James A. Nicholls

Extreme host plant conservatism during at least 20 million years of host plant pursuit by oak gallwasps.

Diversification of insect herbivores is often associated with coevolution between plant toxins and insect countermeasures, resulting in a specificity that restricts host plant shifts. Gall inducers, however, bypass plant toxins and the factors influencing host plant associations in these specialized herbivores remain unclear. We reconstructed the evolution of host plant associations in Western Palaearctic oak gallwasps (Cynipidae: Cynipini), a species-rich lineage of specialist herbivores on oak (Quercus). (1) Bayesian analyses of sequence data for three genes revealed extreme host plant conservatism, with inferred shifts between major oak lineages (sections Cerris and Quercus) closely matching the minimum required to explain observed diversity. It thus appears that the coevolutionary demands of gall induction constrain host plant shifts, both in cases of mutualism (e.g., fig wasps, yucca moths) and parasitism (oak gallwasps). (2) Shifts between oak sections occurred independently in sexual and asexual generations of the gallwasp lifecycle, implying that these can evolve independently. (3) Western Palaearctic gallwasps associated with sections Cerris and Quercus diverged at least 20 million years ago (mya), prior to the arrival of oaks in the Western Palaearctic from Asia 5–7 mya. This implies an Asian origin for Western Palaearctic gallwasps, with independent westwards range expansion by multiple lineages.

A landscape genetics approach for quantifying the relative influence of historic and contemporary habitat heterogeneity on the genetic connectivity of a rainforest bird.

Landscape genetics is an important framework for investigating the influence of spatial pattern on ecological process. Nevertheless, the standard analytic frameworks in landscape genetics have difficulty evaluating hypotheses about spatial processes in dynamic landscapes. We use a predictive hypothesis‐driven approach to quantify the relative contribution of historic and contemporary processes to genetic connectivity. By confronting genetic data with models of historic and contemporary landscapes, we identify dispersal processes operating in naturally heterogeneous and human‐altered systems. We demonstrate the approach using a case study of microsatellite polymorphism and indirect estimates of gene flow for a rainforest bird, the logrunner (Orthonyx temminckii). Of particular interest was how much information in the genetic data was attributable to processes occurring in the reconstructed historic landscape and contemporary human‐modified landscape. A linear mixed model was used to estimate appropriate sampling variance from nonindependent data and information‐theoretic model selection provided strength of evidence for alternative hypotheses. The contemporary landscape explained slightly more information in the genetic differentiation data than the historic landscape, and there was considerable evidence for a temporal shift in dispersal pattern. In contrast, migration rates estimated from genealogical information were primarily influenced by contemporary landscape change. We discovered that landscape heterogeneity facilitated gene flow before European settlement, but contemporary deforestation is rapidly becoming the most important barrier to logrunner dispersal.

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.

GENETIC POPULATION STRUCTURE AND CALL VARIATION IN A PASSERINE BIRD, THE SATIN BOWERBIRD, PTILONORHYNCHUS VIOLACEUS

Abstract Geographic variation in vocalizations is widespread in passerine birds, but its origins and maintenance remain unclear. One hypothesis to explain this variation is that it is associated with geographic isolation among populations and therefore should follow a vicariant pattern similar to that typically found in neutral genetic markers. Alternatively, if environmental selection strongly influences vocalizations, then genetic divergence and vocal divergence may be disassociated. This study compared genetic divergence derived from 11 microsatellite markers with a metric of phenotypic divergence derived from male bower advertisement calls. Data were obtained from 16 populations throughout the entire distribution of the satin bowerbird, an Australian wet‐forest‐restricted passerine. There was no relationship between call divergence and genetic divergence, similar to most other studies on birds with learned vocalizations. Genetic divergence followed a vicariant model of evolution, with the differentiation of isolated populations and isolation‐by‐distance among continuous populations. Previous work on Ptilonorhynchus violaceus has shown that advertisement call structure is strongly influenced by the acoustic environment of different habitats. Divergence in vocalizations among genetically related populations in different habitats indicates that satin bowerbirds match their vocalizations to the environment in which they live, despite the homogenizing influence of gene flow. In combination with convergence of vocalizations among genetically divergent populations occurring in the same habitat, this shows the overriding importance that habitat‐related selection can have on the establishment and maintenance of variation in vocalizations.

Perched at the mito-nuclear crossroads: divergent mitochondrial lineages correlate with environment in the face of ongoing nuclear gene flow in an Australian bird.

Relationships among multilocus genetic variation, geography, and environment can reveal how evolutionary processes affect genomes. We examined the evolution of an Australian bird, the eastern yellow robin Eopsaltria australis, using mitochondrial (mtDNA) and nuclear (nDNA) genetic markers, and bioclimatic variables. In southeastern Australia, two divergent mtDNA lineages occur east and west of the Great Dividing Range, perpendicular to latitudinal nDNA structure. We evaluated alternative scenarios to explain this striking discordance in landscape genetic patterning. Stochastic mtDNA lineage sorting can be rejected because the mtDNA lineages are essentially distinct geographically for > 1500 km. Vicariance is unlikely: the Great Dividing Range is neither a current barrier nor was it at the Last Glacial Maximum according to species distribution modeling; nuclear gene flow inferred from coalescent analysis affirms this. Female philopatry contradicts known female‐biased dispersal. Contrasting mtDNA and nDNA demographies indicate their evolutionary histories are decoupled. Distance‐based redundancy analysis, in which environmental temperatures explain mtDNA variance above that explained by geographic position and isolation‐by‐distance, favors a nonneutral explanation for mitochondrial phylogeographic patterning. Thus, observed mito‐nuclear discordance accords with environmental selection on a female‐linked trait, such as mtDNA, mtDNA–nDNA interactions or genes on W‐chromosome, driving mitochondrial divergence in the presence of nuclear gene flow.

Concordant phylogeography and cryptic speciation in two Western Palaearctic oak gall parasitoid species complexes

Little is known about the evolutionary history of most complex multi‐trophic insect communities. Widespread species from different trophic levels might evolve in parallel, showing similar spatial patterns and either congruent temporal patterns (Contemporary Host‐tracking) or later divergence in higher trophic levels (Delayed Host‐tracking). Alternatively, host shifts by natural enemies among communities centred on different host resources could disrupt any common community phylogeographic pattern. We examined these alternative models using two Megastigmus parasitoid morphospecies associated with oak cynipid galls sampled throughout their Western Palaearctic distributions. Based on existing host cynipid data, a parallel evolution model predicts that eastern regions of the Western Palaearctic should contain ancestral populations with range expansions across Europe about 1.6 million years ago and deeper species‐level divergence at both 8–9 and 4–5 million years ago. Sequence data from mitochondrial cytochrome b and multiple nuclear genes showed similar phylogenetic patterns and revealed cryptic genetic species within both morphospecies, indicating greater diversity in these communities than previously thought. Phylogeographic divergence was apparent in most cryptic species between relatively stable, diverse, putatively ancestral populations in Asia Minor and the Middle East, and genetically depauperate, rapidly expanding populations in Europe, paralleling patterns in host gallwasp species. Mitochondrial and nuclear data also suggested that Europe may have been colonized multiple times from eastern source populations since the late Miocene. Temporal patterns of lineage divergence were congruent within and across trophic levels, supporting the Contemporary Host‐tracking Hypothesis for community evolution.

Chalcid parasitoid community associated with the invading pest Dryocosmus kuriphilus in north-western Italy

Abstract.  1. Biological invasions of exotic species pose a major threat to native biodiversity. Invaders are known to have direct impacts on native species; however, less well studied are the indirect impacts mediated through the integration of invaders into trophically linked communities.

Phylogeography of an east Australian wet‐forest bird, the satin bowerbird (Ptilonorhynchus violaceus), derived from mtDNA, and its relationship to morphology

Australian wet forests have undergone a contraction in range since the mid‐Tertiary, resulting in a fragmented distribution along the east Australian coast incorporating several biogeographical barriers. Variation in mitochondrial DNA and morphology within the satin bowerbird was used to examine biogeographical structure throughout almost the entire geographical extent of these wet forest fragments. We used several genetic analysis techniques, nested clade and barrier analyses, that use patterns inherent in the data to describe the spatial structuring. We also examined the validity of the two previously described satin bowerbird subspecies that are separated by well‐defined biogeographical barriers and tested existing hypotheses that propose divergence occurs within each subspecies across two other barriers, the Black Mountain corridor and the Hunter Valley. Our data showed that the two subspecies were genetically and morphologically divergent. The northern subspecies, found in the Wet Tropics region of Queensland, showed little divergence across the Black Mountain corridor, a barrier found to be significant in other Wet Tropics species. Biogeographical structure was found through southeastern Australia; three geographically isolated populations showed genetic differentiation, although minimal divergence was found across the proposed Hunter Valley barrier. A novel barrier was found separating inland and coastal populations in southern New South Wales. Little morphological divergence was observed within subspecies, bar a trend for birds to be larger in the more southerly parts of the species’ range. The results from both novel and well‐established genetic analyses were similar, providing greater confidence in the conclusions about spatial divergence and supporting the validity of these new techniques.

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.

Using targeted enrichment of nuclear genes to increase phylogenetic resolution in the neotropical rain forest genus Inga (Leguminosae: Mimosoideae)

Evolutionary radiations are prominent and pervasive across many plant lineages in diverse geographical and ecological settings; in neotropical rainforests there is growing evidence suggesting that a significant fraction of species richness is the result of recent radiations. Understanding the evolutionary trajectories and mechanisms underlying these radiations demands much greater phylogenetic resolution than is currently available for these groups. The neotropical tree genus Inga (Leguminosae) is a good example, with ~300 extant species and a crown age of 2–10 MY, yet over 6 kb of plastid and nuclear DNA sequence data gives only poor phylogenetic resolution among species. Here we explore the use of larger-scale nuclear gene data obtained though targeted enrichment to increase phylogenetic resolution within Inga. Transcriptome data from three Inga species were used to select 264 nuclear loci for targeted enrichment and sequencing. Following quality control to remove probable paralogs from these sequence data, the final dataset comprised 259,313 bases from 194 loci for 24 accessions representing 22 Inga species and an outgroup (Zygia). Bayesian phylogenies reconstructed using either all loci concatenated or a gene-tree/species-tree approach yielded highly resolved phylogenies. We used coalescent approaches to show that the same targeted enrichment data also have significant power to discriminate among alternative within-species population histories within the widespread species I. umbellifera. In either application, targeted enrichment simplifies the informatics challenge of identifying orthologous loci associated with de novo genome sequencing. We conclude that targeted enrichment provides the large volumes of phylogenetically-informative sequence data required to resolve relationships within recent plant species radiations, both at the species level and for within-species phylogeographic studies.