Konrad Lohse

Revealing secret liaisons: DNA barcoding changes our understanding of food webs

1. How food webs are structured will affect how species dynamically interact. To date, the construction of quantitative food webs has largely been based on morphological species characters. Yet, recent work suggests that the use of molecular characters may change our perception of both species limits and species identity.

Reconstructing Community Assembly in Time and Space Reveals Enemy Escape in a Western Palearctic Insect Community

How geographically widespread biological communities assemble remains a major question in ecology. Do parallel population histories allow sustained interactions (such as host-parasite or plant-pollinator) among species, or do discordant histories necessarily interrupt them? Though few empirical data exist, these issues are central to our understanding of multispecies evolutionary dynamics. Here we use hierarchical approximate Bayesian analysis of DNA sequence data for 12 herbivores and 19 parasitoids to reconstruct the assembly of an insect community spanning the Western Palearctic and assess the support for alternative host tracking and ecological sorting hypotheses. We show that assembly occurred primarily by delayed host tracking from a shared eastern origin. Herbivores escaped their enemies for millennia before parasitoid pursuit restored initial associations, with generalist parasitoids no better able to track their hosts than specialists. In contrast, ecological sorting played only a minor role. Substantial turnover in host-parasitoid associations means that coevolution must have been diffuse, probably contributing to the parasitoid generalism seen in this and similar systems. Reintegration of parasitoids after host escape shows these communities to have been unsaturated throughout their history, arguing against major roles for parasitoid niche evolution or competition during community assembly.

A General Method for Calculating Likelihoods Under the Coalescent Process

Analysis of genomic data requires an efficient way to calculate likelihoods across very large numbers of loci. We describe a general method for finding the distribution of genealogies: we allow migration between demes, splitting of demes [as in the isolation-with-migration (IM) model], and recombination between linked loci. These processes are described by a set of linear recursions for the generating function of branch lengths. Under the infinite-sites model, the probability of any configuration of mutations can be found by differentiating this generating function. Such calculations are feasible for small numbers of sampled genomes: as an example, we show how the generating function can be derived explicitly for three genes under the two-deme IM model. This derivation is done automatically, using Mathematica. Given data from a large number of unlinked and nonrecombining blocks of sequence, these results can be used to find maximum-likelihood estimates of model parameters by tabulating the probabilities of all relevant mutational configurations and then multiplying across loci. The feasibility of the method is demonstrated by applying it to simulated data and to a data set previously analyzed by Wang and Hey (2010) consisting of 26,141 loci sampled from Drosophila simulans and D. melanogaster. Our results suggest that such likelihood calculations are scalable to genomic data as long as the numbers of sampled individuals and mutations per sequence block are small.

EXPERIMENTAL EVOLUTION OF RESISTANCE IN PARAMECIUM CAUDATUM AGAINST THE BACTERIAL PARASITE HOLOSPORA UNDULATA

Abstract —. Host‐parasite coevolution is often described as a process of reciprocal adaptation and counter adaptation, driven by frequency‐dependent selection. This requires that different parasite genotypes perform differently on different host genotypes. Such genotype‐by‐genotype interactions arise if adaptation to one host (or parasite) genotype reduces performance on others. These direct costs of adaptation can maintain genetic polymorphism and generate geographic patterns of local host or parasite adaptation. Fixation of all‐resistant (or all‐infective) genotypes is further prevented if adaptation trades off with other host (or parasite) life‐history traits. For the host, such indirect costs of resistance refer to reduced fitness of resistant genotypes in the absence of parasites. We studied (co)evolution in experimental microcosms of several clones of the freshwater protozoan Paramecium caudatum, infected with the bacterial parasite Holospora undulata. After two and a half years of culture, inoculation of evolved and naive (never exposed to the parasite) hosts with evolved and founder parasites revealed an increase in host resistance, but not in parasite infectivity. A cross‐infection experiment showed significant host clone‐by‐parasite isolate interactions, and evolved hosts tended to be more resistant to their own (local) parasites than to parasites from other hosts. Compared to naive clones, evolved host clones had lower division rates in the absence of the parasite. Thus, our study indicates de novo evolution of host resistance, associated with both direct and indirect costs. This illustrates how interactions with parasites can lead to the genetic divergence of initially identical populations.

Neandertal Admixture in Eurasia Confirmed by Maximum Likelihood Analysis of Three Genomes

Although there has been much interest in estimating histories of divergence and admixture from genomic data, it has proved difficult to distinguish recent admixture from long-term structure in the ancestral population. Thus, recent genome-wide analyses based on summary statistics have sparked controversy about the possibility of interbreeding between Neandertals and modern humans in Eurasia. Here we derive the probability of full mutational configurations in nonrecombining sequence blocks under both admixture and ancestral structure scenarios. Dividing the genome into short blocks gives an efficient way to compute maximum-likelihood estimates of parameters. We apply this likelihood scheme to triplets of human and Neandertal genomes and compare the relative support for a model of admixture from Neandertals into Eurasian populations after their expansion out of Africa against a history of persistent structure in their common ancestral population in Africa. Our analysis allows us to conclusively reject a model of ancestral structure in Africa and instead reveals strong support for Neandertal admixture in Eurasia at a higher rate (3.4−7.3%) than suggested previously. Using analysis and simulations we show that our inference is more powerful than previous summary statistics and robust to realistic levels of recombination.

Genome-wide tests for introgression between cactophilic Drosophila implicate a role of inversions during speciation

Models of speciation‐with‐gene‐flow have shown that the reduction in recombination between alternative chromosome arrangements can facilitate the fixation of locally adaptive genes in the face of gene flow and contribute to speciation. However, it has proven frustratingly difficult to show empirically that inversions have reduced gene flow and arose during or shortly after the onset of species divergence rather than represent ancestral polymorphisms. Here, we present an analysis of whole genome data from a pair of cactophilic fruit flies, Drosophila mojavensis and D. arizonae, which are reproductively isolated in the wild and differ by several large inversions on three chromosomes. We found an increase in divergence at rearranged compared to colinear chromosomes. Using the density of divergent sites in short sequence blocks we fit a series of explicit models of species divergence in which gene flow is restricted to an initial period after divergence and may differ between colinear and rearranged parts of the genome. These analyses show that D. mojavensis and D. arizonae have experienced postdivergence gene flow that ceased around 270 KY ago and was significantly reduced in chromosomes with fixed inversions. Moreover, we show that these inversions most likely originated around the time of species divergence which is compatible with theoretical models that posit a role of inversions in speciation with gene flow.

Inferring the colonization of a mountain range—refugia vs. nunatak survival in high alpine ground beetles

It has long been debated whether high alpine specialists survived ice ages in situ on small ice‐free islands of habitat, so‐called nunataks, or whether glacial survival was restricted to larger massifs de refuge at the periphery. We evaluate these alternative hypotheses in a local radiation of high alpine carabid beetles (genus Trechus) in the Orobian Alps, Northern Italy. While summits along the northern ridge of this mountain range were surrounded by the icesheet as nunataks during the last glacial maximum, southern areas remained unglaciated. We analyse a total of 1366 bp of mitochondrial (Cox1 and Cox2) data sampled from 150 individuals from twelve populations and 530 bp of nuclear (PEPCK) sequence sampled for a subset of 30 individuals. Using Bayesian inference, we estimate ancestral location states in the gene trees, which in turn are used to infer the most likely order of recolonization under a model of sequential founder events from a massif de refuge from the mitochondrial data. We test for the paraphyly expected under this model and for reciprocal monophyly predicted by a contrasting model of prolonged persistence of nunatak populations. We find that (i) only three populations are incompatible with the paraphyly of the massif de refuge model, (ii) both mitochondrial and nuclear data support separate refugial origins for populations on the western and eastern ends of the northern ridge, and (iii) mitochondrial node ages suggest persistence on the northern ridge for part of the last ice age.

Model-based comparisons of phylogeographic scenarios resolve the intraspecific divergence of cactophilic Drosophila mojavensis.

The cactophilic fly Drosophila mojavensis exhibits considerable intraspecific genetic structure across allopatric geographic regions and shows associations with different host cactus species across its range. The divergence between these populations has been studied for more than 60 years, yet their exact historical relationships have not been resolved. We analysed sequence data from 15 intronic X‐linked loci across populations from Baja California, mainland Sonora‐Arizona and Mojave Desert regions under an isolation‐with‐migration model to assess multiple scenarios of divergence. We also compared the results with a pre‐existing sequence data set of eight autosomal loci. We derived a population tree with Baja California placed at its base and link their isolation to Pleistocene climatic oscillations. Our estimates suggest the Baja California population diverged from an ancestral Mojave Desert/mainland Sonora‐Arizona group around 230 000–270 000 years ago, while the split between the Mojave Desert and mainland Sonora‐Arizona populations occurred one glacial cycle later, 117 000–135 000 years ago. Although we found these three populations to be effectively allopatric, model ranking could not rule out the possibility of a low level of gene flow between two of them. Finally, the Mojave Desert population showed a small effective population size, consistent with a historical population bottleneck. We show that model‐based inference from multiple loci can provide accurate information on the historical relationships of closely related groups allowing us to set into historical context a classic system of incipient ecological speciation.

Testing models of speciation from genome sequences: divergence and asymmetric admixture in Island South-East Asian Sus species during the Plio-Pleistocene climatic fluctuations

In many temperate regions, ice ages promoted range contractions into refugia resulting in divergence (and potentially speciation), while warmer periods led to range expansions and hybridization. However, the impact these climatic oscillations had in many parts of the tropics remains elusive. Here, we investigate this issue using genome sequences of three pig (Sus) species, two of which are found on islands of the Sunda‐shelf shallow seas in Island South‐East Asia (ISEA). A previous study revealed signatures of interspecific admixture between these Sus species (Genome biology, 14, 2013, R107). However, the timing, directionality and extent of this admixture remain unknown. Here, we use a likelihood‐based model comparison to more finely resolve this admixture history and test whether it was mediated by humans or occurred naturally. Our analyses suggest that interspecific admixture between Sunda‐shelf species was most likely asymmetric and occurred long before the arrival of humans in the region. More precisely, we show that these species diverged during the late Pliocene but around 23% of their genomes have been affected by admixture during the later Pleistocene climatic transition. In addition, we show that our method provides a significant improvement over D‐statistics which are uninformative about the direction of admixture.

Quantifying the pleistocene history of the oak gall parasitoid Cecidostiba fungosa using twenty intron loci.

The longitudinal spread of temperate organisms into refugial populations in Southern Europe is generally assumed to predate the last interglacial. However, few studies have attempted to quantify this process in nonmodel organisms using explicit models and multilocus data. We used sequence data for 20 intron‐spanning loci (12 kb per individual) to resolve the history of refugial populations of a widespread western Palaearctic oak gall parasitoid Cecidostiba fungosa (Pteromalidae). Using maximum likelihood and Bayesian methods we assess alternative population tree topologies and estimate divergence times and ancestral population sizes under a model of divergence between three refugia (Middle East, Balkans and Iberia). Both methods support an “Out of the East” history for C. fungosa, matching the pattern previously inferred for their gallwasp hosts. However, coalescent‐based estimates of the ages of population divides are much more recent (coinciding with the Eemian interglacial) than nodal ages of single gene trees for C. fungosa and other species. We also find that increasing the sample size from one haploid sequence per refugial population to three only marginally improves parameter estimates. Our results suggest that there is significant information in the minimal samples currently analyzable with maximum likelihood methods, and that similar methods could be applied to multiple species to test alternative models of assemblage evolution.