Paul E. Marek

Pleistocene glacial refugia across the Appalachian Mountains and coastal plain in the millipede genus Narceus: Evidence from population genetic, phylogeographic, and paleoclimatic data

BackgroundSpecies that are widespread throughout historically glaciated and currently non-glaciated areas provide excellent opportunities to investigate the role of Pleistocene climatic change on the distribution of North American biodiversity. Many studies indicate that northern animal populations exhibit low levels of genetic diversity over geographically widespread areas whereas southern populations exhibit relatively high levels. Recently, paleoclimatic data have been combined with niche-based distribution modeling to locate possible refugia during the Last Glacial Maximum. Using phylogeographic, population, and paleoclimatic data, we show that the distribution and mitochondrial data for the millipede genus Narceus are consistent with classical examples of Pleistocene refugia and subsequent post-glacial population expansion seen in other organismal groups.ResultsThe phylogeographic structure of Narceus reveals a complex evolutionary history with signatures of multiple refugia in southeastern North America followed by two major northern expansions. Evidence for refugial populations were found in the southern Appalachian Mountains and in the coastal plain. The northern expansions appear to have radiated from two separate refugia, one from the Gulf Coastal Plain area and the other from the mid-Atlantic coastal region. Distributional models of Narceus during the Last Glacial Maximum show a dramatic reduction from the current distribution, with suitable ecological zones concentrated along the Gulf and Atlantic coastal plain. We found a strong correlation between these zones of ecological suitability inferred from our paleo-model with levels of genetic diversity derived from phylogenetic and population estimates of genetic structuring.ConclusionThe signature of climatic change, during and after the Pleistocene, on the distribution of the millipede genus Narceus is evident in the genetic data presented. Niche-based historical distribution modeling strengthens the conclusions drawn from the genetic data and proves useful in identifying probable refugia. Such interdisciplinary biogeographic studies provide a comprehensive approach to understanding these processes that generate and maintain biodiversity as well as the framework necessary to explore questions regarding evolutionary diversification of taxa.

A Müllerian mimicry ring in Appalachian millipedes

Few biological phenomena provide such an elegant and straightforward example of evolution by natural selection as color mimicry among unrelated organisms. By mimicking the appearance of a heavily defended aposematic species, members of a second species gain protection from predators and, potentially, enhanced fitness. Mimicking a preexisting warning advertisement is economical because a potentially costly novel one can be avoided; simultaneously, the addition of more aposematic individuals enhances the overall warning effect. The better-known mimetic systems comprise tropical taxa, but here, we show a remarkable example of color mimicry in 7 species of blind, cyanide-generating millipedes endemic to the Appalachian Mountains of temperate North America. Because these millipedes lack eyes, there is no sexual selection or intraspecific signaling for coloration, providing an ideal system for mimicry studies. We document a Müllerian symbiosis where unrelated species vary in color and pattern over geographical space but appear identical where they co-occur. By using spectral color data, estimations of evolutionary history, and detailed field observations of species abundance, we test 4 predictions of Müllerian mimicry theory and begin to unravel the story of an elaborate mimetic diversification in the forests of Appalachia.

Bioluminescent aposematism in millipedes

Summary Bioluminescence — the ability of organisms to emit light — has evolved about 40–50 times independently across the tree of life [1]. Many different functions for bioluminescence have been proposed, for example, mate recognition, prey attraction, camouflage, and warning coloration. Millipedes in the genus Motyxia produce a greenish-blue light at a wavelength of 495 nm that can be seen in darkness [2]. These detritivores defend themselves with cyanide, which they generate internally and discharge through lateral ozopores [3]. Motyxia are an ideal model system to investigate the ecological role of bioluminescence because they are blind, thus limiting their visual signalling to other organisms, for example predators. While the biochemical mechanisms underlying Motyxia bioluminescence have been studied in detail [2,4], its adaptive significance remained unknown [5,6]. We here show that bioluminescence has a single evolutionary origin in millipedes and it serves as an aposematic warning signal to deter nocturnal mammalian predators. Among the numerous examples of bioluminescence, this is the first field experiment in any organism to demonstrate that bioluminescence functions as a warning signal. Video Abstract The editors of Current Biology welcome correspondence on any article in the journal, but reserve the right to reduce the length of any letter to be published. All Correspondence containing data or scientific argument will be refereed. Queries about articles for consideration in this format should be sent by e-mail to cbiol@current-biology.com

Discovery of a glowing millipede in California and the gradual evolution of bioluminescence in Diplopoda.

Significance The enigmatic millipede Xystocheir bistipita has been rediscovered after a half-century. The rediscovery unexpectedly reveals that the species is bioluminescent. By reconstructing its evolutionary history, we show that X. bistipita is the evolutionary sister of Motyxia, the only bioluminescent millipede genus in the order Polydesmida. We demonstrate that bioluminescence originated in the group’s common ancestor and incrementally grew brighter through evolutionary time. Luminescence in Motyxia may have initially evolved to cope with metabolic stress triggered by a hot, dry environment and was repurposed as a warning signal by species colonizing high-elevation habitats with greater predation risk. The discovery of bioluminescence in X. bistipita and its pivotal evolutionary location provides insight into repeated evolution of bioluminescence across the tree of life. The rediscovery of the Californian millipede Xystocheir bistipita surprisingly reveals that the species is bioluminescent. Using molecular phylogenetics, we show that X. bistipita is the evolutionary sister group of Motyxia, the only genus of New World bioluminescent millipedes. We demonstrate that bioluminescence originated in the group’s most recent common ancestor and evolved by gradual, directional change through diversification. Because bioluminescence in Motyxia has been experimentally demonstrated to be aposematic, forewarning of the animal’s cyanide-based toxins, these results are contrary to aposematic theory and empirical evidence that a warning pattern cannot evolve gradually in unpalatable prey. However, gradual evolution of a warning pattern is plausible if faint light emission served another function and was co-opted as an aposematic signal later in the diversification of the genus. Luminescence in Motyxia stem-group taxa may have initially evolved to cope with reactive oxygen stress triggered by a hot, dry environment and was repurposed for aposematism by high-elevation crown-group taxa colonizing new habitats with varying levels of predation. The discovery of bioluminescence in X. bistipita and its pivotal phylogenetic location provides insight into the independent and repeated evolution of bioluminescence across the tree of life.

Biodiversity hotspots: Rediscovery of the world's leggiest animal

The millipede species Illacme plenipes comes the closest to having its namesakes mythical 1,000 legs — individuals can bear up to 750 legs. Here we record the rediscovery of this extremely rare species, which has not been reported since its original description some 80 years ago, at a tiny locality of 0.8 km2 in San Benito County, California. Because of the rarity and narrow geographical range of this delicate species, its fragile habitat must be protected at all costs.

Multigene Phylogenetics Reveals Temporal Diversification of Major African Malaria Vectors

The major vectors of malaria in sub-Saharan Africa belong to subgenus Cellia. Yet, phylogenetic relationships and temporal diversification among African mosquito species have not been unambiguously determined. Knowledge about vector evolutionary history is crucial for correct interpretation of genetic changes identified through comparative genomics analyses. In this study, we estimated a molecular phylogeny using 49 gene sequences for the African malaria vectors An. gambiae, An. funestus, An. nili, the Asian malaria mosquito An. stephensi, and the outgroup species Culex quinquefasciatus and Aedes aegypti. To infer the phylogeny, we identified orthologous sequences uniformly distributed approximately every 5 Mb in the five chromosomal arms. The sequences were aligned and the phylogenetic trees were inferred using maximum likelihood and neighbor-joining methods. Bayesian molecular dating using a relaxed log normal model was used to infer divergence times. Trees from individual genes agreed with each other, placing An. nili as a basal clade that diversified from the studied malaria mosquito species 47.6 million years ago (mya). Other African malaria vectors originated more recently, and independently acquired traits related to vectorial capacity. The lineage leading to An. gambiae diverged 30.4 mya, while the African vector An. funestus and the Asian vector An. stephensi were the most closely related sister taxa that split 20.8 mya. These results were supported by consistently high bootstrap values in concatenated phylogenetic trees generated individually for each chromosomal arm. Genome-wide multigene phylogenetic analysis is a useful approach for discerning historic relationships among malaria vectors, providing a framework for the correct interpretation of genomic changes across species, and comprehending the evolutionary origins of this ubiquitous and deadly insect-borne disease.

A redescription of the leggiest animal, the millipede Illacme plenipes, with notes on its natural history and biogeography (Diplopoda, Siphonophorida, Siphonorhinidae)

Abstract With up to 750 legs, the millipede Illacme plenipes Cook and Loomis, 1928 is the leggiest animal known on Earth. It is endemic to the northwestern foothills of the Gabilan Range in San Benito County, California, where it is the only known species of the family Siphonorhinidae in the Western Hemisphere. Illacme plenipes is only known from 3 localities in a 4.5 km2 area; the 1926 holotype locality is uncertain. Individuals of the species are strictly associated with large arkose sandstone boulders, and are extremely rare, with only 17 specimens known to exist in natural history collections. In contrast with its small size and unassuming outward appearance, the microanatomy of the species is strikingly complex. Here we provide a detailed redescription of the species, natural history notes, DNA barcodes for Illacme plenipes and similar-looking species, and a predictive occurrence map of the species inferred using niche based distribution modeling. Based on functional morphology of related species, the extreme number of legs is hypothesized to be associated with a life spent burrowing deep underground, and clinging to the surface of sandstone boulders.

The evolutionary relationships of North American Diplous Motschulsky (Coleoptera:Carabidae:Patrobini) inferred from morphological and molecular evidence

Individuals of the ground beetle genus Diplous Motschulsky, 1850 occur in riparian areas predominately throughout boreal North America and Asia. In order to infer the species phylogeny of the North American Diplous, we examined 97 morphological characters (56 quantitative characters and 41 qualitative characters) and 458 bp of the mitochondrial cytochrome oxidase subunit I region. We used the four North American species, four Palearctic species, and one undescribed species of a closely related genus to test the monophyly and the direction of character state change in North American Diplous. Overall, we found that North American Diplous appear to represent a monophyletic group, but that the morphological and molecular evidence did not support the same relationships in the placement of one of the species. We found that the total evidence trees agreed most with biogeography and considerations of accelerated morphological evolution. In this paper, we present a morphological phylogenetic tree, a molecular phylogenetic tree, a total evidence phylogenetic tree, a species key, species diagnoses, and a distribution map of Nearctic Diplous. Additional keywords: COI, cytochrome oxidase subunit I, Diplous, glacier, ground beetle, Platidius, Pleistocene, refugia, riparian, total evidence, vicariance.

Ground-Dwelling Arthropod Communities of a Sky Island Mountain Range in Southeastern Arizona, USA: Obtaining a Baseline for Assessing the Effects of Climate Change

The few studies that have addressed past effects of climate change on species distributions have mostly focused on plants due to the rarity of historical faunal baselines. However, hyperdiverse groups like Arthropoda are vital to monitor in order to understand climate change impacts on biodiversity. This is the first investigation of ground-dwelling arthropod (GDA) assemblages along the full elevation gradient of a mountain range in the Madrean Sky Island Region, establishing a baseline for monitoring future changes in GDA biodiversity. To determine how GDA assemblages relate to elevation, season, abiotic variables, and corresponding biomes, GDA were collected for two weeks in both spring (May) and summer (September) 2011 in the Santa Catalina Mountains, Arizona, using pitfall traps at 66 sites in six distinct upland (non-riparian/non-wet canyon) biomes. Four arthropod taxa: (1) beetles (Coleoptera), (2) spiders (Araneae), (3) grasshoppers and crickets (Orthoptera), and (4) millipedes and centipedes (Myriapoda) were assessed together and separately to determine if there are similar patterns across taxonomic groups. We collected 335 species of GDA: 192/3793 (species/specimens) Coleoptera, 102/1329 Araneae, 25/523 Orthoptera, and 16/697 Myriapoda. GDA assemblages differed among all biomes and between seasons. Fifty-three percent (178 species) and 76% (254 species) of all GDA species were found in only one biome and during only one season, respectively. While composition of arthropod assemblages is tied to biome and season, individual groups do not show fully concordant patterns. Seventeen percent of the GDA species occurred only in the two highest-elevation biomes (Pine and Mixed Conifer Forests). Because these high elevation biomes are most threatened by climate change and they harbor a large percentage of unique arthropod species (11–25% depending on taxon), significant loss in arthropod diversity is likely in the Santa Catalina Mountains and other isolated mountain ranges in the Southwestern US.

A general methodology for collecting and preserving xystodesmid and other large millipedes for biodiversity research.

Abstract Background With an estimated 80% of species remaining undescribed (but see Brewer et al. 2012), millipede taxonomy offers the opportunity to discover new species and explore biodiversity. The lack of basic alpha taxonomic information regarding millipedes belies their significant ecological role and potential as premier models in ecological and evolutionary studies. The group possesses many fascinating biological properties (e.g., bioluminescence, mimicry, and complex chemical secretions) that have been the focus of several recent studies and are emerging avenues of future investigation. New information Here we summarize a methodology for large-bodied millipede collection, curation, and preservation for genetic analyses with the hope that sharing these techniques will stimulate interest in these charismatic detritivores.