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Transcriptomic characterization of the immunogenetic repertoires of heteromyid rodents.

Marra NJ, DeWoody JA - BMC Genomics (2014)

Bottom Line: Gene ontology terms including "immune response" were associated with 31 (4.9%) of the 632 upregulated genes.Our data indicate there are significant differences in the expression of genes among the spleen transcriptomes of these species and that a number of these differentially expressed genes do not show the same pattern of differential expression in another tissue type.This points to the possibility of expression differences between these species specific to the spleen transcriptome.

View Article: PubMed Central - PubMed

Affiliation: Department of Population Medicine and Diagnostic Sciences, Cornell University, S3-111 Schurman Hall, Tower Road, Ithaca, NY 14853, USA. njm77@cornell.edu.

ABSTRACT

Background: When populations evolve under disparate environmental conditions, they experience different selective pressures that shape patterns of sequence evolution and gene expression. These may be manifested in genetic and phenotypic differences such as a diverse immunogenetic repertoire in species from tropical latitudes that have greater and/or different parasite burdens than more temperate species. To test this idea, we compared the transcriptomes of one tropical species (Heteromys desmarestianus) and two species from temperate latitudes (Dipodomys spectabilis and Chaetodipus baileyi) from the Heteromyidae. We did so in a search for positive selection on sequences and/or differential expression, while controlling for phylogenetic history in our choice of species.

Results: We identified 127,812 contigs and annotated 34,878 of these, identifying immune genes associated with interleukins, cytokines, and the production of mast cells. We identified 632 genes that were upregulated in H. desmarestianus (8.7% of genes tested) and 492 (6.7%) that were downregulated. Gene ontology terms including "immune response" were associated with 31 (4.9%) of the 632 upregulated genes. We found preliminary evidence for positive selection on three genes (Palmitoyltransferase ZDHHC5 Ubiquitin-conjugating enzyme E2 N, Krueppel-like factor 10, and Spindle and kinetochore-associated protein 1) along the H. desmarestianus lineage.

Conclusions: Overall our findings pinpoint genes in species from disparate environments that are on different evolutionary trajectories in terms of expression levels and/or nucleotide sequence. Our data indicate there are significant differences in the expression of genes among the spleen transcriptomes of these species and that a number of these differentially expressed genes do not show the same pattern of differential expression in another tissue type. This points to the possibility of expression differences between these species specific to the spleen transcriptome.

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Distribution and sampling locations ofChaetodipus baileyi, Dipodomys spectabilis, and Heteromys desmarestianus. Range map of North America displaying habitat and latitude for all three study species constructed on Arc-GIS. Areas occupied by C. baileyi are highlighted by horizontal lines, areas occupied by D. spectabilis are denoted by vertical lines, and the range of H. desmarestianus is denoted by diagonal lines. Overlap between C. baileyi and D. spectabilis is cross hatched. The white star denotes the sampling location of H. desmarestianus at La Selva Biological Station, Costa Rica whereas the white circle marks the sampling location for C. baileyi and D. spectabilis at Portal, AZ, USA, Species range data were obtained from IUCN Red List of Threatened Species. Version 2013.1. [24]. Habitat data is from [25].
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Fig1: Distribution and sampling locations ofChaetodipus baileyi, Dipodomys spectabilis, and Heteromys desmarestianus. Range map of North America displaying habitat and latitude for all three study species constructed on Arc-GIS. Areas occupied by C. baileyi are highlighted by horizontal lines, areas occupied by D. spectabilis are denoted by vertical lines, and the range of H. desmarestianus is denoted by diagonal lines. Overlap between C. baileyi and D. spectabilis is cross hatched. The white star denotes the sampling location of H. desmarestianus at La Selva Biological Station, Costa Rica whereas the white circle marks the sampling location for C. baileyi and D. spectabilis at Portal, AZ, USA, Species range data were obtained from IUCN Red List of Threatened Species. Version 2013.1. [24]. Habitat data is from [25].

Mentions: All three of our study species are members of the Heteromyidae, a family of new world rodents whose native range extends from North America through Central America and into northern South America [19, 20] (see FigureĀ 1). This family is comprised of three subfamilies which diverged from one another roughly 22 mya [21]: the Heteromyinae, Perognathinae, and the Dipodomyinae (represented in our study by H. desmarestianus, C. baileyi, and D. spectabilis, respectively). Heteromys spp. have the most tropical latitudinal distribution of the family and are often found in lowland rainforest whereas Chaetodipus spp. and Dipodomys spp. generally have temperate desert distributions [19, 20, 22]. The historical biogeography of the species used in this study has not been described in detail, but Miocene fossils of the Perognathinae and Dipodomyinae ancestors have been found in the southwestern US and northern Mexico. These regions developed into arid deserts during the Pleistocene (historical biogeography of the Heteromyidae reviewed in [20]). No fossil record exists for Heteromys in Central America, but members of the genus are thought to have inhabited Central America prior to expanding into portions of northern South America as early as 3 mya [20, 23]. This history points to the long-term presence of these species in temperate and tropical latitudes, respectively.Figure 1


Transcriptomic characterization of the immunogenetic repertoires of heteromyid rodents.

Marra NJ, DeWoody JA - BMC Genomics (2014)

Distribution and sampling locations ofChaetodipus baileyi, Dipodomys spectabilis, and Heteromys desmarestianus. Range map of North America displaying habitat and latitude for all three study species constructed on Arc-GIS. Areas occupied by C. baileyi are highlighted by horizontal lines, areas occupied by D. spectabilis are denoted by vertical lines, and the range of H. desmarestianus is denoted by diagonal lines. Overlap between C. baileyi and D. spectabilis is cross hatched. The white star denotes the sampling location of H. desmarestianus at La Selva Biological Station, Costa Rica whereas the white circle marks the sampling location for C. baileyi and D. spectabilis at Portal, AZ, USA, Species range data were obtained from IUCN Red List of Threatened Species. Version 2013.1. [24]. Habitat data is from [25].
© Copyright Policy - open-access
Related In: Results  -  Collection

License 1 - License 2
Show All Figures
getmorefigures.php?uid=PMC4216838&req=5

Fig1: Distribution and sampling locations ofChaetodipus baileyi, Dipodomys spectabilis, and Heteromys desmarestianus. Range map of North America displaying habitat and latitude for all three study species constructed on Arc-GIS. Areas occupied by C. baileyi are highlighted by horizontal lines, areas occupied by D. spectabilis are denoted by vertical lines, and the range of H. desmarestianus is denoted by diagonal lines. Overlap between C. baileyi and D. spectabilis is cross hatched. The white star denotes the sampling location of H. desmarestianus at La Selva Biological Station, Costa Rica whereas the white circle marks the sampling location for C. baileyi and D. spectabilis at Portal, AZ, USA, Species range data were obtained from IUCN Red List of Threatened Species. Version 2013.1. [24]. Habitat data is from [25].
Mentions: All three of our study species are members of the Heteromyidae, a family of new world rodents whose native range extends from North America through Central America and into northern South America [19, 20] (see FigureĀ 1). This family is comprised of three subfamilies which diverged from one another roughly 22 mya [21]: the Heteromyinae, Perognathinae, and the Dipodomyinae (represented in our study by H. desmarestianus, C. baileyi, and D. spectabilis, respectively). Heteromys spp. have the most tropical latitudinal distribution of the family and are often found in lowland rainforest whereas Chaetodipus spp. and Dipodomys spp. generally have temperate desert distributions [19, 20, 22]. The historical biogeography of the species used in this study has not been described in detail, but Miocene fossils of the Perognathinae and Dipodomyinae ancestors have been found in the southwestern US and northern Mexico. These regions developed into arid deserts during the Pleistocene (historical biogeography of the Heteromyidae reviewed in [20]). No fossil record exists for Heteromys in Central America, but members of the genus are thought to have inhabited Central America prior to expanding into portions of northern South America as early as 3 mya [20, 23]. This history points to the long-term presence of these species in temperate and tropical latitudes, respectively.Figure 1

Bottom Line: Gene ontology terms including "immune response" were associated with 31 (4.9%) of the 632 upregulated genes.Our data indicate there are significant differences in the expression of genes among the spleen transcriptomes of these species and that a number of these differentially expressed genes do not show the same pattern of differential expression in another tissue type.This points to the possibility of expression differences between these species specific to the spleen transcriptome.

View Article: PubMed Central - PubMed

Affiliation: Department of Population Medicine and Diagnostic Sciences, Cornell University, S3-111 Schurman Hall, Tower Road, Ithaca, NY 14853, USA. njm77@cornell.edu.

ABSTRACT

Background: When populations evolve under disparate environmental conditions, they experience different selective pressures that shape patterns of sequence evolution and gene expression. These may be manifested in genetic and phenotypic differences such as a diverse immunogenetic repertoire in species from tropical latitudes that have greater and/or different parasite burdens than more temperate species. To test this idea, we compared the transcriptomes of one tropical species (Heteromys desmarestianus) and two species from temperate latitudes (Dipodomys spectabilis and Chaetodipus baileyi) from the Heteromyidae. We did so in a search for positive selection on sequences and/or differential expression, while controlling for phylogenetic history in our choice of species.

Results: We identified 127,812 contigs and annotated 34,878 of these, identifying immune genes associated with interleukins, cytokines, and the production of mast cells. We identified 632 genes that were upregulated in H. desmarestianus (8.7% of genes tested) and 492 (6.7%) that were downregulated. Gene ontology terms including "immune response" were associated with 31 (4.9%) of the 632 upregulated genes. We found preliminary evidence for positive selection on three genes (Palmitoyltransferase ZDHHC5 Ubiquitin-conjugating enzyme E2 N, Krueppel-like factor 10, and Spindle and kinetochore-associated protein 1) along the H. desmarestianus lineage.

Conclusions: Overall our findings pinpoint genes in species from disparate environments that are on different evolutionary trajectories in terms of expression levels and/or nucleotide sequence. Our data indicate there are significant differences in the expression of genes among the spleen transcriptomes of these species and that a number of these differentially expressed genes do not show the same pattern of differential expression in another tissue type. This points to the possibility of expression differences between these species specific to the spleen transcriptome.

Show MeSH