Publications by authors named "Ross H Crozier"

35 Publications

Effect of social structure and introduction history on genetic diversity and differentiation.

Mol Ecol 2021 06 5;30(11):2511-2527. Epub 2021 May 5.

Molecular Ecology Group, Department of Ecology, University of Innsbruck, Innsbruck, Austria.

Invasive species are a global threat to biodiversity, and understanding their history and biology is a major goal of invasion biology. Population-genetic approaches allow insights into these features, as population structure is shaped by factors such as invasion history (number, origin and age of introductions) and life-history traits (e.g., mating system, dispersal capability). We compared the relative importance of these factors by investigating two closely related ants, Tetramorium immigrans and Tetramorium tsushimae, that differ in their social structure and invasion history in North America. We used mitochondrial DNA sequences and microsatellite alleles to estimate the source and number of introduction events of the two species, and compared genetic structure among native and introduced populations. Genetic diversity of both species was strongly reduced in introduced populations, which also differed genetically from native populations. Genetic differentiation between ranges and the reduction in microsatellite diversity were more severe in the more recently introduced and supercolonial T. tsushimae. However, the loss of mitochondrial haplotype diversity was more pronounced in T. immigrans, which has single-queen colonies and was introduced earlier. Tetramorium immigrans was introduced at least twice from Western Europe to North America and once independently to South America. Its monogyny might have limited genetic diversity per introduction, but new mutations and successive introductions over a long time may have added to the gene pool in the introduced range. Polygyny in T. tsushimae probably facilitated the simultaneous introduction of several queens from a Japanese population to St. Louis, USA. In addition to identifying introduction pathways, our results reveal how social structure can influence the population-genetic consequences of founder events.
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http://dx.doi.org/10.1111/mec.15911DOI Listing
June 2021

Intraspecific support for the polygyny-vs.-polyandry hypothesis in the bulldog ant Myrmecia brevinoda.

Mol Ecol 2011 Sep 25;20(17):3681-91. Epub 2011 Jul 25.

School of Marine and Tropical Biology, James Cook University, Townsville, QLD 4811, Australia.

The number of queens per colony and the number of matings per queen are the most important determinants of the genetic structure of ant colonies, and understanding their interrelationship is essential to the study of social evolution. The polygyny-vs.-polyandry hypothesis argues that polygyny and polyandry should be negatively associated because both can result in increased intracolonial genetic variability and have costs. However, evidence for this long-debated hypothesis has been lacking at the intraspecific level. Here, we investigated the colony genetic structure in the Australian bulldog ant Myrmecia brevinoda. The numbers of queens per colony varied from 1 to 6. Nestmate queens within polygynous colonies were on average related (r(qq) = 0.171 ± 0.019), but the overall relatedness between queens and their mates was indistinguishable from zero (r(qm) = 0.037 ± 0.030). Queens were inferred to mate with 1-10 males. A lack of genetic isolation by distance among nests indicated the prevalence of independent colony foundation. In accordance with the polygyny-vs.-polyandry hypothesis, the number of queens per colony was significantly negatively associated with the estimated number of matings (Spearman rank correlation R = -0.490, P = 0.028). This study thus provides the rare intraspecific evidence for the polygyny-vs.-polyandry hypothesis. We suggest that the high costs of multiple matings and the strong effect of multiple mating on intracolonial genetic diversity may be essential to the negative association between polygyny and polyandry and that any attempt to empirically test this hypothesis should place emphasis upon these two key underlying aspects.
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http://dx.doi.org/10.1111/j.1365-294X.2011.05195.xDOI Listing
September 2011

Weaver ants Oecophylla smaragdina encounter nasty neighbors rather than dear enemies.

Ecology 2010 Aug;91(8):2366-72

School of Marine and Tropical Biology, James Cook University, Cairns, Queensland 4878, Australia.

The evolution of territorial behavior requires that the benefits of territoriality outweigh the costs. The costs are primarily those of territorial defense against encroaching neighbors or against floaters seeking to establish their own territory. One way to reduce the cost of defense might be to restrict serious conflict to encounters with those posing the greatest threat. Studies of many animals have found that less aggression is shown toward neighbors than toward, strangers, a phenomenon known as the "dear enemy" effect. However, the opposite can also be true, namely, that more aggression is shown toward neighbors than strangers: the "nasty neighbor" effect. This may be particularly true of group-living species that defend a resource-based territory. Here we show that (1) colonies of the weaver ant Oecophylla smaragdina were able to recognize a greater proportion of workers from neighboring colonies as non-colony members; and (2) when recognized as non-colony members, more aggression was exhibited toward neighbors than non-neighbors. We present for the first time evidence that differential levels of aggression involve both a perceptual and behavioral component. On the other hand, we found no evidence that weaver ant workers were better able to recognize workers from previously unknown colonies or responded more aggressively to them, even after a 10-day period of contact. This contrasts with other species in which rapid learning of the identity of new potential enemies has been demonstrated. We suggest that such a response is unnecessary for weaver ants, as encounters with intruders from non-neighboring colonies are probably rare and of little consequence. This study adds to the growing body of evidence that the nasty neighbor effect may be much more common than the dear enemy effect among group-living species.
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http://dx.doi.org/10.1890/09-0561.1DOI Listing
August 2010

Infection with the trypanosome Crithidia bombi and expression of immune-related genes in the bumblebee Bombus terrestris.

Dev Comp Immunol 2010 Jul 16;34(7):705-9. Epub 2010 Feb 16.

School of Marine and Tropical Biology, Centre for Comparative Genomics, James Cook University, Townsville, Queensland 4811, Australia.

Social bees and other insects are frequently parasitized by a large range of different microorganisms. Among these is Crithidia bombi (Kinetoplastida: Trypanosomatidae), a common gut parasite of bumblebees, Bombus spp. (Insecta: Apidae). Bumblebees are important pollinators in commercial and natural environments. There are clear detrimental effects of C. bombi infections on the fitness of bumblebees. However, little has been known about how the bee's immune system responds to infections with trypanosome parasites. Here, we study the immune response of Bombus terrestris on infection by C. bombi. We measured the expression of four immune-related genes (Hemomucin, MyD88, Relish, and TEP7) using RT-qPCR in adult B. terrestris workers that were either healthy or infected with the trypanosome parasite C. bombi. The potential recognition gene Hemomucin was significantly upregulated in the infected bees. Further, there was substantial and significant variation in all four genes among different bumblebee colonies irrespective of infection status.
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http://dx.doi.org/10.1016/j.dci.2010.02.002DOI Listing
July 2010

Integrative taxonomy: a multisource approach to exploring biodiversity.

Annu Rev Entomol 2010 ;55:421-38

Institute of Ecology, University of Innsbruck, Austria.

Good alpha taxonomy is central to biology. On the basis of a survey of arthropod studies that used multiple disciplines for species delimitation, we evaluated the performance of single disciplines. All included disciplines had a considerable failure rate. Rigor in species delimitation can thus be increased when several disciplines chosen for complementarity are used. We present a flexible procedure and stopping rule for integrative taxonomy that uses the information from different disciplines separately. Disagreement among disciplines over the number and demarcation of species is resolved by elucidating and invoking evolutionary explanations for disagreement. With the identification of further promising study organisms and of new questions for in-depth analysis, evolutionary biology should profit from integrative taxonomy. An important rationale is clarity in researcher bias in the decision-making process. The success of integrative taxonomy will further increase through methodological progress, taxonomic training of evolutionary biologists, and balanced resource allocation.
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http://dx.doi.org/10.1146/annurev-ento-112408-085432DOI Listing
February 2010

Ground dwelling ants as surrogates for establishing conservation priorities in the Australian wet tropics.

J Insect Sci 2009 ;9:12

School of Marine and Tropical Biology, James Cook University, Townsville 4811, Australia.

This study aims to identify a set of areas with high biodiversity value over a small spatial scale within the Australian Wet Tropics. We identified sites of high biodiversity value across an altitudinal gradient of ground dwelling ant communities using three measures of biodiversity. The three measures considered were estimated species richness, complementarity between sites and evolutionary history. The latter measure was derived using the systematic nomenclature of the ants to infer a surrogate phylogeny. The goal of conservation assessments could then be achieved by choosing the most diverse site combinations. This approach was found to be valuable for identifying the most diverse site combinations across an altitudinal gradient that could ensure the preservation of terrestrial ground dwelling invertebrates in the Australian Wet Tropics.
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http://dx.doi.org/10.1673/031.009.1201DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC3011884PMC
August 2009

Animal performance and stress: responses and tolerance limits at different levels of biological organisation.

Biol Rev Camb Philos Soc 2009 May 11;84(2):277-92. Epub 2009 Mar 11.

School of Marine and Tropical Biology, James Cook University, Townsville, QLD 4811, Australia.

Recent advances in molecular biology and the use of DNA microarrays for gene expression profiling are providing new insights into the animal stress response, particularly the effects of stress on gene regulation. However, interpretation of the complex transcriptional changes that occur during stress still poses many challenges because the relationship between changes at the transcriptional level and other levels of biological organisation is not well understood. To confront these challenges, a conceptual model linking physiological and transcriptional responses to stress would be helpful. Here, we provide the basis for one such model by synthesising data from organismal, endocrine, cellular, molecular, and genomic studies. We show using available examples from ectothermic vertebrates that reduced oxygen levels and oxidative stress are common to many stress conditions and that the responses to different types of stress, such as environmental, handling and confinement stress, often converge at the challenge of dealing with oxygen imbalance and oxidative stress. As a result, a common set of stress responses exists that is largely independent of the type of stressor applied. These common responses include the repair of DNA and protein damage, cell cycle arrest or apoptosis, changes in cellular metabolism that reflect the transition from a state of cellular growth to one of cellular repair, the release of stress hormones, changes in mitochondrial densities and properties, changes in oxygen transport capacities and changes in cardio-respiratory function. Changes at the transcriptional level recapitulate these common responses, with many stress-responsive genes functioning in cell cycle control, regulation of transcription, protein turnover, metabolism, and cellular repair. These common transcriptional responses to stress appear coordinated by only a limited number of stress-inducible and redox-sensitive transcription factors and signal transduction pathways, such as the immediate early genes c-fos and c-jun, the transcription factors NFkappaB and HIF-1alpha, and the JNK and p38 kinase signalling pathways. As an example of environmental stress responses, we present temperature response curves at organismal, cellular and molecular levels. Acclimation and physiological adjustments that can shift the threshold temperatures for the onset of these responses are discussed and include, for example, adjustments of the oxygen delivery system, the heat shock response, cellular repair system, and transcriptome. Ultimately, however, an organism's ability to cope with environmental change is largely determined by its ability to maintain aerobic scope and to prevent loss in performance. These systemic constraints can determine an organism's long-term survival well before cellular and molecular functions are disturbed. The conceptual model we propose here discusses some of the crosslinks between responses at different levels of biological organisation and the central role of oxygen balance and oxidative stress in eliciting these responses with the aim to help the interpretation of environmental genomic data in the context of organismal function and performance.
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http://dx.doi.org/10.1111/j.1469-185X.2008.00073.xDOI Listing
May 2009

Meta-population structure in a coral reef fish demonstrated by genetic data on patterns of migration, extinction and re-colonisation.

BMC Evol Biol 2008 Sep 12;8:248. Epub 2008 Sep 12.

School of Marine and Tropical Biology, James Cook University, Townsville, Qld 4811, Australia.

Background: Management strategies for coral reefs are dependant on information about the spatial population structure and connectivity of reef organisms. Genetic tools can reveal important information about population structure, however, this information is lacking for many reef species. We used a mitochondrial molecular marker to examine the population genetic structure and the potential for meta-population dynamics in a direct developing coral reef fish using 283 individuals from 15 reefs on the Great Barrier Reef, Australia. We employed a hierarchical sampling design to test genetic models of population structure at multiple geographical scales including among regions, among shelf position and reefs within regions. Predictions from island, isolation-by-distance and meta-population models, including the potential for asymmetric migration, local extinction and patterns of re-colonisation were examined.

Results: Acanthochromis polyacanthus displayed strong genetic structure among regions (PhiST = 0.81, P < 0.0001) that supported an equilibrium isolation-by-distance model (r = 0.77, P = 0.001). Significant structuring across the continental shelf was only evident in the northern region (PhiST = 0.31, P < 0.001) and no evidence of isolation-by-distance was found within any region. Pairwise PhiST values indicated overall strong but variable genetic structure (mean PhiST among reefs within regions = 0.28, 0.38, 0.41), and asymmetric migration rates among reefs with low genetic structure. Genetic differentiation among younger reefs was greater than among older reefs supporting a meta-population propagule-pool colonisation model. Variation in genetic diversities, demographic expansion and population growth estimates indicated more frequent genetic bottlenecks/founder effects and subsequent population expansion in the central and southern regions compared to the northern one.

Conclusion: Our findings provide genetic evidence for meta-population dynamics in a direct developing coral reef fish and we reject the equilibrium island and isolation-by distance models at local spatial scales. Instead, strong non-equilibrium genetic structure appears to be generated by genetic bottlenecks/founder effects associated with population reductions/extinctions and asymmetric migration/(re)-colonisation of such populations. These meta-population dynamics varied across the geographical range examined with edge populations exhibiting lower genetic diversities and higher rates of population expansion than more central populations. Therefore, coral reef species may experience local population reductions/extinctions that promote overall meta-population genetic differentiation.
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http://dx.doi.org/10.1186/1471-2148-8-248DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC2553088PMC
September 2008

A DNA and morphology based phylogenetic framework of the ant genus Lasius with hypotheses for the evolution of social parasitism and fungiculture.

BMC Evol Biol 2008 Aug 19;8:237. Epub 2008 Aug 19.

Department of Zoology, National Science Museum, Hyakunin-chô 3-23-1, Shinjuku-ku, Tokyo 169-0073, Japan.

Background: Ants of the genus Lasius are ecologically important and an important system for evolutionary research. Progress in evolutionary research has been hindered by the lack of a well-founded phylogeny of the subgenera, with three previous attempts disagreeing. Here we employed two mitochondrial genes (cytochrome c oxidase subunit I, 16S ribosomal RNA), comprising 1,265 bp, together with 64 morphological characters, to recover the phylogeny of Lasius by Bayesian and Maximum Parsimony inference after exploration of potential causes of phylogenetic distortion. We use the resulting framework to infer evolutionary pathways for social parasitism and fungiculture.

Results: We recovered two well supported major lineages. One includes Acanthomyops, Austrolasius, Chthonolasius, and Lasius pallitarsis, which we confirm to represent a seventh subgenus, the other clade contains Dendrolasius, and Lasius sensu stricto. The subgenus Cautolasius, displaying neither social parasitism nor fungiculture, probably belongs to the second clade, but its phylogenetic position is not resolved at the cutoff values of node support we apply. Possible causes for previous problems with reconstructing the Lasius phylogeny include use of other reconstruction techniques, possibly more prone to instabilities in some instances, and the inclusion of phylogenetically distorting characters.

Conclusion: By establishing an updated phylogenetic framework, our study provides the basis for a later formal taxonomic revision of subgenera and for studying the evolution of various ecologically and sociobiologically relevant traits of Lasius, although there is need for future studies to include nuclear genes and additional samples from the Nearctic. Both social parasitism and fungiculture evolved twice in Lasius, once in each major lineage, which opens up new opportunities for comparative analyses. The repeated evolution of social parasitism has been established for other groups of ants, though not for temporary social parasitism as found in Lasius. For fungiculture, the independent emergence twice in a monophyletic group marks a novel scenario in ants. We present alternative hypotheses for the evolution of both traits, with one of each involving loss of the trait. Though less likely for both traits than later evolution without reversal, we consider reversal as sufficiently plausible to merit independent testing.
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http://dx.doi.org/10.1186/1471-2148-8-237DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC2542377PMC
August 2008

Genetic caste determination in termites: out of the shade but not from Mars.

Bioessays 2008 Apr;30(4):299-302

School of Marine and Tropical Biology, James Cook University, Townsville, Queensland, Australia.

Several ant species are known with genetic effects on caste determination but, for termites, the role of environment has been assumed to be omnipotent. Now Hayashi et al. report that commitment to the nymph and worker pathways in Reticulitermes speratus follows a simple model involving two alleles at a sex-linked locus. The spread of this system of genetic caste determination seems best explained by selection at the colony level. This remarkable system may be widely applicable throughout termites, although it cannot be universal, and may provide a window into causal aspects of the molecular biology of caste determination.
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http://dx.doi.org/10.1002/bies.20732DOI Listing
April 2008

A role for parasites in stabilising the fig-pollinator mutualism.

PLoS Biol 2008 Mar;6(3):e59

Division of Biology, Imperial College London, Ascot, United Kingdom.

Mutualisms are interspecific interactions in which both players benefit. Explaining their maintenance is problematic, because cheaters should outcompete cooperative conspecifics, leading to mutualism instability. Monoecious figs (Ficus) are pollinated by host-specific wasps (Agaonidae), whose larvae gall ovules in their "fruits" (syconia). Female pollinating wasps oviposit directly into Ficus ovules from inside the receptive syconium. Across Ficus species, there is a widely documented segregation of pollinator galls in inner ovules and seeds in outer ovules. This pattern suggests that wasps avoid, or are prevented from ovipositing into, outer ovules, and this results in mutualism stability. However, the mechanisms preventing wasps from exploiting outer ovules remain unknown. We report that in Ficus rubiginosa, offspring in outer ovules are vulnerable to attack by parasitic wasps that oviposit from outside the syconium. Parasitism risk decreases towards the centre of the syconium, where inner ovules provide enemy-free space for pollinator offspring. We suggest that the resulting gradient in offspring viability is likely to contribute to selection on pollinators to avoid outer ovules, and by forcing wasps to focus on a subset of ovules, reduces their galling rates. This previously unidentified mechanism may therefore contribute to mutualism persistence independent of additional factors that invoke plant defences against pollinator oviposition, or physiological constraints on pollinators that prevent oviposition in all available ovules.
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http://dx.doi.org/10.1371/journal.pbio.0060059DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC2265770PMC
March 2008

Specificity and transmission mosaic of ant nest-wall fungi.

Proc Natl Acad Sci U S A 2008 Jan 14;105(3):940-3. Epub 2008 Jan 14.

School of Marine and Tropical Biology, James Cook University, Townsville, Queensland 4811, Australia.

Mutualism, whereby species interact to their mutual benefit, is extraordinary in a competitive world. To recognize general patterns of origin and maintenance from the plethora of mutualistic associations proves a persisting challenge. The simplest situation is believed to be that of a single mutualist specific to a single host, vertically transmitted from one host generation to the next. We characterized ascomycete fungal associates cultured for nest architecture by the ant subgenera Dendrolasius and Chthonolasius. The ants probably manage their fungal mutualists by protecting them against fungal competitors. The ant subgenera display different ant-to-fungus specificity patterns, one-to-two and many-to-one, and we infer vertical transmission, in the latter case overlaid by horizontal transmission. Possible evolutionary trajectories include a reversal from fungiculture by other Lasius subgenera and inheritance of fungi through life cycle interactions of the ant subgenera. The mosaic indicates how specificity patterns can be shaped by an interplay between host life-cycles and transmission adaptations.
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http://dx.doi.org/10.1073/pnas.0708320105DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC2242721PMC
January 2008

Abandoning aggression but maintaining self-nonself discrimination as a first stage in ant supercolony formation.

Curr Biol 2007 Nov 25;17(21):1903-7. Epub 2007 Oct 25.

School of Marine and Tropical Biology, James Cook University, Townsville, Queensland 4811, Australia.

An ant supercolony is a very large entity with very many queens. Although normal colonies of small extent and few queens remain distinct, a supercolony is integrated harmoniously over a large area [1, 2]. The lack of aggression is advantageous: Aggression is costly, involving direct and indirect losses and recognition errors [3, 4]. Indeed, supercolonial ants are among the ecologically most successful organisms [5-7]. But how supercolonies arise remains mysterious [1, 2, 8]. Suggestions include that reduced within-colony relatedness or reduced self-nonself discrimination would foster supercolony formation [1, 2, 5, 7, 9-12]. However, one risks confusing correlation and causality in deducing the evolution from distinct colonies to supercolonies when observing established supercolonies. It might help to follow up observations of another lack of aggression, that between single-queened colonies in some ant species. We show that the single-queened Lasius austriacus lacks aggression between colonies and occasionally integrates workers across colonies but maintains high within-colony relatedness and self-nonself discrimination. Provided that the ecological framework permits, reduced aggression might prove adaptive for any ant colony irrespective of within-colony relatedness. Abandoning aggression while maintaining discrimination might be a first stage in supercolony formation. This adds to the emphasis of ecology as central to the evolution of cooperation in general [13].
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http://dx.doi.org/10.1016/j.cub.2007.09.061DOI Listing
November 2007

From transcriptome to biological function: environmental stress in an ectothermic vertebrate, the coral reef fish Pomacentrus moluccensis.

BMC Genomics 2007 Oct 5;8:358. Epub 2007 Oct 5.

School of Marine and Tropical Biology, James Cook University, Townsville, QLD 4811, Australia.

Background: Our understanding of the importance of transcriptional regulation for biological function is continuously improving. We still know, however, comparatively little about how environmentally induced stress affects gene expression in vertebrates, and the consistency of transcriptional stress responses to different types of environmental stress. In this study, we used a multi-stressor approach to identify components of a common stress response as well as components unique to different types of environmental stress. We exposed individuals of the coral reef fish Pomacentrus moluccensis to hypoxic, hyposmotic, cold and heat shock and measured the responses of approximately 16,000 genes in liver. We also compared winter and summer responses to heat shock to examine the capacity for such responses to vary with acclimation to different ambient temperatures.

Results: We identified a series of gene functions that were involved in all stress responses examined here, suggesting some common effects of stress on biological function. These common responses were achieved by the regulation of largely independent sets of genes; the responses of individual genes varied greatly across different stress types. In response to heat exposure over five days, a total of 324 gene loci were differentially expressed. Many heat-responsive genes had functions associated with protein turnover, metabolism, and the response to oxidative stress. We were also able to identify groups of co-regulated genes, the genes within which shared similar functions.

Conclusion: This is the first environmental genomic study to measure gene regulation in response to different environmental stressors in a natural population of a warm-adapted ectothermic vertebrate. We have shown that different types of environmental stress induce expression changes in genes with similar gene functions, but that the responses of individual genes vary between stress types. The functions of heat-responsive genes suggest that prolonged heat exposure leads to oxidative stress and protein damage, a challenge of the immune system, and the re-allocation of energy sources. This study hence offers insight into the effects of environmental stress on biological function and sheds light on the expected sensitivity of coral reef fishes to elevated temperatures in the future.
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http://dx.doi.org/10.1186/1471-2164-8-358DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC2222645PMC
October 2007

Lessons from a beetle and an ant: coping with taxon-dependent differences in microsatellite development success.

J Mol Evol 2007 Sep 29;65(3):304-7. Epub 2007 Aug 29.

Institute of Forest Entomology, Forest Pathology and Forest Protection, Department of Forest and Soil Sciences, Boku, University of Natural Resources & Applied Life Sciences, Vienna, Austria.

Microsatellites are powerful markers often isolated de novo for species yet to be investigated. Enriched genomic libraries are usually used for isolation purposes. We critically evaluate the outcome of an enrichment-based protocol applied to two insect species (the ant Lasius austriacus and the beetle Pityogenes chalcographus) which yielded contrasting numbers of suitable loci. Our findings of differences in microsatellite isolation are consistent with the available data on differences in genomic characteristics across these taxa. In the beetle repeated isolation of identical motifs, difficulties in primer development, and multibanded products caused loss of most candidate clones. We identified critical steps during marker development.
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http://dx.doi.org/10.1007/s00239-007-9012-1DOI Listing
September 2007

Heterologous microarray experiments used to identify the early gene response to heat stress in a coral reef fish.

Mol Ecol 2007 Apr;16(8):1749-63

School of Tropical Biology, James Cook University, Townsville, Qld 4811, Australia.

Coral reef fishes are expected to experience rising sea surface temperatures due to climate change. How well tropical reef fishes will respond to these increased temperatures and which genes are important in the response to elevated temperatures is not known. Microarray technology provides a powerful tool for gene discovery studies, but the development of microarrays for individual species can be expensive and time-consuming. In this study, we tested the suitability of a Danio rerio oligonucleotide microarray for application in a species with few genomic resources, the coral reef fish Pomacentrus moluccensis. Results from a comparative genomic hybridization experiment and direct sequence comparisons indicate that for most genes there is considerable sequence similarity between the two species, suggesting that the D. rerio array is useful for genomic studies of P. moluccensis. We employed this heterologous microarray approach to characterize the early transcriptional response to heat stress in P. moluccensis. A total of 111 gene loci, many of which are involved in protein processing, transcription, and cell growth, showed significant changes in transcript abundance following exposure to elevated temperatures. Changes in transcript abundance were validated for a selection of candidate genes using quantitative real-time polymerase chain reaction. This study demonstrates that heterologous microarrays can be successfully employed to study species for which specific microarrays have not yet been developed, and so have the potential to greatly enhance the utility of microarray technology to the field of environmental and functional genomics.
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http://dx.doi.org/10.1111/j.1365-294X.2006.03178.xDOI Listing
April 2007

Phylogenetic analysis of honey bee behavioral evolution.

Mol Phylogenet Evol 2007 May 20;43(2):543-52. Epub 2006 Oct 20.

School of Marine and Tropical Biology, James Cook University, Townsville, Qld 4811, Australia.

DNA sequences from three mitochondrial (rrnL, cox2, nad2) and one nuclear gene (itpr) from all 9 known honey bee species (Apis), a 10th possible species, Apis dorsata binghami, and three outgroup species (Bombus terrestris, Melipona bicolor and Trigona fimbriata) were used to infer Apis phylogenetic relationships using Bayesian analysis. The dwarf honey bees were confirmed as basal, and the giant and cavity-nesting species to be monophyletic. All nodes were strongly supported except that grouping Apis cerana with A. nigrocincta. Two thousand post-burnin trees from the phylogenetic analysis were used in a Bayesian comparative analysis to explore the evolution of dance type, nest structure, comb structure and dance sound within Apis. The ancestral honey bee species was inferred with high support to have nested in the open, and to have more likely than not had a silent vertical waggle dance and a single comb. The common ancestor of the giant and cavity-dwelling bees is strongly inferred to have had a buzzing vertical directional dance. All pairwise combinations of characters showed strong association, but the multiple comparisons problem reduces the ability to infer associations between states between characters. Nevertheless, a buzzing dance is significantly associated with cavity-nesting, several vertical combs, and dancing vertically, a horizontal dance is significantly associated with a nest with a single comb wrapped around the support, and open nesting with a single pendant comb and a silent waggle dance.
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http://dx.doi.org/10.1016/j.ympev.2006.10.013DOI Listing
May 2007

Charting uncertainty about ant origins.

Authors:
Ross H Crozier

Proc Natl Acad Sci U S A 2006 Nov 20;103(48):18029-30. Epub 2006 Nov 20.

School of Marine and Tropical Biology, James Cook University, Townsville, Queensland 4811, Australia.

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http://dx.doi.org/10.1073/pnas.0608880103DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC1838699PMC
November 2006

Age determination in individual wild-caught Drosophila serrata using pteridine concentration.

J Exp Biol 2006 Aug;209(Pt 16):3155-63

School of Tropical Biology, James Cook University, Townsville QLD 4812, Australia.

Fluorescence spectrophotometry can reliably detect levels of the pteridine 6-biopterin in the heads of individual Drosophila serrata Malloch 1927. Pteridine content in both laboratory and field captured flies is typically a level of magnitude higher than the minimally detectable level (mean(lab)=0.54 units, mean(field)=0.44 units, minimum detectable level=0.01 units) and can be used to predict individual age in laboratory populations with high certainty (r2=57%). Laboratory studies of individuals of known age (from 1 to 48 days old) indicate that while pteridine level increases linearly with age, they also increase in a linear manner with rearing temperature and ambient light levels, but are independent of sex. As expected, the longevity of laboratory-reared males (at least 48 days) is higher than the range of predicted ages of wild-caught males based on individual pteridine levels (40 days). However, the predictive equation based on pteridine level alone suggested that a number of wild-caught males were less than 0 days old, and the 95% confidence limits for these predictions based on the inverse regression are broad. The age of the oldest wild-caught male is predicted to fall within the range of 2 to 50 days. The significant effects of temperature and light intensity determined in the laboratory study (effect sizes omega2=14.3 and 20.4%, respectively) suggests that the calibration of the age prediction equation for field populations would be significantly improved when combined with fine-scaled studies of habitat temperature and light conditions. The ability to determine relative age in individual wild-caught D. serrata presents great opportunities for a variety of evolutionary studies on the dynamics of natural populations.
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http://dx.doi.org/10.1242/jeb.02318DOI Listing
August 2006

The evolution of worker caste diversity in social insects.

Am Nat 2006 Mar 30;167(3):390-400. Epub 2006 Jan 30.

Evolutionary Genetics Laboratory, School of Tropical Biology, James Cook University, Townsville, Queensland 4811, Australia.

Morphological diversification of workers is predicted to improve the division of labor within social insect colonies, yet many species have monomorphic workers. Individual-level selection on the reproductive capacities of workers may counter colony-level selection for diversification, and life-history differences between species (timing of caste determination, colony size, genetic variation available) may mediate the strength of this selection. We tested this through phylogenetically independent contrast analyses on a new data set for 35 ant species. Evidence was found that early divergence of queen-worker developmental pathways may facilitate the evolution of worker diversity because queen-worker dimorphism was strongly positively associated with diversity. By contrast, risks for colonies that invest in specialized workers and colony size effects on costs of worker reproduction seem unlikely to strongly affect the evolution of worker diversity because there was no significant association between colony size and diversity when controlling statistically for queen-worker dimorphism. Finally, worker diversity was greater in species with multiple lineages per colony, and it was negatively associated with relatedness in monogynous species. This could be due to high intracolonial genetic variance favoring the expression and evolution of great worker diversity or to diversity evolving more easily when there is selection for repression of worker reproduction (worker policing).
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http://dx.doi.org/10.1086/499545DOI Listing
March 2006

Phylogenetic relationships among species groups of the ant genus Myrmecia.

Mol Phylogenet Evol 2006 Mar;38(3):575-82

Department of Ecology and Systematics, Graduate School of Agriculture, Hokkaido University, Kita-ku, Sapporo 060-8589, Japan.

Phylogenetic relationships among the nine species groups of the predominately Australian ant genus Myrmecia were inferred using 38 Myrmecia species and an outgroup using DNA sequences from two nuclear genes (622nt from 28S rRNA and 1907nt from the long-wave opsin gene). Nothomyrmecia macrops was selected as the most appropriate outgroup based on recent reliable studies showing monophyly of Myrmecia with Nothomyrmecia. The four species groups with an occipital carina (those of gulosa, nigrocincta, urens, and picta) were found to form a paraphyletic and basal assemblage out of which the five species groups lacking an occipital carina (those of aberrans, mandibularis, tepperi, cephalotes, and pilosula) arise as a strongly supported monophyletic assemblage. Monophyly was supported for four groups (those of gulosa, nigrocincta, picta, and mandibularis) but the situation is unclear for four others (those of urens, aberrans, tepperi, and pilosula). The aberrans group appears to be basal within the group lacking an occipital carina; a previous suggestion that it is the sister group to the rest of the genus is thus not supported.
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http://dx.doi.org/10.1016/j.ympev.2005.09.021DOI Listing
March 2006

Variation in positive selection in termite GNBPs and Relish.

Mol Biol Evol 2006 Feb 12;23(2):317-26. Epub 2005 Oct 12.

School of Tropical Biology, James Cook University, Douglas, Australia.

Social insects are model organisms for investigating molecular evolution in the innate immune system. Their diversity affords comparative analysis among closely related species, and group living is likely to contribute to the pathogen stress imposed on the immune system. We used different models of nucleotide substitution at nonsynonymous (amino acid altering) and synonymous (silent) sites to compare the different levels and type of selection among three immunity genes in 13 Australian termite species (Nasutitermes). The immunity genes include two encoding pathogen recognition proteins (gram-negative bacterial-binding proteins) that duplicated and diverged before or soon after the evolution of the termites and a transcription factor (Relish), which induces the production of antimicrobial peptides. A comparison of evolutionary models that assign four unrestricted classes of dN/dS (the ratio of the nonsynonymous to synonymous substitution rate) to different Nasutitermes lineages revealed that the occurrence of positive selection (dN/dS > 1) varies among lineages and the three genes. Positive selection appears to have driven the evolution of all three genes in an ancestral lineage of three subterranean termites. It had previously been suggested that there was a transition along this ancestral lineage to termite morphology and ecology associated with a diet of decayed wood, a diet that may expose termites to elevated levels of fungal and bacterial pathogens. Relish appears to have experienced the highest levels of selective pressure for change among all three genes. Positively selected sites in the molecule are located in regions that are important for its activation, which suggests that amino acid substitutions at these sites are a counter response to pathogen mechanisms that disrupt the activation of Relish.
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http://dx.doi.org/10.1093/molbev/msj037DOI Listing
February 2006

Molecular phylogeny of the benthic shallow-water octopuses (Cephalopoda: Octopodinae).

Mol Phylogenet Evol 2005 Oct;37(1):235-48

School of Tropical Biology, James Cook University, Townsville, Qld, Australia.

Octopus has been regarded as a "catch all" genus, yet its monophyly is questionable and has been untested. We inferred a broad-scale phylogeny of the benthic shallow-water octopuses (subfamily Octopodinae) using amino acid sequences of two mitochondrial DNA genes: Cytochrome oxidase subunit III and Cytochrome b apoenzyme, and the nuclear DNA gene Elongation Factor-1alpha. Sequence data were obtained from 26 Octopus species and from four related genera. Maximum likelihood and Bayesian approaches were implemented to estimate the phylogeny, and non-parametric bootstrapping was used to verify confidence for Bayesian topologies. Phylogenetic relationships between closely related species were generally well resolved, and groups delineated, but the genes did not resolve deep divergences well. The phylogenies indicated strongly that Octopus is not monophyletic, but several monophyletic groups were identified within the genus. It is therefore clear that octopodid systematics requires major revision.
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http://dx.doi.org/10.1016/j.ympev.2005.05.009DOI Listing
October 2005

Single nucleotide +1 frameshifts in an apparently functional mitochondrial cytochrome b gene in ants of the genus Polyrhachis.

J Mol Evol 2005 Feb;60(2):141-52

Department of Biological Sciences, Simon Fraser University, Burnaby, B.C., Canada V5A 1S6.

Twelve of 30 species examined in the ant genus Polyrhachis carry single nucleotide insertions at one or two positions within the mitochondrial cytochrome b (cytb) gene. Two of the sites are present in more than one species. Nucleotide substitutions in taxa carrying insertions show the strong codon position bias expected of functional protein coding genes, with substitutions concentrated in the third positions of the original reading frame. This pattern of evolution of the sequences strongly suggests that they are functional cytb sequences. This result is not the first report of +1 frameshift insertions in animal mitochondrial genes. A similar site was discovered in vertebrates, where single nucleotide frameshift insertions in many birds and a turtle were reported by Mindell et al. (Mol Biol Evol 15:1568, 1998). They hypothesized that the genes are correctly decoded by a programmed frameshift during translation. The discovery of four additional sites gives us the opportunity to look for common features that may explain how programmed frameshifts can arise. The common feature appears to be the presence of two consecutive rare codons at the insertion site. We hypothesize that the second of these codons is not efficiently translated, causing a pause in the translation process. During the stall the weak wobble pairing of the tRNA bound in the peptidyl site of the ribosome, together with an exact Watson-Crick codon-anticodon pairing in the +1 position, allows translation to continue in the +1 reading frame. The result of these events is an adequate level of translation of a full-length and fully functional protein. A model is presented for decoding of these mitochondrial genes, consistent with known features of programmed translational frameshifting in the yeast TY1 and TY3 retrotransposons.
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http://dx.doi.org/10.1007/s00239-004-0178-5DOI Listing
February 2005

Phylogenetic biodiversity assessment based on systematic nomenclature.

Evol Bioinform Online 2007 Feb 21;1:11-36. Epub 2007 Feb 21.

School of Tropical Biology, James Cook University, Townsville, Queensland, Australia.

Biodiversity assessment demands objective measures, because ultimately conservation decisions must prioritize the use of limited resources for preserving taxa. The most general framework for the objective assessment of conservation worth are those that assess evolutionary distinctiveness, e.g. Genetic (Crozier 1992) and Phylogenetic Diversity (Faith 1992), and Evolutionary History (Nee & May 1997). These measures all attempt to assess the conservation worth of any scheme based on how much of the encompassing phylogeny of organisms is preserved. However, their general applicability is limited by the small proportion of taxa that have been reliably placed in a phylogeny. Given that phylogenizaton of many interesting taxa or important is unlikely to occur soon, we present a framework for using taxonomy as a reasonable surrogate for phylogeny. Combining this framework with exhaustive searches for combinations of sites containing maximal diversity, we provide a proof-of-concept for assessing conservation schemes for systematized but un-phylogenised taxa spread over a series of sites. This is illustrated with data from four studies, on North Queensland flightless insects (Yeates et al. 2002), ants from a Florida Transect (Lubertazzi & Tschinkel 2003), New England bog ants (Gotelli & Ellison 2002) and a simulated distribution of the known New Zealand Lepidosauria (Daugherty et al. 1994). The results support this approach, indicating that species, genus and site numbers predict evolutionary history, to a degree depending on the size of the data set.
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http://www.ncbi.nlm.nih.gov/pmc/articles/PMC2658867PMC
February 2007

Duplication and diversifying selection among termite antifungal peptides.

Mol Biol Evol 2004 Dec 18;21(12):2256-64. Epub 2004 Aug 18.

School of Tropical Biology, James Cook University, Townsville, Queensland, Australia.

We have identified and analyzed the mRNA sequence of 20 new defensin-like peptides from 11 Australian termite species of Nasutitermes and from an outgroup, Drepanotermes rubriceps. The sequence was amplified by reverse transcriptase PCR with a degenerate primer designed from termicin, an antifungal peptide previously characterized from the termite Pseudocanthotermes spiniger. All 20 genes show high sequence identity with P. spiniger termicin and have duplicated repeatedly during the radiation of Nasutitermes. Comparison of the relative fixation rates of synonymous (silent) and nonsynonymous (amino acid altering) mutations indicates that the Nasutitermes termicins are positively selected. This positive selection appears to drive a decrease in termicin charge. In termites with two genes, the decrease in charge is predominantly restricted to one termicin. Furthermore, the spread of charge is significantly greater within species than across species among amino acid sites that appear to be under strong positive selection and this spread is attributable to only three sites. Our results suggest that after termicin duplication, certain critical sites have maintained a positive charge in one duplicate and evolved towards neutrality in the other and that positive selection has directed these changes repeatedly and independently. This diversification among duplicated genes may be a counter-response to the evolution of fungal resistance in social insects that are particularly vulnerable to fungal epidemics.
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http://dx.doi.org/10.1093/molbev/msh236DOI Listing
December 2004

Mating system and population structure of the primitively eusocial wasp Ropalidia revolutionalis: a model system for the evolution of complex societies.

Mol Ecol 2004 Jul;13(7):1943-50

School of Tropical Biology, James Cook University, Douglas, QLD 4811, Australia.

Mating systems are important determinants of genetic structure in cooperative groups, and their effects can influence profoundly the interactions of group members. The primitively eusocial wasp, Ropalidia revolutionalis, has an interesting genetic and social structure that makes it an excellent model system for examining the evolution of more complex societies. In particular, its colonies sometimes have multiple queens, a key characteristic of more advanced wasp societies. In this study, we have characterized the mating system of the social wasp Ropalidia revolutionalis to understand better its colony genetic structure. R. revolutionalis females nearly always mate singly and they are unrelated to their mates. However, different females in the same colony do mate with males, on average, who are related as cousins. Single mating will help to maintain high relatedness, which should be important for continued cooperation in multiple queen societies, but it creates potential conflicts in single queen colonies over the production of males as well as over the timing of male production. We have also characterized the population structure of R. revolutionalis from Townsville, in tropical north Queensland, to Brisbane in the subtropics. Even at such a large scale, the population is remarkably unstructured with an average F(ST) of 0.0546. There is weak isolation by distance, and evidence for subtle differentiation between a southern region with no dry season, which extends as far north as Rockhampton, and a northern region with a severe to moderate dry season. This may reflect historical effects of extreme aridity on the population structure.
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http://dx.doi.org/10.1111/j.1365-294X.2004.02176.xDOI Listing
July 2004

A tree island approach to inferring phylogeny in the ant subfamily Formicinae, with especial reference to the evolution of weaving.

Mol Phylogenet Evol 2003 Nov;29(2):317-30

Department of Genetics and Evolution, La Trobe University, Bundoora, Vic 3083, Australia.

The ant subfamily Formicinae is a large assemblage (2458 species (J. Nat. Hist. 29 (1995) 1037), including species that weave leaf nests together with larval silk and in which the metapleural gland-the ancestrally defining ant character-has been secondarily lost. We used sequences from two mitochondrial genes (cytochrome b and cytochrome oxidase 2) from 18 formicine and 4 outgroup taxa to derive a robust phylogeny, employing a search for tree islands using 10000 randomly constructed trees as starting points and deriving a maximum likelihood consensus tree from the ML tree and those not significantly different from it. Non-parametric bootstrapping showed that the ML consensus tree fit the data significantly better than three scenarios based on morphology, with that of Bolton (Identification Guide to the Ant Genera of the World, Harvard University Press, Cambridge, MA) being the best among these alternative trees. Trait mapping showed that weaving had arisen at least four times and possibly been lost once. A maximum likelihood analysis showed that loss of the metapleural gland is significantly associated with the weaver life-pattern. The graph of the frequencies with which trees were discovered versus their likelihood indicates that trees with high likelihoods have much larger basins of attraction than those with lower likelihoods. While this result indicates that single searches are more likely to find high- than low-likelihood tree islands, it also indicates that searching only for the single best tree may lose important information.
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http://dx.doi.org/10.1016/s1055-7903(03)00114-3DOI Listing
November 2003

Isolation and characterization of a termite transferrin gene up-regulated on infection.

Insect Mol Biol 2003 Feb;12(1):1-7

School of Tropical Biology, James Cook University, Townsville, Queensland, Australia.

PCR-based subtractive hybridization was used to isolate genes preferentially expressed in a termite (Mastotermes darwiniensis) following exposure to an entomopathogenic fungus. The subtraction procedure yielded a cDNA clone encoding a putative transferrin that, when sequenced to its ends, is the largest (728 amino acids) for any insect transferrin characterized to date. Cysteines and residues comprising putative iron-binding sites are conserved in both N- and C-terminal lobes, suggesting structural and functional similarity to diferric vertebrate transferrins. A quantitative PCR assay confirmed a significant increase in transferrin expression following infection, suggesting its up-regulation is part of the innate immune response. However, codon-based tests for selection among known insect transferrins revealed only a small proportion of codon-sites positively selected. Thus, unlike certain vertebrate transferrin lineages, no widespread evidence for pathogen-mediated positive selection was detected at this locus.
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http://dx.doi.org/10.1046/j.1365-2583.2003.00381.xDOI Listing
February 2003
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