.].

Diversity patterns and speciation processes in a two-island system with continuous migration.

Geographic isolation is a central mechanism of speciation, but perfect isolation of populations is rare. Although speciation can be hindered if gene flow is large, intermediate levels of migration can enhance speciation by introducing genetic novelty in the semi-isolated populations or founding small communities of migrants. Here, we consider a two-island neutral model of speciation with continuous migration and study diversity patterns as a function of the migration probability, population size, and number of genes involved in reproductive isolation (dubbed as genome size). For small genomes, low levels of migration induce speciation on the islands that otherwise would not occur. Diversity, however, drops sharply to a single species inhabiting both islands as the migration probability increases. For large genomes, sympatric speciation occurs even when the islands are strictly isolated. Then species richness per island increases with the probability of migration, but the total number of species decreases as they become cosmopolitan. For each genome size, there is an optimal migration intensity for each population size that maximizes the number of species. We discuss the observed modes of speciation induced by migration and how they increase species richness in the insular system while promoting asymmetry between the islands and hindering endemism.

Imperfect synchrony in animal displays: why does it occur and what is the true role of leadership?

Synchrony can be defined as the precise coordination between independent individuals, and this behaviour is more enigmatic when it is imperfect. The traditional theoretical explanation for imperfect synchronous courtship is that it arises as a by-product of the competition between males to broadcast leading signals to attract female attention. This competition is considered an evolutionary stable strategy maintained through sexual selection. However, previous studies have revealed that leading signals are not honest indicators of male quality. We studied imperfect courtship synchrony in fiddler crabs to mainly test whether (i) signal leadership and rate are defined by male quality and (ii) signal leadership generates synchrony. Fiddler crab males wave their enlarged claws during courtship, and females prefer leading males-displaying ahead of their neighbour(s). We filmed groups of waving males in the field to detect how often individuals were leaders and if they engaged in synchrony. Overall, we found that courtship effort is not directly related to male size, a general proxy for quality. Contrary to the long-standing assumption, we also revealed that leadership is not directly related to group synchrony, but faster wave rate correlates with both leadership and synchrony. This article is part of the theme issue 'Synchrony and rhythm interaction: from the brain to behavioural ecology'.

The role of ecological opportunity in shaping host-parasite networks.

Despite the great interest to quantify the structure of host-parasite interaction networks, the real influence of some factors such as taxonomy, host body size and ecological opportunity remains poorly understood. In this paper, we investigate the general patterns of organization and structure of interactions in two anuran-parasite networks in the Brazilian Pantanal (seasonally flooded environment) and Atlantic Forest (non-flooded forest). We present theoretical models to test whether the structures of these host-parasite interaction networks are influenced by neutrality, host taxonomy and host body size. Subsequently, we calculated metrics of connectance, nestedness and modularity to characterize the network structure. We demonstrated the structure networks were influenced mainly by body size and taxonomy of the host. Moreover, our results showed that the seasonally flooded environment present networks with higher connectance/nestedness and lower modularity compared to the other environment. The results also suggest that seasonal floods may promote ecological opportunities for new species associations.

Ecology and signal structure drive the evolution of synchronous displays.

Animal synchrony is found in phylogenetically distant animal groups, indicating behavioral adaptations to different selective pressures and in different signaling modalities. A notable example of synchronous display is found in fiddler crabs in that males wave their single enlarged claw during courtship. They present species-specific signals, which are composed of distinctive movement signatures. Given that synchronous waving has been reported for several fiddler crab species, the display pattern could influence the ability of a given species to sufficiently adjust wave timing to allow for synchrony. In this study, we quantified the wave displays of fiddler crabs to predict their synchronous behavior. We combined this information with the group's phylogenetic relationships to trace the evolution of display synchrony in an animal taxon. We found no phylogenetic signal in interspecific variation in predicted wave synchrony, which mirrors the general nonphylogenetic pattern of synchrony across animal taxa. Interestingly, our analyses show that the phenomenon of synchronization stems from the peculiarities of display pattern, mating systems, and the complexity of microhabitats. This is the first study to combine mathematical simulations and phylogenetic comparative methods to reveal how ecological factors and the mechanics of animal signals affect the evolution of the synchronous phenomena.

Host use dynamics in a heterogeneous fitness landscape generates oscillations in host range and diversification.

Colonization of novel hosts is thought to play an important role in parasite diversification, yet little consensus has been achieved about the macroevolutionary consequences of changes in host use. Here, we offer a mechanistic basis for the origins of parasite diversity by simulating lineages evolved in silico. We describe an individual-based model in which (i) parasites undergo sexual reproduction limited by genetic proximity, (ii) hosts are uniformly distributed along a one-dimensional resource gradient, and (iii) host use is determined by the interaction between the phenotype of the parasite and a heterogeneous fitness landscape. We found two main effects of host use on the evolution of a parasite lineage. First, the colonization of a novel host allowed parasites to explore new areas of the resource space, increasing phenotypic and genotypic variation. Second, hosts produced heterogeneity in the parasite fitness landscape, which led to reproductive isolation and therefore, speciation. As a validation of the model, we analyzed empirical data from Nymphalidae butterflies and their host plants. We then assessed the number of hosts used by parasite lineages and the diversity of resources they encompass. In both simulated and empirical systems, host diversity emerged as the main predictor of parasite species richness.

Understanding Host-Switching by Ecological Fitting.

Despite the fact that parasites are highly specialized with respect to their hosts, empirical evidence demonstrates that host switching rather than co-speciation is the dominant factor influencing the diversification of host-parasite associations. Ecological fitting in sloppy fitness space has been proposed as a mechanism allowing ecological specialists to host-switch readily. That proposal is tested herein using an individual-based model of host switching. The model considers a parasite species exposed to multiple host resources. Through time host range expansion can occur readily without the prior evolution of novel genetic capacities. It also produces non-linear variation in the size of the fitness space. The capacity for host colonization is strongly influenced by propagule pressure early in the process and by the size of the fitness space later. The simulations suggest that co-adaptation may be initiated by the temporary loss of less fit phenotypes. Further, parasites can persist for extended periods in sub-optimal hosts, and thus may colonize distantly related hosts by a "stepping-stone" process.

Patterns of interaction between Neotropical freshwater fishes and their gill Monogenoidea (Platyhelminthes).

Using network analysis, we looked for broad patterns of distribution of Monogenoidea gill parasites on Neotropical freshwater fishes within a host phylogenetic framework. We analyzed a database of Monogenoidea parasitizing fishes from Neotropical rivers, from 23 watersheds, based on species descriptions published until 2011. Host-parasite interactions were organized into five matrices grouping species at different taxonomic levels. The network of interactions between host families and parasite genera was significantly modular and revealed that each fish order has a unique composition of parasite genera. Hence, interactions between lower taxa were analyzed separately for the largest fish orders (Perciformes, Siluriformes, and Characiformes). Networks tended to be loosely connected and organized in modules. Despite the putative high host specificity of monogenoids, some have a wider host range that includes distantly related host species. Among the hosts, the clade composed by the piranhas (Serrasalmus spp. and related species, Serrasalmidae) stands out in terms of parasite richness per host species, resulting in a more connected network. The history of the lineages of each host order within Neotropical freshwaters seems to have a great influence on the extent of parasite sharing. The observed modularity was influenced by both spatial structure and phylogenetic relatedness of species. In average, 37 % of modules of networks between host species and parasite genera were associated with a particular river basin and 63 % of modules were associated with a host family. Hence, spatial structure determines the co-occurrence of host and parasite species, but their evolutionary history is the main factor defining which interactions are possible.

Synchronization and stability in noisy population dynamics.

We study the stability and synchronization of predator-prey populations subjected to noise. The system is described by patches of local populations coupled by migration and predation over a neighborhood. When a single patch is considered, random perturbations tend to destabilize the populations, leading to extinction. If the number of patches is small, stabilization in the presence of noise is maintained at the expense of synchronization. As the number of patches increases, both the stability and the synchrony among patches increase. However, a residual asynchrony, large compared with the noise amplitude, seems to persist even in the limit of an infinite number of patches. Therefore, the mechanism of stabilization by asynchrony recently proposed by Abta [Phys. Rev. Lett. 98, 098104 (2007)], combining noise, diffusion, and nonlinearities, seems to be more general than first proposed.

Pattern formation, outbreaks, and synchronization in food chains with two and three species.

We study the dynamics of populations of predators and preys using a mean field approach and a spatial model. The mean field description assumes that the individuals are homogeneously mixed and interact with one another with equal probability, so that space can be ignored. In the spatial model, on the other hand, predators can prey only in a certain neighborhood of their spatial location. We show that the size of these predation neighborhoods has dramatic effects on the dynamics and on the organization of the species in space. In the case of a three species food chain, in particular, the populations of predators display a sequence of apparently irregular outbreaks when the predation neighborhood has intermediate values, as compared to the size of the available space. Nonetheless, further increasing their size makes the outbreaks disappear and the dynamics approach that of the mean field model. Our study of synchronization also shows that the periodic behavior displayed by the average populations in a spatially extended system may hide the existence of patches that oscillate out of phase in a highly coordinated fashion.