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1. Genomic innovations, transcriptional plasticity and gene loss underlying the evolution and divergence of two highly polyphagous and invasive Helicoverpa pest species

Author

Pearce, SL, Clarke, DF, East, PD, Elfekih, S, Gordon, KHJ, Jermiin, LS, McGaughran, A, Oakeshott, JG, Papanikolaou, A, Perera, OP, Rane, RV, Richards, S, Tay, WT, Walsh, TK, Anderson, A, Anderson, CJ, Asgari, S, Board, PG, Bretschneider, A, Campbell, PM, Chertemps, T, Christeller, JT, Coppin, CW, Downes, SJ, Duan, G, Farnsworth, CA, Good, RT, Han, LB, Han, YC, Hatje, K, Horne, I, Huang, YP, Hughes, DST, Jacquin-Joly, E, James, W, Jhangiani, S, Kollmar, M, Kuwar, SS, Li, S, Liu, N-Y, Maibeche, MT, Miller, JR, Montagne, N, Perry, T, Qu, J, Song, SV, Sutton, GG, Vogel, H, Walenz, BP, Xu, W, Zhang, H-J, Zou, Z, Batterham, P, Edwards, OR, Feyereisen, R, Gibbs, RA, Heckel, DG, McGrath, A, Robin, C, Scherer, SE, Worley, KC, Wu, YD, Pearce, SL, Clarke, DF, East, PD, Elfekih, S, Gordon, KHJ, Jermiin, LS, McGaughran, A, Oakeshott, JG, Papanikolaou, A, Perera, OP, Rane, RV, Richards, S, Tay, WT, Walsh, TK, Anderson, A, Anderson, CJ, Asgari, S, Board, PG, Bretschneider, A, Campbell, PM, Chertemps, T, Christeller, JT, Coppin, CW, Downes, SJ, Duan, G, Farnsworth, CA, Good, RT, Han, LB, Han, YC, Hatje, K, Horne, I, Huang, YP, Hughes, DST, Jacquin-Joly, E, James, W, Jhangiani, S, Kollmar, M, Kuwar, SS, Li, S, Liu, N-Y, Maibeche, MT, Miller, JR, Montagne, N, Perry, T, Qu, J, Song, SV, Sutton, GG, Vogel, H, Walenz, BP, Xu, W, Zhang, H-J, Zou, Z, Batterham, P, Edwards, OR, Feyereisen, R, Gibbs, RA, Heckel, DG, McGrath, A, Robin, C, Scherer, SE, Worley, KC, and Wu, YD

Abstract

BACKGROUND: Helicoverpa armigera and Helicoverpa zea are major caterpillar pests of Old and New World agriculture, respectively. Both, particularly H. armigera, are extremely polyphagous, and H. armigera has developed resistance to many insecticides. Here we use comparative genomics, transcriptomics and resequencing to elucidate the genetic basis for their properties as pests. RESULTS: We find that, prior to their divergence about 1.5 Mya, the H. armigera/H. zea lineage had accumulated up to more than 100 more members of specific detoxification and digestion gene families and more than 100 extra gustatory receptor genes, compared to other lepidopterans with narrower host ranges. The two genomes remain very similar in gene content and order, but H. armigera is more polymorphic overall, and H. zea has lost several detoxification genes, as well as about 50 gustatory receptor genes. It also lacks certain genes and alleles conferring insecticide resistance found in H. armigera. Non-synonymous sites in the expanded gene families above are rapidly diverging, both between paralogues and between orthologues in the two species. Whole genome transcriptomic analyses of H. armigera larvae show widely divergent responses to different host plants, including responses among many of the duplicated detoxification and digestion genes. CONCLUSIONS: The extreme polyphagy of the two heliothines is associated with extensive amplification and neofunctionalisation of genes involved in host finding and use, coupled with versatile transcriptional responses on different hosts. H. armigera's invasion of the Americas in recent years means that hybridisation could generate populations that are both locally adapted and insecticide resistant.

Published
2017

2. Genomic innovations, transcriptional plasticity and gene loss underlying the evolution and divergence of two highly polyphagous and invasive Helicoverpa pest species (vol 15, 63, 2017)

Author

Pearce, SL, Clarke, DF, East, PD, Elfekih, S, Gordon, KHJ, Jermiin, LS, McGaughran, A, Oakeshott, JG, Papanicolaou, A, Perera, OP, Rane, RV, Richards, S, Tay, WT, Walsh, TK, Anderson, A, Anderson, CJ, Asgari, S, Board, PG, Bretschneider, A, Campbell, PM, Chertemps, T, Christeller, JT, Coppin, CW, Downes, SJ, Duan, G, Farnsworth, CA, Good, RT, Han, LB, Han, YC, Hatje, K, Horne, I, Huang, YP, Hughes, DST, Jacquin-Joly, E, James, W, Jhangiani, S, Kollmar, M, Kuwar, SS, Li, S, Liu, N-Y, Maibeche, MT, Miller, JR, Montagne, N, Perry, T, Qu, J, Song, SV, Sutton, GG, Vogel, H, Walenz, BP, Xu, W, Zhang, H-J, Zou, Z, Batterham, P, Edwards, OR, Feyereisen, R, Gibbs, RA, Heckel, DG, McGrath, A, Robin, C, Scherer, SE, Worley, KC, Wu, YD, Pearce, SL, Clarke, DF, East, PD, Elfekih, S, Gordon, KHJ, Jermiin, LS, McGaughran, A, Oakeshott, JG, Papanicolaou, A, Perera, OP, Rane, RV, Richards, S, Tay, WT, Walsh, TK, Anderson, A, Anderson, CJ, Asgari, S, Board, PG, Bretschneider, A, Campbell, PM, Chertemps, T, Christeller, JT, Coppin, CW, Downes, SJ, Duan, G, Farnsworth, CA, Good, RT, Han, LB, Han, YC, Hatje, K, Horne, I, Huang, YP, Hughes, DST, Jacquin-Joly, E, James, W, Jhangiani, S, Kollmar, M, Kuwar, SS, Li, S, Liu, N-Y, Maibeche, MT, Miller, JR, Montagne, N, Perry, T, Qu, J, Song, SV, Sutton, GG, Vogel, H, Walenz, BP, Xu, W, Zhang, H-J, Zou, Z, Batterham, P, Edwards, OR, Feyereisen, R, Gibbs, RA, Heckel, DG, McGrath, A, Robin, C, Scherer, SE, Worley, KC, and Wu, YD

Published
2017

3. The genomes of two key bumblebee species with primitive eusocial organization.

Author

Sadd, BM, Barribeau, SM, Bloch, G, de Graaf, DC, Dearden, P, Elsik, CG, Gadau, J, Grimmelikhuijzen, CJP, Hasselmann, M, Lozier, JD, Robertson, HM, Smagghe, G, Stolle, E, Van Vaerenbergh, M, Waterhouse, RM, Bornberg-Bauer, E, Klasberg, S, Bennett, AK, Câmara, F, Guigó, R, Hoff, K, Mariotti, M, Munoz-Torres, M, Murphy, T, Santesmasses, D, Amdam, GV, Beckers, M, Beye, M, Biewer, M, Bitondi, MMG, Blaxter, ML, Bourke, AFG, Brown, MJF, Buechel, SD, Cameron, R, Cappelle, K, Carolan, JC, Christiaens, O, Ciborowski, KL, Clarke, DF, Colgan, TJ, Collins, DH, Cridge, AG, Dalmay, T, Dreier, S, du Plessis, L, Duncan, E, Erler, S, Evans, J, Falcon, T, Flores, K, Freitas, FCP, Fuchikawa, T, Gempe, T, Hartfelder, K, Hauser, F, Helbing, S, Humann, FC, Irvine, F, Jermiin, LS, Johnson, CE, Johnson, RM, Jones, AK, Kadowaki, T, Kidner, JH, Koch, V, Köhler, A, Kraus, FB, Lattorff, HMG, Leask, M, Lockett, GA, Mallon, EB, Antonio, DSM, Marxer, M, Meeus, I, Moritz, RFA, Nair, A, Näpflin, K, Nissen, I, Niu, J, Nunes, FMF, Oakeshott, JG, Osborne, A, Otte, M, Pinheiro, DG, Rossié, N, Rueppell, O, Santos, CG, Schmid-Hempel, R, Schmitt, BD, Schulte, C, Simões, ZLP, Soares, MPM, Swevers, L, Winnebeck, EC, Wolschin, F, Yu, N, Zdobnov, EM, Aqrawi, PK, Blankenburg, KP, Coyle, M, Francisco, L, Hernandez, AG, Holder, M, Hudson, ME, Jackson, L, Jayaseelan, J, Joshi, V, Kovar, C, Lee, SL, Mata, R, Mathew, T, Newsham, IF, Ngo, R, Okwuonu, G, Pham, C, Pu, L-L, Saada, N, Santibanez, J, Simmons, D, Thornton, R, Venkat, A, Walden, KKO, Wu, Y-Q, Debyser, G, Devreese, B, Asher, C, Blommaert, J, Chipman, AD, Chittka, L, Fouks, B, Liu, J, O'Neill, MP, Sumner, S, Puiu, D, Qu, J, Salzberg, SL, Scherer, SE, Muzny, DM, Richards, S, Robinson, GE, Gibbs, RA, Schmid-Hempel, P, Worley, KC, Sadd, BM, Barribeau, SM, Bloch, G, de Graaf, DC, Dearden, P, Elsik, CG, Gadau, J, Grimmelikhuijzen, CJP, Hasselmann, M, Lozier, JD, Robertson, HM, Smagghe, G, Stolle, E, Van Vaerenbergh, M, Waterhouse, RM, Bornberg-Bauer, E, Klasberg, S, Bennett, AK, Câmara, F, Guigó, R, Hoff, K, Mariotti, M, Munoz-Torres, M, Murphy, T, Santesmasses, D, Amdam, GV, Beckers, M, Beye, M, Biewer, M, Bitondi, MMG, Blaxter, ML, Bourke, AFG, Brown, MJF, Buechel, SD, Cameron, R, Cappelle, K, Carolan, JC, Christiaens, O, Ciborowski, KL, Clarke, DF, Colgan, TJ, Collins, DH, Cridge, AG, Dalmay, T, Dreier, S, du Plessis, L, Duncan, E, Erler, S, Evans, J, Falcon, T, Flores, K, Freitas, FCP, Fuchikawa, T, Gempe, T, Hartfelder, K, Hauser, F, Helbing, S, Humann, FC, Irvine, F, Jermiin, LS, Johnson, CE, Johnson, RM, Jones, AK, Kadowaki, T, Kidner, JH, Koch, V, Köhler, A, Kraus, FB, Lattorff, HMG, Leask, M, Lockett, GA, Mallon, EB, Antonio, DSM, Marxer, M, Meeus, I, Moritz, RFA, Nair, A, Näpflin, K, Nissen, I, Niu, J, Nunes, FMF, Oakeshott, JG, Osborne, A, Otte, M, Pinheiro, DG, Rossié, N, Rueppell, O, Santos, CG, Schmid-Hempel, R, Schmitt, BD, Schulte, C, Simões, ZLP, Soares, MPM, Swevers, L, Winnebeck, EC, Wolschin, F, Yu, N, Zdobnov, EM, Aqrawi, PK, Blankenburg, KP, Coyle, M, Francisco, L, Hernandez, AG, Holder, M, Hudson, ME, Jackson, L, Jayaseelan, J, Joshi, V, Kovar, C, Lee, SL, Mata, R, Mathew, T, Newsham, IF, Ngo, R, Okwuonu, G, Pham, C, Pu, L-L, Saada, N, Santibanez, J, Simmons, D, Thornton, R, Venkat, A, Walden, KKO, Wu, Y-Q, Debyser, G, Devreese, B, Asher, C, Blommaert, J, Chipman, AD, Chittka, L, Fouks, B, Liu, J, O'Neill, MP, Sumner, S, Puiu, D, Qu, J, Salzberg, SL, Scherer, SE, Muzny, DM, Richards, S, Robinson, GE, Gibbs, RA, Schmid-Hempel, P, and Worley, KC

Abstract

BACKGROUND: The shift from solitary to social behavior is one of the major evolutionary transitions. Primitively eusocial bumblebees are uniquely placed to illuminate the evolution of highly eusocial insect societies. Bumblebees are also invaluable natural and agricultural pollinators, and there is widespread concern over recent population declines in some species. High-quality genomic data will inform key aspects of bumblebee biology, including susceptibility to implicated population viability threats. RESULTS: We report the high quality draft genome sequences of Bombus terrestris and Bombus impatiens, two ecologically dominant bumblebees and widely utilized study species. Comparing these new genomes to those of the highly eusocial honeybee Apis mellifera and other Hymenoptera, we identify deeply conserved similarities, as well as novelties key to the biology of these organisms. Some honeybee genome features thought to underpin advanced eusociality are also present in bumblebees, indicating an earlier evolution in the bee lineage. Xenobiotic detoxification and immune genes are similarly depauperate in bumblebees and honeybees, and multiple categories of genes linked to social organization, including development and behavior, show high conservation. Key differences identified include a bias in bumblebee chemoreception towards gustation from olfaction, and striking differences in microRNAs, potentially responsible for gene regulation underlying social and other traits. CONCLUSIONS: These two bumblebee genomes provide a foundation for post-genomic research on these key pollinators and insect societies. Overall, gene repertoires suggest that the route to advanced eusociality in bees was mediated by many small changes in many genes and processes, and not by notable expansion or depauperation.

Published
2015

4. The genomes of two key bumblebee species with primitive eusocial organization

Author

Sadd, BM, Barribeau, SM, Bloch, G, de Graaf, DC, Dearden, P, Elsik, CG, Gadau, J, Grimmelikhuijzen, CJP, Hasselmann, M, Lozier, JD, Robertson, HM, Smagghe, G, Stolle, E, Van Vaerenbergh, M, Waterhouse, RM, Bornberg-Bauer, E, Klasberg, S, Bennett, AK, Camara, F, Guigo, R, Hoff, K, Mariotti, M, Munoz-Torres, M, Murphy, T, Santesmasses, D, Amdam, GV, Beckers, M, Beye, M, Biewer, M, Bitondi, MMG, Blaxter, ML, Bourke, AFG, Brown, MJF, Buechel, SD, Cameron, R, Cappelle, K, Carolan, JC, Christiaens, O, Ciborowski, KL, Clarke, DF, Colgan, TJ, Collins, DH, Cridge, AG, Dalmay, T, Dreier, S, du Plessis, L, Duncan, E, Erler, S, Evans, J, Falcon, T, Flores, K, Freitas, FCP, Fuchikawa, T, Gempe, T, Hartfelder, K, Hauser, F, Helbing, S, Humann, FC, Irvine, F, Jermiin, LS, Johnson, CE, Johnson, RM, Jones, A, Kadowaki, T, Kidner, JH, Koch, V, Kohler, A, Kraus, FB, Lattorff, HMG, Leask, M, Lockett, GA, Mallon, EB, Marco Antonio, DS, Marxer, M, Meeus, I, Moritz, RFA, Nair, A, Napflin, K, Nissen, I, Niu, J, Nunes, FMF, Oakeshott, JG, Osborne, A, Otte, M, Pinheiro, DG, Rossie, N, Rueppell, O, Santos, CG, Schmid-Hempel, R, Schmitt, BD, Schulte, C, Simoes, ZLP, Soares, MPM, Swevers, L, Winnebeck, EC, Wolschin, F, Yu, N, Zdobnov, EM, Aqrawi, PK, Blankenburg, KP, Coyle, M, Francisco, L, Hernandez, AG, Holder, M, Hudson, ME, Jackson, L, Jayaseelan, J, Joshi, V, Kovar, C, Lee, SL, Mata, R, Mathew, T, Newsham, IF, Ngo, R, Okwuonu, G, Pham, C, Pu, L, Saada, N, Santibanez, J, Simmons, D, Thornton, R, Venkat, A, Walden, KKO, Wu, Y, Debyser, G, Devreese, B, Asher, C, Blommaert, J, Chipman, AD, Chittka, L, Fouks, B, Liu, J, O'Neill, MP, Sumner, S, Puiu, D, Qu, J, Salzberg, SL, Scherer, SE, Muzny, DM, Richards, S, Robinson, GE, Gibbs, RA, Schmid-Hempel, P, Worley, KC, Sadd, BM, Barribeau, SM, Bloch, G, de Graaf, DC, Dearden, P, Elsik, CG, Gadau, J, Grimmelikhuijzen, CJP, Hasselmann, M, Lozier, JD, Robertson, HM, Smagghe, G, Stolle, E, Van Vaerenbergh, M, Waterhouse, RM, Bornberg-Bauer, E, Klasberg, S, Bennett, AK, Camara, F, Guigo, R, Hoff, K, Mariotti, M, Munoz-Torres, M, Murphy, T, Santesmasses, D, Amdam, GV, Beckers, M, Beye, M, Biewer, M, Bitondi, MMG, Blaxter, ML, Bourke, AFG, Brown, MJF, Buechel, SD, Cameron, R, Cappelle, K, Carolan, JC, Christiaens, O, Ciborowski, KL, Clarke, DF, Colgan, TJ, Collins, DH, Cridge, AG, Dalmay, T, Dreier, S, du Plessis, L, Duncan, E, Erler, S, Evans, J, Falcon, T, Flores, K, Freitas, FCP, Fuchikawa, T, Gempe, T, Hartfelder, K, Hauser, F, Helbing, S, Humann, FC, Irvine, F, Jermiin, LS, Johnson, CE, Johnson, RM, Jones, A, Kadowaki, T, Kidner, JH, Koch, V, Kohler, A, Kraus, FB, Lattorff, HMG, Leask, M, Lockett, GA, Mallon, EB, Marco Antonio, DS, Marxer, M, Meeus, I, Moritz, RFA, Nair, A, Napflin, K, Nissen, I, Niu, J, Nunes, FMF, Oakeshott, JG, Osborne, A, Otte, M, Pinheiro, DG, Rossie, N, Rueppell, O, Santos, CG, Schmid-Hempel, R, Schmitt, BD, Schulte, C, Simoes, ZLP, Soares, MPM, Swevers, L, Winnebeck, EC, Wolschin, F, Yu, N, Zdobnov, EM, Aqrawi, PK, Blankenburg, KP, Coyle, M, Francisco, L, Hernandez, AG, Holder, M, Hudson, ME, Jackson, L, Jayaseelan, J, Joshi, V, Kovar, C, Lee, SL, Mata, R, Mathew, T, Newsham, IF, Ngo, R, Okwuonu, G, Pham, C, Pu, L, Saada, N, Santibanez, J, Simmons, D, Thornton, R, Venkat, A, Walden, KKO, Wu, Y, Debyser, G, Devreese, B, Asher, C, Blommaert, J, Chipman, AD, Chittka, L, Fouks, B, Liu, J, O'Neill, MP, Sumner, S, Puiu, D, Qu, J, Salzberg, SL, Scherer, SE, Muzny, DM, Richards, S, Robinson, GE, Gibbs, RA, Schmid-Hempel, P, and Worley, KC

Abstract

Background The shift from solitary to social behavior is one of the major evolutionary transitions. Primitively eusocial bumblebees are uniquely placed to illuminate the evolution of highly eusocial insect societies. Bumblebees are also invaluable natural and agricultural pollinators, and there is widespread concern over recent population declines in some species. High-quality genomic data will inform key aspects of bumblebee biology, including susceptibility to implicated population viability threats. Results We report the high quality draft genome sequences of Bombus terrestris and Bombus impatiens, two ecologically dominant bumblebees and widely utilized study species. Comparing these new genomes to those of the highly eusocial honeybee Apis mellifera and other Hymenoptera, we identify deeply conserved similarities, as well as novelties key to the biology of these organisms. Some honeybee genome features thought to underpin advanced eusociality are also present in bumblebees, indicating an earlier evolution in the bee lineage. Xenobiotic detoxification and immune genes are similarly depauperate in bumblebees and honeybees, and multiple categories of genes linked to social organization, including development and behavior, show high conservation. Key differences identified include a bias in bumblebee chemoreception towards gustation from olfaction, and striking differences in microRNAs, potentially responsible for gene regulation underlying social and other traits. Conclusions These two bumblebee genomes provide a foundation for post-genomic research on these key pollinators and insect societies. Overall, gene repertoires suggest that the route to advanced eusociality in bees was mediated by many small changes in many genes and processes, and not by notable expansion or depauperation

Published
2015

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