Parmakelis et al. 2010 PLoS ONE

Anopheles immune genes and amino acid sites evolving under the effect of positive selection

Abstract- It has long been the goal of vector biology to generate genetic knowledge that can be used to "manipulate" natural populations of vectors to eliminate or lessen disease burden. While long in coming, progress toward reaching this goal has been made. Aiming to increase our understanding regarding the interaction between Plasmodium and the Anopheles immune genes, we investigate the patterns of genetic diversity of four anti-Plasmodium genes in the Anopheles gambiae complex of species.

A Parmakelis, M Moustaka, N Poulakakis, C Louis, MA Slotman, JC Marshall, PH Awono-Ambene, C Antonio-Nkondjio, F Simard, A Caccone, and JR Powell (2010) PLoS ONE 5:e8885

Marshall et al. 2009 IJEE

In the academic job market, will you be competitive? A case study in ecology and evolutionary biology

Abstract- Over the last several decades, the percentage of permanent faculty positions at universities has declined significantly. This creates intense competiton for these positions. Data summarizing the general qualifications of newly hired first-time professors are valuable for students contemplating graduate school. Here we present data collected in a survey from 181 newly hired faculty members in the fields of ecology and evolutionary biology from around the world. We report the average number of publications, courses taught, years as postdoctoral fellows, and research grants received for successful job applicants. Our results indicate and extremely competitive environment for permanent academic jobs in the field of ecology and evolutionary biology.

JC Marshall, P Butars, T Callahan, JJ Dennehy, DJ Harris, B Lunt, M Mika, and R Shupe (2009) Israel Journal of Ecology and Evolutionary Biology 55:381-392

New DNA Analysis Station

Dr. Jon Clark and I received a grant this year to build a DNA analysis station to add to the College of Science DNA laboratory. The funds were generously provided by the Dee Family Technology Grant. Above WSU undergraduate student Austin Earley edits DNA sequences at the new station.

Rameriz et al. 2009 HCB

Fat body and liver mass cycles in S. grammicus (Squamata: Phrynosomatidae) from southern Hidalgo, Mexico

Abstract—We describe changes in liver and fat body mass of males and females of the viviparous lizard, Sceloporus grammicus from southeastern Hidalgo, México. The changes in the masses of the liver and fat bodies of males and females are usually asynchronous. Typically, reproductively active males and females deplete fat body reserves and experience increased liver mass. However, we observed maximum fat body and liver masses during spermatogenesis (July-August) and vitellogenesis (July-November). In females, the liver and fat body masses decreased while carrying developing embryos. This pattern demonstrates the ability of these lizards to bolster energy reserves during reproductive activity and the high energetic cost associated with embryo development. Also, this response pattern is similar to other populations of this species and to some other species of temperate lizards.

A RAMÍREZ-BAUTISTA,D HERNÁNDEZ-RAMOS, AR MARTINEZ, AND JC MARSHALL

Centro de Investigaciones Biológicas, Universidad Autónoma del Estado de Hidalgo, A.P. 1-69 Plaza Juárez, C.P. 42001, Pachuca, Hidalgo, México, Department of Zoology, Weber State University, Ogden, Utah 84408, USA

Herpetological Conservation and Biology 4(2):164-170

Traveling Field Station

New addition to the Marshall lab.

Summer Field Work 2009

Dr. Marshall was invited to give a talk at the research campus of the Universidade do Porto in May a few days after classes ended.  After the talk he spent nearly two weeks in the field collecting lizards, snakes, turtles, and spiders, across Portugal, Spain, and mostly Morocco.  The research team was headed by Dr. D. James Harris and included people from Spain, Portugal, England, and Holland.

Perez-Losada et al. MPE 2009

The Aporrectodea caliginosa species complex includes the most abundant earthworms in grasslands and agricultural ecosystems of the Paleartic region. Historically this complex consisted of the following taxa: A. caliginosa s.s. Savigny, 1826, A. trapezoides Dugés (1828), A. tuberculata (Eisen, 1874), and A. nocturna Evans (1946). These four taxa are morphologically very similar and difficult to differentiate because of their morphological variability. Consequently, their taxonomic status and their phylogenetic relationships have been a matter of discussion for more than a century. To study these questions, we sequenced the COII (686 bp), 12S (362 bp), 16S (1200 bp), ND1 (917 bp), and tRNAs_{Asn-Asp-Val-Leu-Ala-Ser-Leu} (402 bp) mitochondrial and 28S (809 bp) nuclear gene regions for 85 European earthworms from 27 different localities belonging to the A. caliginosa species complex and four outgroup taxa. DNA sequences were analyzed using maximum parsimony, maximum likelihood, and Bayesian approaches of phylogenetic inference. The resulting trees were combined with morphological, ecological, and genomic evidence to test species boundaries (i.e., integrative approach). Our molecular analyses showed that A. caliginosa s.s. and A. tuberculata form a sister clade to A. trapezoides, A. longa, and A. nocturna, which indicates that A. longa is part of the A. caliginosa species complex. We confirm the species status of all these taxa and identify two unrecognized Aporrectodea species in Corsica (France). Moreover our analyses also showed the presence of highly divergent lineages within A. caliginosa, A. trapezoides, and A. longa, suggesting the existence of cryptic diversity within these taxa.

Perez-Losada, M., R. Maigualida, J.C. Marshall, and J. Dominguez (2009) Phylogenetic assessment of the earthworm Aporrectodea caliginosa species complex (Oligochaeta: Lumbricidae) based on mitochondrial and nuclear DNA sequences. Molecular Phylogenetics and Evolution 52: 293–302

Evolution Meetings, Moscow, Idaho 2009

Weber State undergraduate student Paul Buttars presents the poster:

In the Academic Job Market, Will You Be Competitive? A Case Study in Ecology and Evolutionary Biology

Jonathon C. Marshall¹*, Paul Buttars¹, Thomas Callahan², John J. Dennehy³, D. James Harris⁴, Bryce Lunt², and Robert Shupe²

¹Dept. of Zoology, Weber State University, Ogden, UT, USA; ²Dept. of Biology Southern Utah University, Cedar City, UT, USA; ³Queens College and the Graduate Center of the City University of New York, Flushing, NY, USA; ⁴Centro de Investigação em Biodiversidade e Recursos Genéticos, Vairão, Portugal.

Marshall et al. EA 2008

Abstract- The evolutionary processes at play between island and mainland populations of the malaria mosquito vector Anopheles gambiae sensu stricto are of great interest as islands may be suitable sites for preliminary application of transgenic-based vector control strategies. Sao Tome´ and Prıncipe, located off the West African coast, have received such attention in recent years. This study investigates the degree of isolation of An. gambiae s.s. populations between these islands and the mainland based on mitochondrial and ribosomal DNA molecular data. We identify possible continental localities from which these island populations derived. For these purposes, we used FST values, haplotype networks, and nested clade analysis to estimate migration rates and patterns. Haplotypes from both markers are geographically widespread across the African continent. Results indicate that the populations from Sao Tome´ and Prıncipe are relatively isolated from continental African populations, suggesting they are promising sites for test releases of transgenic individuals. These island populations are possibly derived from two separate continental migrations. This result is discussed in the context of the history of the African slave trade with respect to Sao Tome and Prıncipe.

Marshall, JC, J Pinto, JD Charlwood, G Gabriele, F Santolamazza, F Simard, A della Torre, MJ Donnelly, and A Caccone. 2008. Exploring the origin and degree of isolation of Anopheles gambiae from the islands of Sao Tome and Principe, potential sites for testing transgenic-based vector control. Evolutionary Applications 1: 631-644.

Parmakelis et al. 2008

Background: If the insect innate immune system is to be used as a potential blocking step in transmission of malaria, then it will require targeting one or a few genes with highest relevance and ease of manipulation. The problem is to identify and manipulate those of most importance to malaria infection without the risk of decreasing the mosquito's ability to stave off infections by microbes in general. Molecular evolution methodologies and concepts can help identify such genes. Within the setting of a comparative molecular population genetic and phylogenetic framework, involving six species of the Anopheles gambiae complex, we investigated whether a set of four preselected immunity genes (gambicin, NOS, Rel2 and FBN9) might have evolved under selection pressure imposed by the malaria parasite.

Results: We document varying levels of polymorphism within and divergence between the species, in all four genes. Introgression and the sharing of ancestral polymorphisms, two processes that have been documented in the past, were verified in this study in all four studied genes. These processes appear to affect each gene in different ways and to different degrees. However, there is no evidence of positive selection acting on these genes.

Conclusion: Considering the results presented here in concert with previous studies, genes that interact directly with the Plasmodium parasite, and play little or no role in defense against other microbes, are probably the most likely candidates for a specific adaptive response against P. falciparum. Furthermore, since it is hard to establish direct evidence linking the adaptation of any candidate gene to P. falciparum infection, a comparative framework allowing at least an indirect link should be provided. Such a framework could be achieved, if a similar approach like the one involved here, was applied to all other anopheline complexes that transmit P. falciparum malaria.

Parmakelis, A, M Slotman, JC Marshall, PH Awono-Ambene, C Antonion-Nkondjio, F Simard, A Caccone, JR Powell. 2008.  The molecular evolution of four anti-malarial immune genes in the Anopholes gambiae species complex. BMC Evolutionary Biology 8:79

Scientific American 2008

I was interviewed for this article titled 'What is a Species' by Carl Zimmer that appeared in the June issue of Scientific American pages 72-79.  This is a great article, written for a general audience, on some of the scientific issues around identifying species in nature.

Slotman et al. PLoS ONE 2007

Background. Co-evolution between Plasmodium species and its vectors may result in adaptive changes in genes that are crucial components of the vector’s defense against the pathogen. By analyzing which genes show evidence of positive selection in malaria vectors, but not in closely related non-vectors, we can identify genes that are crucial for the mosquito’s resistance against Plasmodium. Methodology/Principle Findings. We investigated genetic variation of three anti-malarial genes; CEC1, GNBP-B1 and LRIM1, in both vector and non-vector species of the Anopheles gambiae complex. Whereas little protein differentiation was observed between species in CEC1 and GNBP-B1, McDonald-Kreitman and maximum likelihood tests of positive selection show that LRIM1 underwent adaptive evolution in a primary malaria vector; An. arabiensis. In particular, two adjacent codons show clear signs of adaptation by having accumulated three out of four replacement substitutions. Furthermore, our data indicate that this LRIM1 allele has introgressed from An. arabiensis into the other main malaria vector An. gambiae. Conclusions/Significance. Although no evidence exists to link the adaptation of LRIM1 to P. falciparum infection, an adaptive response of a known anti-malarial gene in a primary malaria vector is intriguing, and may suggest that this gene could play a role in Plasmodium resistance in An. arabiensis. If so, our data also predicts that LRIM1 alleles in An. gambiae vary in their level of resistance against P. falciparum.

Slotman MA, A Parmakelis, JC Marshall, PH Awono-Ambene, C Antonio-Nkondjo, F Simard, A Caccone, JR Powell. 2007. Patterns of selection in anti-malarial immune genes in malaria vectors: evidence for adaptive evolution in LRIM1 in Anopheles arabiensis.  PLoS ONE 2: e793

Marshall et al. Evolution 2006

Abstract. Species form the fundamental units of analysis in many areas of biology and, therefore, rigorous delimitation of this unit is important to a broad array of researchers. Recently, many new empirical methods have been proposed to delimit species in nature, and a large literature exists on the theoretical merit and superiority of each method. However, few empirical studies actually compare the results of these methods applied in the same study system. We used a large allozyme and chromosome dataset to apply a number of genetic-distance, character-based, and tree-based methods to a well-studied, data-rich system: the Sceloporus grammicus lizard complex of central Mexico. We hypothesized species boundaries under a general lineage or evolutionary species conceptual framework in an a priori fashion using mapped restriction-site data (mitochondrial DNA and nuclear rDNA), allozymes, and morphology. We then compared the ability of different methods to recover the ‘‘hypothesized evolutionary species’’ (HES). Highton’s genetic-distance method and a tree-based method consistently recovered all four HES, although sometimes with weak support. With two exceptions, other methods recovered the same HES, but additional groups were weakly delimited and nested within the HES. Given the apparent recent divergence of some of the chromosome races and distinct populations in this complex, these are encouraging results. We emphasize the value of specifying testable criteria as clearly as possible and testing these with methods that make use of different properties of a single dataset.

Marshall, JC, E Arevalo, E Benavides, JL Sites, JW Sites, Jr. 2006. Delimiting species: Comparing methods for mendelian characters using lizards of the Sceloporus grammicus (Squamata: Phrynosomatidae) complex. Evolution 60: 1050-1065

Lee et al. 2006

Abstract- We surveyed Melanoplus femurrubrum populations within the state of Connecticut for genetic diversity at multiple genetic markers, including three mitochondrial [cytochrome oxidase subunit 1 (COI), reduced form of nicotinamide adenine dinucleotide dehydrogenase subunit 2 (ND2), and AT rich] and one nuclear [internal transcribed spacers of the ribosomal DNA cluster (ITS1)] gene regions. All markers were variable, and the AT-rich gene showed the highest sequence divergence. Analysis of molecular variance (AMOVA), fixation index (Fst) analysis, and phylogeographic patterns showed little divergence between northern and southern regions. Estimates of genetic diversity (p) showed higher mitochondrial diversity in the northern region but nearly equal diversity for the ITS1 gene. This study shows for the first time in Melanoplus genetic variation for the ND2, AT rich, and ITS genes within a small geographic area. Our methods and results should be useful for other researchers interested in conducting population-level studies on closely related species.

Lee J, JC Marshall, OJ Schmitz, A Caccone. 2006. Genetic divergence of Connecticut Melanoplus femurrubrum populations. Journal of Heredity 97: 290-293

Crandall & Marshall 2006

KUTV:Researchers Don't Agree If WY Mouse Exists Or Not

May 19, 2006 

Researchers Don't Agree If WY Mouse Exists Or Not

CHEYENNE, Wyo. More research is out on whether the Preble's meadow jumping mouse exists or NOT, and the latest study offers a different view than the last one.This latest review of the Preble's mouse was requested and paid for by the state of Wyoming. Wyoming officials say that two researchers -- Keith Crandall and Jonathan Marshall -- could find NO genetic difference between the Preble's mouse and other mice. Governor Freudenthal said today (Friday) that the latest research shows that the mouse does NOT exist, and thus is NOT entitled to protection as an endangered species. Federal protections for the Preble's mouse stand to hold up development in Preble's mouse habitat in Colorado and Wyoming. Wyoming has asked the federal government to remove the mouse from endangered species protection. A decision is expected sometime before August sixth. A study released in January concluded that the mouse is in fact a distinct subspecies of jumping mouse and therefore is entitled to protection as an endangered species.

Leyte-Manrique et al. BSHM 2006

Resume- El complejo Sceloporus grammicus ha sido un sistema modelo en diversas areas de investigacion. Aqui proporcionamos un resumen de los estudios sobre la morfologia, ecologia, variacion cromosomica, y limites de especies dentro del complejo.  Concluimos que a pesar de la problematica de las sistematica de complejo, se ha realizado un gran avance en el conocimiento del mismo.  Finalmente, es necesario un conocimiento mas coordinado entre las distinctas areas de investigacion para establecer mejor el estatus taxonomico de las poblaciones de este complejo.

Leyte-Manrique, A, U Hernandez-Salinas, E Chavez-Calzada, M del Carmen Sanchez, JC Marshall, y A Ramirez-Bautista. 2006. El complejo Sceloporus grammicus un grup de largartilla en especiacion. Boletin de la Sociedad Herpetologico de Mexico 14: 18-24.

Jimenez-Cruz et al. SWN 2005

ABSTRACT Reproductive and fat body cycles were studied in a population of viviparous lizards (Sceloporus grammicus) from the Teotihuaca´n area, state of Mexico between October 1984 and September 1985. Males reached sexual maturity at a snout-vent length (SVL) of 44.5 mm and at an age of 6 to 7 mo; females reached sexual maturity at 44.1 mm SVL and at an age of 8 to 9 mo. Testicular mass of adult males began to increase in size in May and peaked during July, August, and September. Maximum testicular growth was associated with precipitation, but not with temperature and photoperiod. Enlarged vitellogenic follicles appeared during October, and females contained embryos in stages 1 through 8 during November. Females had embryos in later embryonic stages 29 through 40 from January to April. Vitellogenesis and embryonic development were associated with increasing photoperiod, temperature, and precipitation. Mean litter size was 5.09 6 0.24 (2 to 9). Mean RCM was 0.338 6 0.024 (0.015 to 0.80). Litter size and RCM were positively correlated with female SVL.

JImenez-Cruz, E, A Ramirez-Bautista, JC Marshall, M Lizana-Avia, A Nieto-Montes de Oca. 2005. Reproductive cycel of Sceloporus grammicus (Squamata:Phrynosomatidae) from Teotihuacan, Mexico. The Southwestern Naturalist 50: 178-187.

Marshall et al. AJTMH 2005

Abstract. Malaria kills more than one million people a year, and understanding the historical association between its most notorious causative agent, Plasmodium falciparum, and its mosquito vectors is important in fighting the disease. We present a phylogenetic analysis of a number of species within the mosquito subgenus Cellia based on a selection of mitochondrial and nuclear genes. Although some of these relationships have been estimated in other studies, generally few species were included and/or statistical support at many nodes was low. Here we include two additional species of anthropophilic P. falciparum malaria vectors and reanalyze these relationships using a Bayesian method that allows us to simultaneously incorporate different models of evolution. We report data that indicate a paraphyletic relationship between five anthropophilic African mosquito vectors. Such a relationship suggests that these species can serve as independent natural experiments for anopheline immunologic responses to regular, prolonged contact with P. falciparum.

Marshall, JC, JR Powell, and A Caccone. 2005. Phylogenetic relationships of the anthropophilic Plasmodium falciparum malaria vectors in Africa. American Journal of Tropical Medicine and Hygiene 73: 749-752.

Sites & Marshall AREES 2004

Abstract: Species are routinely used as fundamental units of analysis in biogeography, ecology, macroevolution, and conservation biology. A large literature focuses on defining species conceptually, but until recently little attention has been given to the issue of empirically delimiting species. Researchers confronted with the task of delimiting species in nature are often unsure which method(s) is (are) most appropriate for their system and data type collected. Here, we review twelve of these methods organized into two general categories of tree- and nontree-based approaches. We also summarize the relevant biological properties of species amenable to empirical evaluation, the classes of data required, and some of the strengths and limitations of each method. We conclude that all methods will sometimes fail to delimit species boundaries properly or will give conflicting results, and that virtually all methods require researchers to make qualitative judgments. These facts, coupled with the fuzzy nature of species boundaries, require an eclectic approach to delimiting species and caution against the reliance on any single data set or method when delimiting species.

No one definition has as yet satisfied all naturalists; yet every naturalist knows vaguely what he means when he speaks of a species.

Darwin (1859)

Sites, JW & JC Marshall. 2004. Operational criteria for delimiting species. Annual Review of Ecology, Evolution, and Systematics. 35: 199-227.

Marshall & Ramirez TREE 2004

This is a book review we wrote for the journal Trends in Ecology and Evolution.  In it we compare a socio-political phenomenon that Yale law professor Amy Chua describes with what is happening with scientific research in developing countries and how open-source scientific journals can help ease these tensions.

Marshall, JC and A Ramirez-Bautista. 2004. Politics, science, and global tensions. Trends in Ecology and Evolution 19: 117-118.