Remko Leys

Birth of a biome: insights into the assembly and maintenance of the Australian arid zone biota

The integration of phylogenetics, phylogeography and palaeoenvironmental studies is providing major insights into the historical forces that have shaped the Earths biomes. Yet our present view is biased towards arctic and temperate/tropical forest regions, with very little focus on the extensive arid regions of the planet. The Australian arid zone is one of the largest desert landform systems in the world, with a unique, diverse and relatively well-studied biota. With foci on palaeoenvironmental and molecular data, we here review what is known about the assembly and maintenance of this biome in the context of its physical history, and in comparison with other mesic biomes. Aridification of Australia began in the Mid-Miocene, around 15 million years, but fully arid landforms in central Australia appeared much later, around 1-4 million years. Dated molecular phylogenies of diverse taxa show the deepest divergences of arid-adapted taxa from the Mid-Miocene, consistent with the onset of desiccation. There is evidence of arid-adapted taxa evolving from mesic-adapted ancestors, and also of speciation within the arid zone. There is no evidence for an increase in speciation rate during the Pleistocene, and most arid-zone species lineages date to the Pliocene or earlier. The last 0.8 million years have seen major fluctuations of the arid zone, with large areas covered by mobile sand dunes during glacial maxima. Some large, vagile taxa show patterns of recent expansion and migration throughout the arid zone, in parallel with the ice sheet-imposed range shifts in Northern Hemisphere taxa. Yet other taxa show high lineage diversity and strong phylogeographical structure, indicating persistence in multiple localised refugia over several glacial maxima. Similar to the Northern Hemisphere, Pleistocene range shifts have produced suture zones, creating the opportunity for diversification and speciation through hybridisation, polyploidy and parthenogenesis. This review highlights the opportunities that development of arid conditions provides for rapid and diverse evolutionary radiations, and re-enforces the emerging view that Pleistocene environmental change can have diverse impacts on genetic structure and diversity in different biomes. There is a clear need for more detailed and targeted phylogeographical studies of Australias arid biota and we suggest a framework and a set of a priori hypotheses by which to proceed.

Subterranean archipelago in the Australian arid zone: mitochondrial DNA phylogeography of amphipods from central Western Australia

In 1998, a unique subterranean ecosystem was discovered in numerous isolated calcrete (carbonate) aquifers in the arid Yilgarn region of Western Australia. Previous morphological and genetic analyses of a subterranean water beetle fauna suggest that calcrete aquifers are equivalent to closed island habitats that have been isolated for millions of years. We tested this hypothesis further by phylogeographic analyses of subterranean amphipods (Crangonyctoidea: Paramelitidae and Hyalidae) using mitochondrial DNA sequence data derived from the cytochrome oxidase I gene. Phylogenetic analyses and population genetic analyses (samova) provided strong evidence for the existence of at least 16 crangonyctoid and six hyalid divergent mitochondrial lineages, each restricted in their distribution to a single calcrete aquifer, in support of the ‘subterranean island (archipelago) hypothesis’ and extending its scope to include entirely water respiring invertebrates. Sequence divergence estimates between proximate calcrete populations suggest that calcretes have been isolated at least since the Pliocene, coinciding with a major aridity phase that led to the intermittent drying of surface water. The distribution of calcretes along palaeodrainage channels and on either side of drainage divides, have had less influence on the overall phylogeographic structure of populations, with evidence that ancestral crangonyctoid and hyalid species moved between catchments multiple times prior to their isolation within calcretes. At least two potential modes of evolution may account for the diversity of subterranean amphipod populations: dispersal/vicariance of stygobitic species or colonization of calcretes by surface species and independent evolution of stygobitic characteristics.

Molecular systematics of Australian carrion-breeding blowflies (Diptera : Calliphoridae) based on mitochondrial DNA

Carrion-breeding blowflies have substantial ecological and forensic importance. Because morphological recognition of their immatures is difficult, sequencing of the mtDNA of these flies may assist with their identification. Molecular phylogenetic analysis based on DNA sequences can also clarify evolutionary relationships. In this study, the mitochondrial genes CO1, CO2, ND4 and ND4L were sequenced for 34 species of blowflies, among which are almost all species known or suspected to breed in carrion in Australia. The resulting sequences were analysed using parsimony and maximum-likelihood Bayesian techniques. The results showed that the combination of these four genes should identify most species reliably, although some very closely related taxa could still be misdiagnosed. The data also helped clarify the life histories of Calliphora centralis Malloch, 1927, C. fuscofemorata Malloch, 1927 and C. gilesi Norris, 1994, which have hitherto only been suspected carrion breeders, and revealed that the current subgeneric assignment of taxa within Calliphora Robineau-Desvoidy, based on morphology, requires revision. Unexpectedly, both Chrysomya rufifacies (Macquart, 1843) and Lucilia cuprina (Wiedemann, 1830) were paraphyletic; each probably comprises two distinct species. The application of a molecular-clock approach to the study of the evolutionary divergence of the carrion-breeding blowflies suggests that the speciation of at least the endemic Australian taxa may have been the result of increasing aridification in Australia during the last five million years.

Systematics and evolution of the Australian subterranean hydroporine diving beetles (Dytiscidae), with notes on Carabhydrus

Calcrete aquifers of the Yilgarn area of Western Australia and the Ngalia Basin, Northern Territory, Australia are known to contain a rich invertebrate stygofauna, including the world’s most diverse assemblage of subterranean diving beetles. Here we determine the generic relationships of these subterranean diving beetle species in the tribe Hydroporini and assess their evolutionary origins. Phylogenetic analyses of 1642 base pairs of mitochondrial DNA (mtDNA), comprising segments of CO1, 16S rRNA, tRNAleu and ND1 genes, revealed that the subterranean species from the arid zone, previously classified under the genus Nirripirti Watts & Humphreys (Hydroporini), are all closely related to the genus Paroster Sharp. We synonymise the stygobitic genus Nirripirti with the genus Paroster. Factors that may have been important for the transitions to stygobitic life such as historical and contemporary species distributions, reproductive ecology and body size are discussed. We show that pre-adaptations such as preference for temporary, but seasonally reliable, water and preference to live among gravel and sand along running water would have favoured transitions from surface to stygobitic life, but that large body size may have restricted the likelihood of successful transitions.

Regressive evolution of an eye pigment gene in independently evolved eyeless subterranean diving beetles

Regressive evolution, the reduction or total loss of non-functional characters, is a fairly common evolutionary phenomenon in subterranean taxa. However, the genetic basis of regressive evolution is not well understood. Here we investigate the molecular evolution of the eye pigment gene cinnabar in several independently evolved lineages of subterranean water beetles using maximum likelihood analyses. We found that in eyeless lineages cinnabar has an increased rate of sequence evolution, as well as mutations leading to frame shifts and stop codons, indicative of pseudogenes. These results are consistent with the hypothesis that regressive evolution of eyes proceeds by random mutations, in the absence of selection, that ultimately lead to the loss of gene function in protein-coding genes specific to the eye pathway.

A Mid-Cretaceous Origin of Sociality in Xylocopine Bees with Only Two Origins of True Worker Castes Indicates Severe Barriers to Eusociality

The origin of sterile worker castes, resulting in eusociality, represents one of the major evolutionary transitions in the history of life. Understanding how eusociality has evolved is therefore an important issue for understanding life on earth. Here we show that in the large bee subfamily Xylocopinae, a simple form of sociality was present in the ancestral lineage and there have been at least four reversions to purely solitary nesting. The ancestral form of sociality did not involve morphological worker castes and maximum colony sizes were very small. True worker castes, entailing a life-time commitment to non-reproductive roles, have evolved only twice, and only one of these resulted in discrete queen-worker morphologies. Our results indicate extremely high barriers to the evolution of eusociality. Its origins are likely to have required very unusual life-history and ecological circumstances, rather than the amount of time that selection can operate on more simple forms of sociality.

The superseded female's dilemma: ultimate and proximate factors that influence guarding behaviour of the carpenter bee Xylocopa pubescens

Both solitary and primitively social nests of the facultatively social carpenter bee Xylocopa pubescens can be found throughout most of the breeding season. In social nests there is reproductive division of labour between a dominant forager and a guarding female. Two types of guarding females can be discerned: the young pre-reproductive guards, and older, formerly reproductive guards. The latter type of guard is found when, after a take-over of reproductive dominance either by a nestmate (mostly a daughter) or an intruder, the defeated female stays in the nest instead of leaving to try and found or usurp another nest. She is then manipulated into the role of a guard. The dominant female profits from the presence of the guard since she protects the nest against pollen robbery by conspecifics (Hogendoorn and Velthuis 1993). We have studied why superseded females might “prefer” to remain as a guard, rather than try their luck somewhere else. The hypotheses investigated pertain to (1) the difficulty for the defeated female of finding a new nest and of restarting reproductive activities due to (a) ecological constraints (nest and pollen shortage) and (b) the effect of age and wear on the defeated female; (2) the effects of guarding in terms of inclusive fitness. We found that superseded females remained as guards significantly more often when a nestmate (not necessarily close kin) took over reproductive dominance than when an intruder did so. Other factors associated with the decision of the defeated female to stay or leave were her age and the number of her own young still present after the supersedure. The probability of finding or constructing a new nest was lower for old than for young females. After finding a nest, old females produced less brood than young foundresses. As a result of these two factors old superseded females gained, in terms of inclusive fitness, by staying as guards, whereas young females profited from leaving the nest. We interpret these results as an indication that guarding behaviour has evolved due to kin selection. However, kin discrimination apparently did not occur. Therefore we conclude that in this species kin selection is not, in the proximate frame of reference, based on kin recognition and preference for helping kin.

First Evidence for a Massive Extinction Event Affecting Bees Close to the K-T Boundary

Bees and eudicot plants both arose in the mid-late Cretaceous, and their co-evolutionary relationships have often been assumed as an important element in the rise of flowering plants. Given the near-complete dependence of bees on eudicots we would expect that major extinction events affecting the latter would have also impacted bees. However, given the very patchy distribution of bees in the fossil record, identifying any such extinctions using fossils is very problematic. Here we use molecular phylogenetic analyses to show that one bee group, the Xylocopinae, originated in the mid-Cretaceous, coinciding with the early radiation of the eudicots. Lineage through time analyses for this bee subfamily show very early diversification, followed by a long period of seemingly no radiation and then followed by rapid diversification in each of the four constituent tribes. These patterns are consistent with both a long-fuse model of radiation and a massive extinction event close to the K-T boundary. We argue that massive extinction is much more plausible than a long fuse, given the historical biogeography of these bees and the diversity of ecological niches that they occupy. Our results suggest that events near the K-T boundary would have disrupted many plant-bee relationships, with major consequences for the subsequent evolution of eudicots and their pollinators.

Correlated evolution of mating behaviour and morphology in large carpenter bees (Xylocopa)

Carpenter bees (Xylocopa) display variation in mating strategies. In several subgenera males defend territories that contain resources for females. In other subgenera males defend a small non-resource territory. Here, we investigate the correlation between three morphological traits and mating strategy. We found associations between mating strategy and male eye size, size of the mesosomal gland and sexual colour dimorphism, as well as correlative evolution between the morphological characters. Analysis of the evolutionary pathways shows that resource defence, small glands and monomorphic sexes are ancestral states. Increases in gland size seem to precede or coincide with changes in mating behaviour, but changes towards sexual dimorphism follow changes in mating behaviour. Once a non-resource defence strategy with correlated morphology has evolved there are no reversals to the ancestral states. We discuss the types of selection that may have caused these correlative changes.ZusammenfassungGroße Holzbienen (Gattung Xylocopa) sind sehr unterschiedlich in ihren Paarungsstrategien. In vielen Untergattungen verteidigen die Männchen Territorien, die Ressourcen für die Weibchen enthalten, wie etwa Blüten oder Nistplätze. In anderen Unterordnungen werden verteilte Paarungsplätze (Leks) gefunden, in denen einzelne Männchen kleine Territorien verteidigen, die keine Ressourcen enthalten. Zusätzlich zu dieser Variation der Paarungs Strategien findet man große Unterschiede in der Morphologie der Männchen und in der Farbverschiedenheit zwischen den Geschlechtern. Die zwei wichtigsten morphologischen Unterschiede sind die Größe der männlichen mesosomalen Drüsen, die ein Paarungspheromon erzeugen und die Größe der Augen der Männchen. Sie können erheblich größer oder gleich groß sein wie die der Weibchen.Eine auf zwei nuklearen und zwei mitochondrialen Gensequenzen beruhende gut aufgelöste Phylogenie der Untergattungen (Leys, 2002) erlaubt die Nutzung einer Bayesischen Analyse (Bayestraits) zur Untersuchung des Zusammenhangs zwischen den morphologischen Charakteren (Augengröße, mesosomale Drüsengröße und sexuelle Färbung des Männchens) und der Paarungsstrategie.Wir fanden eine signifikante Assoziation zwischen der Paarungsstrategie und den morphologischen Eigenschaften, sowie eine signifikante korrelative Evolution zwischen den morphologischen Charakteren. Eine Analyse der evolutionären Abläufe legt nahe, dass die Verteidigung von Ressourcen, kleine Drüsen und gleichgestaltige Geschlechter den ursprünglichen Zustand darstellen. Allerdings blieb der ursprüngliche Zustand der Augengröße unklar. Der Zuwachs der Drüsengröße ging offensichtlich der Änderung im Paarungsverhaltens voran oder ist gleichzeitig aufgetreten, während Änderungen des Sexualdimorphismus erst nach den Änderungen des Paarungsverhaltens erfolgten. Sobald sich eine ressourcenunabhängige Verteidigungsstrategie mit den korrelierten morphologischen Veränderungen in Richtung größerer Drüsen, Geschlechtsdimorphismus und normal großen Augen entwickelt hatte, gab es keine Rückkehr zum ursprünglichen Zustand.Die Assoziation zwischen großen Augen und der Strategie der Ressourcenverteidigung könnte das Ergebnis sexueller Selektion innerhalb des Geschlechts sein, bei der die großen Augen den Männchen ermöglichen, eindringende Männchen rasch zu erkennen und zu verjagen. Ohne diese Möglichkeit auszuschließen ist es ebenfalls möglich, dass große Augen durch sexuelle Selektion zwischen den Geschlechtern entstanden, wenn die Männchen, die Weibchen rasch erkennen, einen Selektionsvorteil haben. Die Assoziation zwischen großen mesosomalen Drüsen und der Verteidigung von ressourcenfreien Territorien ist wahrscheinlich ein Resultat von zwischengeschlechtlicher sexueller Selektion, da Männchen mit großen Drüsen Weibchen über größere Entfernungen anlocken können. Wir nehmen weiter an, dass der Färbungsdimorphismus zwischen Männchen und Weibchen das Resultat einer natürlichen Selektion auf kryptische Färbung der Männchen ist.

A revision of the Australian carpenter bees, genus Xylocopa Latreille, subgenera Koptortosoma Gribodo and Lestis Lepeletier & Serville (Hymenoptera : Apidae)

The Australian carpenter bees, genusXylocopa Latreille, subgeneraKoptortosoma Gribodo, and LestisLepeletier & Serville, are revised. Six species of X.(Koptortosoma) are recognised after solving problems with the association of the sexes.Xylocopa (K.) waterhousei, sp. nov. andX. (K.) lieftincki, sp. nov. are described as new, and two previously recognised species, X. (K.) wallabiaLieftinck and X. (K.) xerophila Lieftinck are synonymised withX. (K.) parvula Rayment. Two species ofthe subgenus Lestis are recognised, while the threespecies-level names, X. (L.) gibbonsi Cockerell,X. (L.) violascens Cockerell, andX. (L.) australensis Kirby are synonymised withX. (L.) bombylans (Fabricius). A key for theidentification of the species is provided, and descriptions, information aboutmating behaviour, nesting substrates, flower records and distribution maps aregiven for all species.