Below, I give short summaries of the papers I have (co-)authored, along with a key graphic from each paper.
Multiple recombination events between two cytochrome P450 loci contribute to global pyrethroid resistance in Helicoverpa armigera
In this study, we examine a chimeric cytochrome P450 gene that has been identified as being involved in resistance of H. armigera to the insecticides, fenvalerate and cypermethrin. We show that resistance at this locus involves at least eight different alleles, which are likely to have arisen independently in multiple geographic locations around the world. Importantly, we find that the alleles present in Brazil are the same as those most commonly found in Asia, suggesting a potential origin for the incursion of H. armigera into the Americas.
Penguin ectoparasite panmixia suggests extensive host movement within a colony
In this study, we wanted to determine how much penguins move and interact within their colonies. However, high abundances, physical similarity, and nocturnal habits of penguins all hinder observation of fine-scale movements. Thus, we use ectoparasites to infer penguin movements by studying the fine-scale genetic structure of penguin ticks, which depend on host movements for their dispersal. We examine these ticks on little penguin colonies at Philip Island (Victoria, Australia) and find no evidence for barriers to gene flow in our genetic data. Thus, we infer that extensive penguin movement and socialisation occurs throughout the colony, despite strong nest-site philopatry.
genomic innovations, transcriptional plasticity and gene loss underlying the evolution and divergence of two highly polyphagous and invasive helicoverpa pest species
This work by the Helicoverpa Genome Consortium uses comparative genomics, transcriptomics, and genome re-sequencing to elucidate the genetic basis for pest properties in two Helicoverpa species. We find that polyphagy in H. armigera and H. zea is associated with extensive amplification and neofunctionalisation of genes involved in host finding and use, coupled with versatile transcriptional responses on different hosts. See this news feature for more info!
variation in rates of spontaneous male production within the nematode species Pristionchus pacificus supports an adaptive role for males and outcrossing
The nematode Pristionchus pacificus has an androdioecious mating system, where populations consist predominantly of self-fertilising hermaphrodites and relatively few males. We look at male production in P. pacificus in this study and find that sampling location on La Réunion Island and temperature treatment in the lab interact to significantly influence rates of spontaneous male production. In other words, when this nematode is exposed to a temperature that differs from its usual environment it responds with an increased rate of male production. This potentially results in higher out-crossing rates, hence driving increased effective recombination and the creation of potentially adaptive novel allelic combinations.
population structure and gene flow in the global pest, helicoverpa armigera
This study focuses on the major agricultural pest, Helicoverpa armigera. We use genomic data to assess gene flow in H. armigera with samples collected from six continents. We find that, despite the large geographic distances separating populations, there is little signal for genetic structure. However, we find support for a distinct subspecies, H. a. conferta, residing exclusively in Australasia. We also find several lines of evidence to support admixture of H. armigera with the closely-related species H. zea.
the importance of replicating genomic analyses to verify phylogenetic signal for recently evolved lineages
Genome-wide SNP data are increasingly being used in phylogenetic and phylogeographic analyses, often when little is known about the locations and evolution of the SNPs. In this study we test the robustness of phylogenetic inference based on SNP data for closely related lineages. We find that tree topologies change depending on the number of SNPs used in the analysis and that bootstrap values alone can give misleading impressions of the strength of phylogenetic inferences. These results highlight the importance of independently replicating SNP analyses to verify that phylogenetic inferences based on non-targeted SNP data are robust.
parallel adaptation to higher temperatures in divergent clades of the nematode pristionchus pacificus
In this study we want to find out if nematode strains collected from different locations on La Réunion Island differ in their ability to tolerate high temperatures due to the fact that they are adapted to their local habitat environments. We find that heat tolerance differs among strains depending on which ancestral clade they belong to and which local environment they are collected from. We reconstruct ancestral states to show that heat tolerance has evolved independently in parallel at least twice in the evolutionary history of Pristionchus pacificus.
GENOMIC PROFILES OF DIVERSIFICATION AND GENOTYPE-PHENOTYPE ASSOCIATION IN ISLAND NEMATODE LINEAGES
This is a massive project where we sequence the genomes of over 250 nematode strains. With four different genetic lineages present on La Réunion Island, we want to see if the different lineages are diversifying in the same ways in parallel. We also want to look at phenotypic evolution with this amazing study system. We show that shared divergent genomic regions occur at a higher frequency than expected by chance among nematode populations of the same evolutionary lineage. Phenotypically, we find that pH tolerance is diverging in a manner that corresponds to environmental differences among populations. We then look at pH tolerance further and are able to functionally validate a significant genotype-phenotype association for this trait. Our results are consistent with Pristionchus pacificus undergoing heterogeneous genotypic and phenotypic diversification related to both evolutionary and environmental processes.
oxygen-induced social behaviours in pristionchus pacificus have a distinct evolutionary history and genetic regulation from caenorhabditis elegans
Wild isolates of the nematode Caenorhabditis elegans perform clumping and bordering behaviours on an agar plate to avoid hyperoxia under laboratory conditions. Conversely, a laboratory reference strain ('N2') has acquired a solitary behaviour in the laboratory and no longer borders/clumps. In this study we examine the evolution and natural variation of clumping and bordering behaviours in Pristionchus pacificus nematodes using >100 strains collected from La Réunion Island. We find that the majority of strains display a solitary behaviour similar to C. elegans N2, but we see social behaviours in strains that inhabit high-altitude locations on La Réunion. We show experimentally that P. pacificus social strains perform clumping and bordering to avoid hyperoxic conditions in the laboratory, suggesting that social strains may have adapted to, or evolved a preference for, the lower relative oxygen levels available at high altitude in nature. Thus, clumping and bordering behaviours represent an example of phenotypic convergence in the two nematode species, underlain by different evolutionary histories and distinct genetic control.
integrating a population genomics focus into biogeographic and macroecological research
In this paper I argue that population genomics data can be used to better inform macro-evolutionary research. In order to truly understand the limits of species distributions we must understand the development of life history traits and evolutionary potential among taxa, as well as the interactions within and among species, as it is these that define which species live where, both now and in the future. Population genomic data can provide key insights into phenotypic trait variation and adaptive potential that may promote future species responses to environmental change, as well as tell us how groups of related taxa have responded across historical and contemporary scales to reach their current distribution extents.
Population genetics and the La Réunion case study
In this book chapter we provide a nice summary of everything we know about the population genetics of Pristionchus pacifiucs. We describe the patterns of genetic diversity and distribution that characterise P. pacificus populations globally. We evaluate the evolutionary history of this nematode on La Réunion Island, looking at colonisation mechanisms, divergence estimates and demography of populations. We also cover the role of the environment in local population dynamics of P. pacificus, finishing with a discussion of the scope for future work in this system.
transcriptomic characterisation and genomic glimps into the toxigenic dinoflagellate azadinium spinosum, with emphasis on polyketide synthase genes
Unicellular dinoflagellates are an important group of primary producers within the marine plankton community. Many of these species are capable of forming harmful algae blooms and of producing potent phycotoxins, thereby causing deleterious impacts on their environment and posing a threat to human health. The recently discovered toxigenic dinoflagellate Azadinium spinosum is known to produce azaspiracid toxins and, despite the global distribution of A. spinosum, little is known about its molecular features. In this study we investigate the genomic and transcriptomic features of A. spinosum with a focus on toxin synthesis and evolution.
natural variation in cold tolerance in the nematode pristionchus pacificus: the role of genotype and environment
Low temperature is a primary determinant of growth and survival among organisms and almost all animals need to withstand temperature fluctuations in their surroundings. In this study we examine variation in cold tolerance in Pristionchus pacificus collected from 18 widespread locations on La Réunion Island. We find that P. pacificus displays a high degree of natural variation in cold tolerance that may be partly driven by differential trait sensitivity in diverse environments.
environmental variables explain genetic structure in a beetle-associated nematode
The distribution of a species is a complex expression of its ecological and evolutionary history and integrating population genetic, environmental, and ecological data can provide new insights into the effects of the environment on the population structure of species. In this study we evaluate the role of the environment in shaping the structure and distribution of nematode populations. Despite the fact that geographic populations of Pristionchus pacificus comprise vast genetic diversity sourced from multiple ancestral lineages, we find strong evidence for local associations between environment and genetic variation. Significantly more genetic variation in P. pacificus populations is explained by environmental variation than by geographic distances. This supports a strong role for environmental heterogeneity vs. genetic drift in the divergence of populations, which we suggest may be influenced by adaptive forces.
landscape and oceanic barriers shape dispersal and population structure in the island nematode pristionchus pacificus
Despite the biological importance and diversity of nematodes, little is known of the factors influencing their dispersal and shaping their evolutionary history. Here we study La Réunion and Mauritius Islands and find that both locations were most likely colonised by Pristionchus pacificus from similar multiple geographical sources. We show evidence for periodic bi-directional trans-oceanic dispersal between the islands, as well as non-uniform dispersal within La Réunion. Collectively, we show that gene flow in P. pacificus is limited by environmental and oceanic barriers and largely shaped by the intricacies of the nematode–beetle host interaction.
the nematode Pristionchus pacificus as a model system for integrative studies in evolutionary biology
Comprehensive studies of evolution have historically been hampered by division among disciplines. Now, as biology sits firmly in the '-omics' era, it is more important than ever to tackle the evolution of function and form by considering all those research areas involved in the regulation of phenotypes. In this study we review Pristionchus pacificus as a model organism that allows integrative studies of development and evo-devo with ecology and population genetics.
unravelling the evolutionary history of the nematode pristionchus pacificus: from lineage diversification to island colonisation
The hermaphroditic nematode Pristionchus pacificus is a model organism with a range of fully developed genetic tools. The species is globally widespread and highly diverse genetically, consisting of four major independent lineages (lineages A, B, C, and D). Despite its young age (~2.1 Ma), volcanic La Réunion Island harbours all four genetic lineages. In this study we use model-based statistical methods to rigorously test hypotheses regarding the diversification and island colonisation of P. pacificus. Our dating estimates place the most recent common ancestor of P. pacificus lineages at nearly 500,000 generations past. Our demographic analysis supports recent (<150,000 generations) spatial expansion for the island populations and our ABC approach identifies the most likely colonisation order of the island populations. Collectively, our study comprehensively improves previous inferences about the evolutionary history of P. pacificus.
natural variation in chemosensation: lessons from an island nematode
All organisms must interact with their environment, responding in behavioural, chemical, and other ways to various stimuli throughout their life cycles. Characterising traits that directly represent an organisms ability to sense and react to their environment provides useful insight into the evolution of life-history strategies. One such trait for the nematode Pristionchus pacificus, chemosensation, is involved in navigation to beetle hosts. In this study we examine chemosensation in P. pacificus from La Réunion Island. We select strains from a variety of beetle hosts and geographic locations and examine their chemoattraction response toward organic compounds, beetle washes, and live beetles. We find that nematodes show significant differences in their response to various chemicals and show a concerted response towards compounds they most likely directly encounter in the wild. We suggest that divergence in odour-guided behaviour in P. pacificus may therefore have an important ecological component.
multi locus analysis of Pristionchus pacificus on La Réunion island reveals an evolutionary history shaped by multiple introductions, constrained dispersal events and rare out-crossing
In this study we look in depth at fine-scale genetic structure in La Réunion Pristionchus pacificus using microsatellite and mitochondrial sequence data. We find rich genetic diversity among strains, shaped by differentially-timed introductions from diverse sources and in association with different beetle species. We find that genetic differences among strains correspond to arid western and wet eastern climatic zones that have likely limited westward dispersal.
extreme glacial legacies: a synthesis of the antarctic springtail phylogeographic record
In this study we review current phylogeographic knowledge of Antarctic springtail taxa. We show that patterns of high genetic diversity and structure are consistent across different species, which have persisted in glacial refugia across Antarctica over time.
extended ecophysiological analysis of gomphiocephalus hodgsoni (Collembola): flexibility in life history strategy and population response
The springtail Gomphiocephalus hodgsoni is possibly the most well-studied of the continental Antarctic springtails. In this study we examine dispersal ability, desiccation tolerance, and metabolic rate. We show that some G. hodgsoni individuals can survive at least ten days of suspension on the surface of both fresh and sea water. This, coupled with the presence of G. hodgsoni specimens in air and pitfall traps, suggests that dispersal over local scales (i.e. metres) is possible for this species. Our metabolic data show that different populations within the same Antarctic region have different average metabolic rates at both temporal and spatial scales, indicating that distinct populations may respond differently to environmental variables. Overall, we suggest that G. hodgsoni maintains a flexible life history strategy that allows its ecophysiological responses to be dependent on local environmental conditions.
biogeography of circum-antarctic springtails
In this study we examine the effects of isolation on evolutionary diversification and speciation for springtail species in circum-Antarctica, with special focus on members of the genus Cryptopygus. We use phylogenetic analysis of mitochondrial and ribosomal DNA to evaluate existing taxonomy as well as the biogeographic origin of our chosen suite of springtail species. We find that Cryptopygus antarcticus subspecies and species are not monophyletic, while distribution patterns among species/lineages are both dispersal- and vicariance-driven.
testing the effect of metabolic rate on dna variability at the intra-specific level
We are interested in the relationship between metabolic rate and mutation rate so, in this study, we examine whether mass-specific metabolic rate is correlated with root-to-tip distance on a set of mtDNA trees for the springtail Cryptopygus antarcticus travei from sub-Antarctic Marion Island. Unfortunately, we do not find significant evidence that contemporary metabolic rates directly correlate with mutation rate (i.e., root-to-tip distance) once the underlying phylogeny is taken into account. However, we do find significant evidence that metabolic rate is dependent on the underlying mtDNA tree. In other words, lineages with related mtDNA also have similar metabolic rates.
metabolic rate, genetic and microclimate variation among springtail populations from sub-antarctic marion island
In this study we measure metabolic rates in the springtail Cryptopygus antarcticus travei from six geographically distinct populations on sub-Antarctic Marion Island. In conjunction, we screen samples for their mtDNA (COI) haplotype so that we can examine physiological and genetic variation of distinct populations in parallel. We find evidence of genetic differentiation among populations and a general indication of long-term isolation with limited gene flow. We also find support for an overall pattern of metabolic rate structure among populations from different geographic locations on the island. Thus, over the relatively short timescale of Marion Island’s history (<1 Ma), the geographic barriers that have driven population differentiation from a molecular perspective may also have resulted in some physiological differentiation of populations.
temporal and spatial metabolic rate variation in the antarctic springtail gomphiocephalus hodgsoni
Spatial and temporal environmental variation in terrestrial Antarctic ecosystems are known to impact species strongly at a local scale but limited empirical work exists. Building on previous work, in this study we investigate variation in metabolic activity of Gomphiocephalus hodgsoni at Cape Bird, Garwood and Taylor Valleys. We find significant differences between metabolic rates across two years of measurement at Cape Bird. We also find that metabolic rates in Garwood and Taylor Valleys are significantly higher than those at Cape Bird, where habitats are comparable but environmental characteristics differ.
contrasting phylogeographical patterns for springtails reflect different evolutionary histories between the antarctic peninsula and continental antarctica
In this study we examine genetic structure among populations and regions for the springtails Cryptopygus antarcticus antarcticus and Gomphiocephalus hodgsoni. We find that both species have population structures compatible with the presence of historical glacial refugia on Pleistocene (2 Ma–present) time-scales, followed by post-glacial expansions. However, G. hodgsoni shows a fragmented pattern with several ‘phylogroups’ retaining strong ancestral linkages among present-day populations. Conversely, C. a. antarcticus has an excess of rare haplotypes with a much reduced volume of ancestral lineages, possibly indicating historical founder/bottleneck events and widespread expansion. These differences most likely reflect distinct evolutionary histories in each locality despite the resident species having similar life-history characteristics.
temporal metabolic rate variation in a continental antarctic springtail
Few studies on metabolic responses to the unpredictable Antarctic environment have been completed. So, in this study, we measure metabolic rate variation for individual springtails at a continental Antarctic site using a fiber-optic closed respirometry system incorporating a custom-made respiration chamber. We find clear intra-seasonal and temperature-independent variation in mass-specific metabolic rate in Gomphiocephalus hodgsoni, which appears capable of both physiologically and behaviourally 'tuning' in to short-term thermal variability to respond appropriately to the local unpredictable Antarctic habitat.
patterns of population genetic structure for springtails and mites in southern victoria land, antarctica
In this phylogeographic study we compare genetic structure of the springtail Gomphiocephalus hodgsoni and the sympatric mite Stereotydeus mollis throughout their ranges in southern Victoria Land, Antarctica. We find that the two species show similar population sub-structuring among locations and we highlight several potential refugia that may have existed during glacial maxima. We also identify greater levels of genetic divergence in S. mollis and suggest that there is a nucleotide substitution (mutation) rate difference between S. mollis and G. hodgsoni and/or that S. mollis has had a longer association with the Antarctic landscape.
phylogeographic structure suggests multiple glacial refugia in northern victoria land for the endemic antarctic springtail desoria klovstadi (collembola, isotomidae)
In this study we focus on the endemic springtail Desoria klovstadi from northern Victoria Land, Antarctica. We find low levels of sequence divergence (≤ 1.6%) and a strong link between genetic haplotype and geographic location. Such discrete haplotype groupings suggest rare historical dispersal across the Pleistocene (1.8 Ma −11 Ka) and Holocene (11 Ka–present), coupled with repeated extinction, range contraction and expansion events and/or incomplete sampling across the species range.
genetic divergence of three freshwater isopod species from southern new zealand
In this study we switch the focus towards my home country to examine biogeography of three freshwater isopod species (Austridotea annectens, A. lacustris, A. benhami). We find that these three New Zealand species are genetically distinct, with up to 31% divergence. Genetic variability is highest between populations of the two most widely distributed species and divergence is greatest on islands distant from mainland New Zealand and in the discrete Fiordland region. The magnitude of genetic divergence of isopods on the Auckland and Chatham Islands is consistent with these populations having been founded in the Pliocene (5 - 2 Ma) via oceanic dispersal from mainland New Zealand.