EEB Papers - Jeremy Searle

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Professor Searle is Chair of the Department of Ecology and Evolutionary Biology at Cornell University, and is interested in the construction of post-glacial small mammal communities and has studied the natural colonization history of European shrews, voles, mice and small carnivores, revealing a wide range of species- and lineage-specific responses in terms of source areas and pattern of spread. Unnatural colonization history (i.e. transport by humans) is also of interest to him, particularly the way that the phylogeography of small mammals transported by humans can inform about the history of the humans moving them.

Those separate lineages that make up a species and which are formed in different places and colonize in different ways, are genetically differentiated to various degrees and may become separate species themselves. He is interested in the speciation process and the analysis of hybrid zones to inform about that. He has, in particular, studied the origin of chromosomally distinctive lineages, and the hybrid zones between those lineages, using shrews and mice as models.

A more complete and current listing of Prof. Searle's work and scholarly output can be found on his EEB Department web page and the Searle Lab web site, or through the links below.

ResearchGate Profile Page



Recent Submissions

Now showing 1 - 10 of 31
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    The Changing pace of Insular Life: 5000 Years of Microevolution in the Orkney Vole (microtus Arvalis Orcadensis)
    Cucchi, T.; Barnett, R.; Martínková, N.; Renaud, S.; Renvoisé, E.; Evin, A.; Sheridan, A.; Mainland, I.; Wickham?Jones, C.; Tougard, C.; Quéré, J.P.; Pascal, M.; Pascal, M.; Heckel, G.; O'Higgins, P.; Searle, J.B.; Dobney, K.M. (Society for the Study of Evolution, 2014-06-23)
    Island evolution may be expected to involve fast initial morphological divergence followed by stasis. We tested this model using the dental phenotype of modern and ancient common voles (Microtus arvalis), introduced onto the Orkney archipelago (Scotland) from continental Europe some 5000 years ago. First, we investigated phenotypic divergence of Orkney and continental European populations and assessed climatic influences. Second, phenotypic differentiation among Orkney populations was tested against geography, time, and neutral genetic patterns. Finally, we examined evolutionary change along a time series for the Orkney Mainland. Molar gigantism and anterior?lobe hypertrophy evolved rapidly in Orkney voles following introduction, without any transitional forms detected. Founder events and adaptation appear to explain this initial rapid evolution. Idiosyncrasy in dental features among different island populations of Orkney voles is also likely the result of local founder events following Neolithic translocation around the archipelago. However, against our initial expectations, a second marked phenotypic shift occurred between the 4th and 12th centuries AD, associated with increased pastoral farming and introduction of competitors (mice and rats) and terrestrial predators (foxes and cats). These results indicate that human agency can generate a more complex pattern of morphological evolution than might be expected in island rodents.
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    The hypothetical Old-Northern chromosome race of Sorex araneus found in the Ural Mts
    Polyakov, A.V.; Borodin, P.M.; Luká?ová, L.; Searle, J.B.; Zima, J. (Finnish Zoological and Botanical Publishing Board, 1997)
    Chromosomes of two populations of the common shrew, Sorex araneus L. (Mammalia, Insectivora, Soricidae), from the northern Ural Mts. were investigated. In both sites, homozygous, all-metacentric autosomal complements were revealed, with the autosomal arm combinations af, bc, go, hn, ip, jl, km, qr, tu. This karyotype is identical to that predicted by Halkka et al. (1994) as the hypothetical Old-Northern race connecting the northern and eastern ratial groups of Sorex araneus in Eurasia.
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    Synchronous diversification of Sulawesi’s iconic artiodactyls driven by recent geological events
    Frantz, Laurent A. F.; Rudzinski, Anna; Nugraha, Abang Mansyursyah Surya; Evin, Allowen; Burton, James; Hulme-Beaman, Ardern; Linderholm, Anna; Barnett, Ross; Vega, Rodrigo; Irving-Pease, Evan K.; Haile, James; Allen, Richard; Leus, Kristin; Shephard, Jill; Hillyer, Mia; Gillemot, Sarah; van den Hurk, Jeroen; Ogle, Sharron; Atofanei, Cristina; Thomas, Mark G.; Johansson, Friederike; Mustari, Abdul Haris; Williams, John; Mohamad, Kusdiantoro; Damayanti, Chandramaya Siska; Wiryadi, Ita Djuwita; Obbles, Dagmar; Mona, Stephano; Day, Hally; Yasin, Muhammad; Meker, Stefan; McGuire, Jimmy A.; Evans, Ben J.; von Rintelen, Thomas; Ho, Simon Y. W.; Searle, J. B.; Kitchener, Andrew C.; Macdonald, Alastair A.; Shaw, Darren J.; Hall, Robert; Galbusera, Peter; Larson, Greger (The Royal Society, 2018-04-11)
    The high degree of endemism on Sulawesi has previously been suggested to have vicariant origins, dating back to 40 Ma. Recent studies, however, suggest that much of Sulawesi's fauna assembled over the last 15 Myr. Here, we test the hypothesis that more recent uplift of previously submerged portions of land on Sulawesi promoted diversification and that much of its faunal assemblage is much younger than the island itself. To do so, we combined palaeogeographical reconstructions with genetic and morphometric datasets derived from Sulawesi's three largest mammals: the babirusa, anoa and Sulawesi warty pig. Our results indicate that although these species most likely colonized the area that is now Sulawesi at different times (14 Ma to 2–3 Ma), they experienced an almost synchronous expansion from the central part of the island. Geological reconstructions indicate that this area was above sea level for most of the last 4 Myr, unlike most parts of the island. We conclude that emergence of land on Sulawesi (approx. 1–2 Myr) may have allowed species to expand synchronously. Altogether, our results indicate that the establishment of the highly endemic faunal assemblage on Sulawesi was driven by geological events over the last few million years.
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    R2d2 Drives Selfish Sweeps in the House Mouse
    Didion, John P.; Morgan, Andrew P.; Yadgary, Liran; Bell, Timothy A.; McMullan, Rachel C.; Ortiz de Solorzano, Lydia; Britton-Davidian, Janice; Bult, Carol J.; Campbell, Karl J.; Castiglia, Riccardo; Ching, Yung-Hao; Chunco, Amanda J.; Crowley, James J.; Chesler, Elissa J.; Förster, Daniel W.; French, John E.; Gabriel, Sofia I.; Gatti, Daniel M.; Garland, Theodore; Giagia-Athanasopoulou, Eva B.; Giménez, Mabel D.; Grize, Sofia A.; Gündüz, ?slam; Holmes, Andrew; Hauffe, Heidi C.; Herman, Jeremy S.; Holt, James M.; Hua, Kunjie; Jolley, Wesley J.; Lindholm, Anna K.; López-Fuster, María J.; Mitsainas, George; da Luz Mathias, Maria; McMillan, Leonard; da Graça Morgado Ramalhinho, Maria; Rehermann, Barbara; Rosshart, Stephan P.; Searle, J. B.; Shiao, Meng-Shin; Solano, Emanuela; Svenson, Karen L.; Thomas-Laemont, Patricia; Threadgill, David W.; Ventura, Jacint; Weinstock, George M.; Pomp, Daniel; Churchill, Gary A.; Pardo-Manuel de Villena, Fernando (Oxford University Press on behalf of the Society for Molecular Biology and Evolution, 2016-02-15)
    A selective sweep is the result of strong positive selection driving newly occurring or standing genetic variants to fixation, and can dramatically alter the pattern and distribution of allelic diversity in a population. Population-level sequencing data have enabled discoveries of selective sweeps associated with genes involved in recent adaptations in many species. In contrast, much debate but little evidence addresses whether “selfish” genes are capable of fixation—thereby leaving signatures identical to classical selective sweeps—despite being neutral or deleterious to organismal fitness. We previously described R2d2, a large copy-number variant that causes nonrandom segregation of mouse Chromosome 2 in females due to meiotic drive. Here we show population-genetic data consistent with a selfish sweep driven by alleles of R2d2 with high copy number (R2d2HC) in natural populations. We replicate this finding in multiple closed breeding populations from six outbred backgrounds segregating for R2d2 alleles. We find that R2d2HC rapidly increases in frequency, and in most cases becomes fixed in significantly fewer generations than can be explained by genetic drift. R2d2HC is also associated with significantly reduced litter sizes in heterozygous mothers, making it a true selfish allele. Our data provide direct evidence of populations actively undergoing selfish sweeps, and demonstrate that meiotic drive can rapidly alter the genomic landscape in favor of mutations with neutral or even negative effects on overall Darwinian fitness. Further study will reveal the incidence of selfish sweeps, and will elucidate the relative contributions of selfish genes, adaptation and genetic drift to evolution.
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    Staggered chromosomal hybrid zones in the house mouse: relevance to reticulate evolution and speciation
    Gündüz, ?.; Pollock, C.L.; Giménez, M.D.; Förster, D.W.; White, T.A.; Sans-Fuentes, M.A.; Hauffe, H.C.; Ventura, J.; López-Fuster, M.J.; Searle, J.B. (Multidisciplinary Digital Publishing Insitute (MDPI), 2010-09)
    In the house mouse there are numerous chromosomal races distinguished by different combinations of metacentric chromosomes. These may come into contact with each other and with the ancestral all-acrocentric race, and form hybrid zones. The chromosomal clines that make up these hybrid zones may be coincident or separated from each other (staggered). Such staggered hybrid zones are interesting because they may include populations of individuals homozygous for a mix of features of the hybridizing races. We review the characteristics of four staggered hybrid zones in the house mouse and discuss whether they are examples of primary or secondary contact and whether they represent reticulate evolution or not. However, the most important aspect of staggered hybrid zones is that the homozygous populations within the zones have the potential to expand their distributions and become new races (a process termed 'zonal raciation'). In this way they can add to the total 'stock' of chromosomal races in the species concerned. Speciation is an infrequent phenomenon that may involve an unusual set of circumstances. Each one of the products of zonal raciation has the potential to become a new species and by having more races increases the chance of a speciation event. © 2010 by the authors; licensee MDPI, Basel, Switzerland.
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    Reconstructing Asian faunal introductions to eastern Africa from multi-proxy biomolecular and archaeological datasets
    Prendergast, M.E.; Buckley, M.; Crowther, A.; Eager, H.; Frantz, L.; Lebrasseur, O.; Hutterer, R.; Hulme-Beaman, A.; Van Neer, W.; Douka, K.; Veall, M.-A.; Quintana Morales, E.M.; Schuenemann, V.J.; Reiter, E.; Allen, R.; Helm, R.; Shipton, C.; Mwebi, O.; Denys, C.; Horton, M.; Wynne-Jones, S.; Fleisher, J.; Radimilahy, C.; Wright, H.; Searle, J.B.; Krause, J.; Larson, G.; Boivin, N.L. (Public Library of Science, 2017-08)
    Human-mediated biological exchange has had global social and ecological impacts. In sub-Saharan Africa, several domestic and commensal animals were introduced from Asia in the pre-modern period; however, the timing and nature of these introductions remain contentious. One model supports introduction to the eastern African coast after the mid-first millennium CE, while another posits introduction dating back to 3000 BCE. These distinct scenarios have implications for understanding the emergence of long-distance maritime connectivity, and the ecological and economic impacts of introduced species. Resolution of this longstanding debate requires new efforts, given the lack of well-dated fauna from high-precision excavations, and ambiguous osteomorphological identifications. We analysed fau-nal remains from 22 eastern African sites spanning a wide geographic and chronological range, and applied biomolecular techniques to confirm identifications of two Asian taxa: domestic chicken (Gallus gallus) and black rat (Rattus rattus). Our approach included ancient DNA (aDNA) analysis aided by BLAST-based bioinformatics, Zooarchaeology by Mass Spectrometry (ZooMS) collagen fingerprinting, and direct AMS (accelerator mass spectrometry) radiocarbon dating. Our results support a late, mid-first millennium CE introduction of these species. We discuss the implications of our findings for models of biological exchange, and emphasize the applicability of our approach to tropical areas with poor bone preservation.
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    Playing Hide-and-Seek in Beta-Globin Genes: Gene Conversion Transferring a Beneficial Mutation between Differentially Expressed Gene Duplicates
    Strážnická, Michaela; Marková, Silvia; Searle, J. B.; Kotlík, Petr (Multidisciplinary Digital Publishing Institute (MDPI), 2018-10-12)
    Increasing evidence suggests that adaptation to diverse environments often involves selection on existing variation rather than new mutations. A previous study identified a nonsynonymous single nucleotide polymorphism (SNP) in exon 2 of two paralogous ?-globin genes of the bank vole (Clethrionomys glareolus) in Britain in which the ancestral serine (Ser) and the derived cysteine (Cys) allele represent geographically partitioned functional variation affecting the erythrocyte antioxidative capacity. Here we studied the geographical pattern of the two-locus Ser/Cys polymorphism throughout Europe and tested for the geographic correlation between environmental variables and allele frequency, expected if the polymorphism was under spatially heterogeneous environment-related selection. Although bank vole population history clearly is important in shaping the dispersal of the oxidative stress protective Cys allele, analyses correcting for population structure suggest the Europe-wide pattern is affected by geographical variation in environmental conditions. The ?-globin phenotype is encoded by the major paralog HBB-T1 but we found evidence of bidirectional gene conversion of exon 2 with the low-expression paralog HBB-T2. Our data support the model where gene conversion reshuffling genotypes between high- and low- expressed paralogs enables tuning of erythrocyte thiol levels, which may help maintain intracellular redox balance under fluctuating environmental conditions. Therefore, our study suggests a possible role for gene conversion between differentially expressed gene duplicates as a mechanism of physiological adaptation of populations to new or changing environments.
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    Mapping 3' transcript ends in the bank vole (Clethrionomys glareolus) mitochondrial genome with RNA-Seq
    Marková, S.; Filipi, K.; Searle, J.B.; Kotlík, P. (Springer Nature, 2015-10-26)
    Background: Although posttranscriptional modification of mitochondrial (mt) transcripts plays key roles in completion of the coding information and in the expression of mtDNA-encoded genes, there is little experimental evidence on the polyadenylation status and the location of mt gene poly(A) sites for non-human mammals. Results: Poly(A)-enriched RNA-Seq reads collected for two wild-caught bank voles (Clethrionomys glareolus) were mapped to the complete mitochondrial genome of that species. Transcript polyadenylation was detected as unmapped adenine residues at the ends of the mapped reads. Where the tRNA punctuation model applied, there was the expected polyadenylation, except for the nad5 transcript, whose polyadenylated 3' end is at an intergenic sequence/cytochrome b boundary. As in human, two pairs of bank vole genes, nad4l/nad4 and atp8/atp6, are expressed from bicistronic transcripts. TAA stop codons of four bank vole protein-coding genes (nad1, atp6, cox3 and nad4) are incompletely encoded in the DNA and are completed by polyadenylation. This is three genes (nad2, nad3 and cob) less than in human. The bank vole nad2 gene encodes a full stop codon (TAA in one vole and TAG in the other), which is followed by a 2bp UTR and the gene conforms to the tRNA punctuation model. In contrast, the annotations of the reference mouse and some other rodent mt genomes in GenBank include complete TAG stop codons in both nad1 and nad2, which overlap downstream trnI and trnW, respectively. Thus the RNA-Seq data of bank voles provides a model for stop codons of mt-encoded genes in mammals comparable to humans, but at odds with some of the interpretation based purely on genomic data in mouse and other rodents. Conclusions: This work demonstrates how RNA-Seq data were useful to recover mtDNA transcriptome data in a non-model rodent and to shed more light on mammalian mtDNA transcriptome and post-transcriptional modification. Even though gene content and organisation of mtDNA are strongly conserved among mammals, annotations that neglect the transcriptome may be prone to errors in relation to the stop codons.
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    Over a Thousand Years of Evolutionary History of Domestic Geese from Russian Archaeological Sites, Analysed Using Ancient DNA
    Honka, J.; Heino, M.T.; Kvist, L.; Askeyev, I.V.; Shaymuratova, D.N.; Askeyev, O.V.; Askeyev, A.O.; Heikkinen, M.E.; Searle, J.B.; Aspi, J. (Multidisciplinary Digital Publishing Institute (MDPI), 2018-07-20)
    The European domestic goose is a widely farmed species known to have descended from the wild greylag goose (Anser anser). However, the evolutionary history of this domesticate is still poorly known. Ancient DNA studies have been useful for many species, but there has been little such work on geese. We have studied temporal genetic variation among domestic goose specimens excavated from Russian archaeological sites (4th–18th centuries) using a 204 base pair fragment of the mitochondrial control region. Specimens fell into three different genetic clades: the domestic D-haplogroup, the F-haplogroup that includes both wild and domestic geese, and a clade comprising another species, the taiga bean goose. Most of the subfossil geese carried typical domestic D-haplotypes. The domestication status of the geese carrying F-haplotypes is less certain, as the haplotypes identified were not present among modern domestic geese and could represent wild geese (misclassified as domestics), introgression from wild geese, or local domestication events. The bones of taiga bean goose were most probably misidentified as domestic goose but the domestication of bean goose or hybridization with domestic goose is also possible. Samples from the 4th to 10th century were clearly differentiated from the later time periods due to a haplotype that was found only in this early period, but otherwise no temporal or geographical variation in haplotype frequencies was apparent.
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    Dual mechanism of chromatin remodeling in the common shrew sex trivalent (XY1Y2)
    Matveevsky, S.N.; Pavlova, S.V.; Atsaeva, M.M.; Searle, J.B.; Kolomiets, O.L. (Pensoft Publishers, 2017-11-03)
    Here we focus on the XY1Y2 condition in male common shrew Sorex araneus Linnaeus, 1758, applying electron microscopy and immunocytochemistry for a comprehensive analysis of structure, synapsis and behaviour of the sex trivalent in pachytene spermatocytes. The pachytene sex trivalent consists of three distinct parts: short and long synaptic SC fragments (between the X and Y1 and between the X and Y2, respectively) and a long asynaptic region of the X in-between. Chromatin inactivation was revealed in the XY1 synaptic region, the asynaptic region of the X and a very small asynaptic part of the Y2. This inactive part of the sex trivalent, that we named the 'head', forms a typical sex body and is located at the periphery of the meiotic nucleus at mid pachytene. The second part or 'tail', a long region of synapsis between the X and Y2 chromosomes, is directed from the periphery into the nucleus. Based on the distribution patterns of four proteins involved in chromatin inactivation, we propose a model of meiotic silencing in shrew sex chromosomes. Thus, we conclude that pachytene sex chromosomes are structurally and functionally two different chromatin domains with specific nuclear topology: the peripheral inactivated 'true' sex chromosome regions (part of the X and the Y1) and more centrally located transcriptionally active autosomal segments (part of the X and the Y2).