Sarah J. Adamowicz

The scale of divergence: A phylogenetic appraisal of intercontinental allopatric speciation in a passively dispersed freshwater zooplankton genus

Molecular studies have enlightened our understanding of freshwater zooplankton biogeography, yet questions remain regarding the scale and commonality of geographic speciation. Here, we present a mtDNA-based phylogenetic hypothesis for 92 Daphnia species from all seven continents, with a focus on North and South America, Europe, and Australia, and use it to explore the frequency, scale, and geographical orientation of allopatric divergence events. Allopatric speciation can conservatively account for at least 42% of cladogenetic events among the species included in our study; most of these involve intercontinental splits. Closely related species pairs are concentrated in the circumarctic region and between northern and southern continents, aligned with bird migration routes, suggesting recent dispersal. By contrast, deeper phylogenetic patterns are consistent with vicariance scenarios linked to continental fragmentation. The possible reasons for the puzzling persistence of these ancient patterns in light of the eroding force of dispersal are considered. Our results demonstrate the high frequency and complex pattern of allopatric speciation in this ancient, passively dispersed genus.

Ephemeroptera, Plecoptera, and Trichoptera fauna of Churchill (Manitoba, Canada): insights into biodiversity patterns from DNA barcoding

Abstract The insect orders Ephemeroptera, Plecoptera, and Trichoptera (EPT) are particularly important for freshwater ecological and biomonitoring studies, but difficulties in their identification to species level impede research. DNA barcoding provides a solution to this problem by linking newly collected specimens to a reference library of authoritatively identified specimens. Here, we consider the ways in which patterns of intraspecific and interspecific genetic divergences in the barcode region can provide rapid insights into the taxonomic identity, morphological features, and geographical distributions of species. Our study led to a >5× increase in the EPT fauna, including 68 caddisfly, 37 mayfly, and 7 stonefly species, recorded from Churchill. DNA barcoding also aided detection of rare taxa, allowed identification of otherwise unidentifiable life stages, revealed several potentially new species of caddisflies and mayflies, and suggested the presence of cryptic species. The new insights into this fauna and the strong congruence between morphological and molecular characters affirm the utility of DNA barcoding for rapid characterization of the diversity of EPT faunas. We also explore the phenology and habitat preferences of Churchills trichopterans and demonstrate that comprehensive sampling is important for documenting biodiversity through DNA barcoding.

New insights into the distribution of polyploid Daphnia : the holarctic revisited and Argentina explored

It has long been known that polyploid organisms are more prevalent in arctic than in temperate environments. Past explanations for this geographical trend have focused on the role of glacial cycles in generating polyploids and the influence of abiotic factors in favouring polyploidy in the north. In combination, these mechanisms probably suffice to explain the observed geographical cline in ploidy levels in members of the Daphnia pulex complex in the Holarctic. While only diploid members of the D. pulex complex are found in the temperate regions of North America and Europe, allozyme and DNA quantification analyses indicate that the southern Argentine pulex‐complex fauna is dominated by polyploids. Indeed, the present study is the first to document the presence of polyploid members of the D. pulex complex in any temperate climate. The results of phylogeographic analyses suggest that this difference in polyploid distribution between the northern and southern hemispheres is based more on ecological and historical contingencies than direct selection for polyploidy. Specifically, competition with diploid relatives probably limits the lower latitudinal range of polyploids in the north, but appears not to have occurred in Argentina. Because of these differences, the present study provides important insights into the diverse factors that determine the distributions and evolutionary fates of polyploid organisms.

DNA barcoding of Northern Nearctic Muscidae (Diptera) reveals high correspondence between morphological and molecular species limits

BackgroundVarious methods have been proposed to assign unknown specimens to known species using their DNA barcodes, while others have focused on using genetic divergence thresholds to estimate “species” diversity for a taxon, without a well-developed taxonomy and/or an extensive reference library of DNA barcodes. The major goals of the present work were to: a) conduct the largest species-level barcoding study of the Muscidae to date and characterize the range of genetic divergence values in the northern Nearctic fauna; b) evaluate the correspondence between morphospecies and barcode groupings defined using both clustering-based and threshold-based approaches; and c) use the reference library produced to address taxonomic issues.ResultsOur data set included 1114 individuals and their COI sequences (951 from Churchill, Manitoba), representing 160 morphologically-determined species from 25 genera, covering 89% of the known fauna of Churchill and 23% of the Nearctic fauna. Following an iterative process through which all specimens belonging to taxa with anomalous divergence values and/or monophyly issues were re-examined, identity was modified for 9 taxa, including the reinstatement of Phaonia luteva (Walker) stat. nov. as a species distinct from Phaonia errans (Meigen). In the post-reassessment data set, no distinct gap was found between maximum pairwise intraspecific distances (range 0.00-3.01%) and minimum interspecific distances (range: 0.77-11.33%). Nevertheless, using a clustering-based approach, all individuals within 98% of species grouped with their conspecifics with high (>95%) bootstrap support; in contrast, a maximum species discrimination rate of 90% was obtained at the optimal threshold of 1.2%. DNA barcoding enabled the determination of females from 5 ambiguous species pairs and confirmed that 16 morphospecies were genetically distinct from named taxa. There were morphological differences among all distinct genetic clusters; thus, no cases of cryptic species were detected.ConclusionsOur findings reveal the great utility of building a well-populated, species-level reference barcode database against which to compare unknowns. When such a library is unavailable, it is still possible to obtain a fairly accurate (within ~10%) rapid assessment of species richness based upon a barcode divergence threshold alone, but this approach is most accurate when the threshold is tuned to a particular taxon.

Increasing morphological complexity in multiple parallel lineages of the Crustacea

The prospect of finding macroevolutionary trends and rules in the history of life is tremendously appealing, but very few pervasive trends have been found. Here, we demonstrate a parallel increase in the morphological complexity of most of the deep lineages within a major clade. We focus on the Crustacea, measuring the morphological differentiation of limbs. First, we show a clear trend of increasing complexity among 66 free-living, ordinal-level taxa from the Phanerozoic fossil record. We next demonstrate that this trend is pervasive, occurring in 10 or 11 of 12 matched-pair comparisons (across five morphological diversity indices) between extinct Paleozoic and related Recent taxa. This clearly differentiates the pattern from the effects of lineage sorting. Furthermore, newly appearing taxa tend to have had more types of limbs and a higher degree of limb differentiation than the contemporaneous average, whereas those going extinct showed higher-than-average limb redundancy. Patterns of contemporary species diversity partially reflect the paleontological trend. These results provide a rare demonstration of a large-scale and probably driven trend occurring across multiple independent lineages and influencing both the form and number of species through deep time and in the present day.

Ancient lakes revisited: from the ecology to the genetics of speciation.

Explosive speciation in ancient lakes has fascinated biologists for centuries and has inspired classical work on the tempo and modes of speciation. Considerable attention has been directed towards the extrinsic forces of speciation—the geological, geographical and ecological peculiarities of ancient lakes. Recently, there has been a resurgence of interest in the intrinsic nature of these radiations, the biological characteristics conducive to speciation. While new species are thought to arise mainly by the gradual enhancement of reproductive isolation among geographically isolated populations, ancient lakes provide little evidence for a predominant role of geography in speciation. Recent phylogenetic work provides strong evidence that multiple colonization waves were followed by parallel intralacustrine radiations that proceeded at relatively rapid rates despite long‐term gene flow through hybridization and introgression. Several studies suggest that hybridization itself might act as a key evolutionary mechanism by triggering major genomic reorganization/revolution and enabling the colonization of new ecological niches in ancient lakes. These studies propose that hybridization is not only of little impediment to diversification but could act as an important force in facilitating habitat transitions, promoting postcolonization adaptations and accelerating diversification. Emerging ecological genomic approaches are beginning to shed light on the long‐standing evolutionary dilemma of speciation in the face of gene flow. We propose an integrative programme for future studies on speciation in ancient lakes.

DNA barcoding reveals diversity of Hymenoptera and the dominance of parasitoids in a sub-arctic environment.

BackgroundInsect diversity typically declines with increasing latitude, but previous studies have shown conflicting latitude-richness gradients for some hymenopteran parasitoids. However, historical estimates of insect diversity and species richness can be difficult to confirm or compare, because they may be based upon dissimilar methods. As a proxy for species identification, we used DNA barcoding to identify molecular operational taxonomic units (MOTUs) for 7870 Hymenoptera specimens collected near Churchill, Manitoba, from 2004 through 2010.ResultsWe resolved 1630 MOTUs for this collection, of which 75% (1228) were ichneumonoids (Ichneumonidae + Braconidae) and 91% (1484) were parasitoids. We estimate the total number of Hymenoptera MOTUs in this region at 2624-2840.ConclusionsThe diversity of parasitoids in this sub-Arctic environment implies a high diversity of potential host species throughout the same range. We discuss these results in the contexts of resolving interspecific interactions that may include cryptic species, and developing reproducible methods to estimate and compare species richness across sites and between surveys, especially when morphological specialists are not available to identify every specimen.

Comparative phylogeography of two North American ‘glacial relict’ crustaceans

The Pleistocene glaciations represent the most recent and dramatic series of habitat changes since the Cretaceous. The impact of these events was particularly acute for aquatic taxa with poor powers of dispersal, but few organisms have evolutionary histories more intimately entwined with the advance and retreat of ice than the ‘glacial relicts’. In this study, we used a mitochondrial gene, cytochrome c oxidase subunit I (COI), to examine and compare the phylogeographical structure of two glacial relict crustaceans (Limnocalanus macrurus and members of the Mysis relicta species group) across North America. In both cases, we found a sharp phylogenetic division between populations from inland lakes formed during glacial retreat, and arctic lakes isolated from polar seas via isostatic rebound. However, the depth of this phylogenetic partition varied between taxa. In L. macrurus, nucleotide sequence divergence of 2.2% between these zones is consistent with its current status as a single morphologically variable species, but in Mysis the split occurred among recently described, morphologically conserved species, at a divergence of 8.2%. The disparity in the depth of divergence indicates a history of recurrent freshwater invasions from the arctic seas, in concordance with previous studies of Eurasian glacial relicts. However, we suggest further consideration of a largely overlooked explanation that could account for some of the discrepancies between molecular divergences and glaciation events. Many cladogenetic events could have occurred in arctic seas prior to the transition to inland waters, a possibility supported both by the complex physical and ionic history of arctic seas and by high marine and estuarine lineage diversity in the north.

Species diversity and phylogeographical affinities of the Branchiopoda (Crustacea) of Churchill, Manitoba, Canada.

The region of Churchill, Manitoba, contains a wide variety of habitats representative of both the boreal forest and arctic tundra and has been used as a model site for biodiversity studies for nearly seven decades within Canada. Much previous work has been done in Churchill to study the Daphnia pulex species complex in particular, but no study has completed a wide-scale survey on the crustacean species that inhabit Churchills aquatic ecosystems using molecular markers. We have employed DNA barcoding to study the diversity of the Branchiopoda (Crustacea) in a wide variety of freshwater habitats and to determine the likely origins of the Churchill fauna following the last glaciation. The standard animal barcode marker (COI) was sequenced for 327 specimens, and a 3% divergence threshold was used to delineate potential species. We found 42 provisional and valid branchiopod species from this survey alone, including several cryptic lineages, in comparison with the 25 previously recorded from previous ecological works. Using published sequence data, we explored the phylogeographic affinities of Churchills branchiopods, finding that the Churchill fauna apparently originated from all directions from multiple glacial refugia (including southern, Beringian, and high arctic regions). Overall, these microcrustaceans are very diverse in Churchill and contain multiple species complexes. The present study introduces among the first sequences for some understudied genera, for which further work is required to delineate species boundaries and develop a more complete understanding of branchiopod diversity over a larger spatial scale.

Flight loss linked to faster molecular evolution in insects

The loss of flight ability has occurred thousands of times independently during insect evolution. Flight loss may be linked to higher molecular evolutionary rates because of reductions in effective population sizes (Ne) and relaxed selective constraints. Reduced dispersal ability increases population subdivision, may decrease geographical range size and increases (sub)population extinction risk, thus leading to an expected reduction in Ne. Additionally, flight loss in birds has been linked to higher molecular rates of energy-related genes, probably owing to relaxed selective constraints on energy metabolism. We tested for an association between insect flight loss and molecular rates through comparative analysis in 49 phylogenetically independent transitions spanning multiple taxa, including moths, flies, beetles, mayflies, stick insects, stoneflies, scorpionflies and caddisflies, using available nuclear and mitochondrial protein-coding DNA sequences. We estimated the rate of molecular evolution of flightless (FL) and related flight-capable lineages by ratios of non-synonymous-to-synonymous substitutions (dN/dS) and overall substitution rates (OSRs). Across multiple instances of flight loss, we show a significant pattern of higher dN/dS ratios and OSRs in FL lineages in mitochondrial but not nuclear genes. These patterns may be explained by relaxed selective constraints in FL ectotherms relating to energy metabolism, possibly in combination with reduced Ne.