David M. Rowell

Arthropod phylogeny: onychophoran brain organization suggests an archaic relationship with a chelicerate stem lineage

Neuroanatomical studies have demonstrated that the architecture and organization among neuropils are highly conserved within any order of arthropods. The shapes of nerve cells and their neuropilar arrangements provide robust characters for phylogenetic analyses. Such analyses so far have agreed with molecular phylogenies in demonstrating that entomostracans+malacostracans belong to a clade (Tetraconata) that includes the hexapods. However, relationships among what are considered to be paraphyletic groups or among the stem arthropods have not yet been satisfactorily resolved. The present parsimony analyses of independent neuroarchitectural characters from 27 arthropods and lobopods demonstrate relationships that are congruent with phylogenies derived from molecular studies, except for the status of the Onychophora. The present account describes the brain of the onychophoran Euperipatoides rowelli, demonstrating that the structure and arrangements of its neurons, cerebral neuropils and sensory centres are distinct from arrangements in the brains of mandibulates. Neuroanatomical evidence suggests that the organization of the onychophoran brain is similar to that of the brains of chelicerates.

Fine-Scale Phylogeographic Congruence Despite Demographic Incongruence in Two Low-Mobility Saproxylic Springtails

Abstract Evolutionary trajectories of codistributed taxa with comparable ecological preferences and dispersal abilities may be similarly impacted by historical landscape-level processes. Species’ responses to changes in a shared biogeographic landscape may be purely concerted, completely independent, or classified as falling within an intermediate part of the continuum bounded by these two extremes. With sufficient molecular data, temporal contrasts of congruence among taxa with respect to these responses can be made. Such contrasts provide insights into the relative influence of ancient versus more recent climatic (and other) impacts on genetic structuring. Using phylogenetic, allele frequency, and genotypic data from two low-mobility, rotting-log-adapted (saproxylic) springtail species (Collembola) from an isolated 100-km-long section of the Great Dividing Range in southeastern Australia, we tested the concerted-response hypothesis over three timescales. Tests of phylogeographic, demographic, and contemporary population-genetic congruence were performed using an integrative approach that draws on both direct (pattern-based) and indirect (scenario-based) analyses. Our data revealed a general pattern of broad-scale similarities in species’ responses to the interaction between Pleistocene climatic cycles and landscape setting, overlaid with some species-specific differences on local geographic and more recent temporal scales. This general pattern of phylogeographic congruence was accompanied by evidence for contemporaneous demographic incongruence indicating that, even at relatively small spatial scales, biogeographic context can exert an overarching influence on genetic structuring.

Phylogeography recapitulates topography: very fine‐scale local endemism of a saproxylic ‘giant’ springtail at Tallaganda in the Great Dividing Range of south–east Australia

Comparative phylogeography can reveal processes and historical events that shape the biodiversity of species and communities. As part of a comparative research program, the phylogeography of a new, endemic Australian genus and species of log‐dependent (saproxylic) collembola was investigated using mitochondrial sequences, allozymes and anonymous single‐copy nuclear markers. We found the genetic structure of the species corresponds with five a priori microbiogeographical regions, with population subdivision at various depths owing to palaeoclimatic influences. Closely related mtDNA haplotypes are codistributed within a single region or occur in adjacent regions, nuclear allele frequencies are more similar among more proximate populations, and interpopulation migration is rare. Based on mtDNA divergence, a late Miocene–late Pliocene coalescence is likely. The present‐day distribution of genetic diversity seems to have been impacted by three major climatic events: Pliocene cooling and drying (2.5–7 million years before present, Mybp), early Pleistocene wet‐dry oscillations (c. 1.2 Mybp) and the more recent glacial‐interglacial cycles that have characterized the latter part of the Quaternary (< 0.4 Mybp).

A tale of two flatties : different responses of two terrestrial flatworms to past environmental climatic fluctuations at Tallaganda in montane southeastern Australia.

Comparative phylogeographic studies of animals with low mobility and/or high habitat specificity remain rare, yet such organisms may hold fine‐grained palaeoecological signal. Comparisons of multiple, codistributed species can elucidate major historical events. As part of a multitaxon programme, mitochondrial cytochrome oxidase I (COI) variation was analysed in two species of terrestrial flatworm, Artioposthia lucasi and Caenoplana coerulea. We applied coalescent demographic estimators and nested clade analysis to examine responses to past, landscape‐scale, cooling‐drying events in a model system of montane forest (Tallaganda). Correspondence of haplotype groups in both species to previously proposed microbiogeographic regions indicates at least four refuges from cool, dry conditions. The region predicted to hold the highest quality refuges (the Eastern Slopes Region), is indicated to have been a long‐term refuge in both species, but so are several other regions. Coalescent analyses suggest that populations of A. lucasi are declining, while C. coerulea is expanding, although stronger population substructure in the former could yield similar patterns in the data. The differences in spatial and temporal genetic variation in the two species could be explained by differences in ecological attributes: A. lucasi is predicted to have lower dispersal ability but may be better able to withstand cold conditions. Thus, different contemporary population dynamics may reflect different responses to recent (Holocene) climate warming. The two species show highly congruent patterns of catchment‐based local genetic endemism with one another and with previously studied slime‐mould grazing Collembola.

Catchments catch all: long-term population history of a giant springtail from the southeast Australian highlands — a multigene approach

Phylogeography can reveal evolutionary processes driving natural genetic‐geographical patterns in biota, providing an empirical framework for optimizing conservation strategies. The long‐term population history of a rotting‐log‐adapted giant springtail (Collembola) from montane southeast Australia was inferred via joint analysis of mitochondrial and multiple nuclear gene genealogies. Contemporary populations were identified using multilocus nuclear genotype clustering. Very fine‐scale sampling combined with nested clade and coalescent‐based analyses of sequences from mitochondrial cytochrome oxidase I and three unlinked nuclear loci uncovered marked population structure, deep molecular divergences, and abrupt phylogeographical breaks over distances on the order of tens of kilometres or less. Despite adaptations that confer low mobility, rare long‐distance gene flow was implicated: novel computer simulations that jointly modelled stochasticity inherent in coalescent processes and that of DNA sequence evolution showed that incomplete lineage sorting alone was unable to explain the observed spatial‐genetic patterns. Impacts of Pleistocene or earlier climatic cycles were detected on multiple timescales, and at least three putative moist forest refuges were identified. Water catchment divisions predict phylogeographical patterning and present‐day population structure with high precision, and may serve as an excellent surrogate for biodiversity indication in sedentary arthropods from topographically heterogeneous montane temperate forests.

Complex sex-linked fusion heterozygosity in the Australian huntsman spider Delena cancerides (Araneae: Sparassidae)

In the vast majority of spider species studied to date, the karyotype is homogeneous in morphology and exclusively telocentric. The sex-determining system consists of one to three X chromosomes in the male and, correspondingly, two to six in the female. This is the case in species of huntsman spiders belonging to the genera Heteropoda (2n=40+3X), Isopoda, Olios, and Pediana (2n=40+3X) and some populations of the colonial species Delena cancerides (2n=40+3X). In other populations of D. cancerides, wholesale fusion of the karyotype has occurred, reducing the standard huntsman karyotype of 43 telocentric chromosomes to 21 metacentrics and 1 telocentric. Eight of the centric fusion products, including an X-autosome fusion, are maintained in the heterozygous condition in males and, with the single telocentric, form a chain of nine chromosomes at meiosis. The two complexes comprising the chain behave as neo-X and neo-Y chromosomes, and thus the ancestral X1X2X3♂∶X1X1X2X2X3X3♀ sex-determining system has been converted to a system of six X and four Y chromosomes in the male and twelve X chromosomes in the female. Since sex-linked complex heterozygosity is also found in a number of species of social termites, it is suggested that such heterozygosity may have adaptive significance for a colonial lifestyle. Breakdown products of the chain of nine are present in specimens of D. cancerides from Canberra and these appear to represent hybrid products between the 2n=22 and 2n=43 forms. Hybridisation may also have been involved in the origin of the chain-forming races.

How did the platypus get its sex chromosome chain? A comparison of meiotic multiples and sex chromosomes in plants and animals

The duck-billed platypus is an extraordinary mammal. Its chromosome complement is no less extraordinary, for it includes a system in which ten sex chromosomes form an extensive meiotic chain in males. Such meiotic multiples are unprecedented in vertebrates but occur sporadically in plant and invertebrate species. In this paper, we review the evolution and formation of meiotic multiples in plants and invertebrates to try to gain insights into the origin of the platypus meiotic multiple. We describe the meiotic hurdles that translocated mammalian chromosomes face, which make longer chains disadvantageous in mammals, and we discuss how sex chromosomes and dosage compensation might have affected the evolution of sex-linked meiotic multiples. We conclude that the evolutionary conservation of the chain in monotremes, the structural properties of the translocated chromosomes and the highly accurate segregation at meiosis make the platypus system remarkably different from meiotic multiples in other species. We discuss alternative evolutionary models, which fall broadly into two categories: either the chain is the result of a sequence of translocation events from an ancestral pair of sex chromosomes (Model I) or the entire chain came into being at once by hybridization of two populations with different chromosomal rearrangements sharing monobrachial homology (Model II).

Unexplored Character Diversity in Onychophora (Velvet Worms): A Comparative Study of Three Peripatid Species

Low character variation among onychophoran species has been an obstacle for taxonomic and phylogenetic studies in the past, however we have identified a number of new and informative characters using morphological, molecular, and chromosomal techniques. Our analyses involved a detailed examination of Epiperipatus biolleyi from Costa Rica, Eoperipatus sp. from Thailand, and a new onychophoran species and genus from Costa Rica, Principapillatus hitoyensis gen. et sp. nov.. Scanning electron microscopy on embryos and specimens of varying age revealed novel morphological characters and character states, including the distribution of different receptor types along the antennae, the arrangement and form of papillae on the head, body and legs, the presence and shape of interpedal structures and fields of modified scales on the ventral body surface, the arrangement of lips around the mouth, the number, position and structure of crural tubercles and anal gland openings, and the presence and shape of embryonic foot projections. Karyotypic analyses revealed differences in the number and size of chromosomes among the species studied. The results of our phylogenetic analyses using mitochondrial COI and 12S rRNA gene sequences are in line with morphological and karyotype data. However, our data show a large number of unexplored, albeit informative, characters in the Peripatidae. We suggest that analysing these characters in additional species would help unravel species diversity and phylogeny in the Onychophora, and that inconsistencies among most diagnostic features used for the peripatid genera in the literature could be addressed by identifying a suite of characters common to all peripatids.

Fixed fusion heterozygosity inDelena cancerides Walck. (Araneae: Sparassidae): an alternative to speciation by monobrachial fusion

Autosomal fusion in spiders is generally an all-or-nothing phenomenon. That is, in respect of the autosomes, spider karyotypes are usually totally telocentric or saturated for fusions.D. cancerides behaves in this manner, but possesses a number of racial cytotypes with different fusion combinations. Two of these are heterozygous for a number of fusions which include a sex chromosome and consequently form long chain multiples during male meiosis. Data are presented to support the hypothesis that these races arose as the result of hybridisation between parental forms homozygous for different fusion combinations. A generalisation of this model states that, when an X-autosome fusion is present, hybridisation of two races with monobrachial homology may result in either of two distinct outcomes. As has been discussed elsewhere, selection may result in premating isolation and hence speciation, however a plausible alternative is that selection for routine alternate segregation will produce stable sex-linked translocation heterozygosity. The adoption of either strategy negates selection for the other and so an evolutionary race between the two ensues.

Source population characteristics affect heterosis following genetic rescue of fragmented plant populations

Understanding the relative importance of heterosis and outbreeding depression over multiple generations is a key question in evolutionary biology and is essential for identifying appropriate genetic sources for population and ecosystem restoration. Here we use 2455 experimental crosses between 12 population pairs of the rare perennial plant Rutidosis leptorrhynchoides (Asteraceae) to investigate the multi-generational (F1, F2, F3) fitness outcomes of inter-population hybridization. We detected no evidence of outbreeding depression, with inter-population hybrids and backcrosses showing either similar fitness or significant heterosis for fitness components across the three generations. Variation in heterosis among population pairs was best explained by characteristics of the foreign source or home population, and was greatest when the source population was large, with high genetic diversity and low inbreeding, and the home population was small and inbred. Our results indicate that the primary consideration for maximizing progeny fitness following population augmentation or restoration is the use of seed from large, genetically diverse populations.