Candidate genes for individual recognition in Polistes fuscatus paper wasps

Zeitschrift für vergleichende Physiologie - Tập 202 - Trang 115-129 - 2015
A. J. Berens1,2, E. A. Tibbetts3, A. L. Toth1,2,4
1Program in Bioinformatics and Computational Biology, Iowa State University, Ames, USA
2Department of Ecology, Evolution, and Organismal Biology, Iowa State University, Ames, USA
3Department of Ecology and Evolutionary Biology, University of Michigan, Ann Arbor, USA
4Department of Entomology, Iowa State University, Ames, USA;

Tóm tắt

Few animals are known to individually recognize conspecifics, i.e. learn and recall unique individuals during subsequent encounters, and nearly all are social vertebrates. Remarkably, the social paper wasp Polistes fuscatus has recently been discovered to possess this ability, which is useful for remembering identities during competitive social interactions. We analyzed brain gene expression in staged encounters between pairs of individuals to explore potential mechanisms underlying wasps’ ability to recall familiar individuals using real-time qRT-PCR. We identified four candidate genes (IP3K, IP3R, Nckx30C and Su(var)2-10) that were down-regulated in the presence of familiar individuals compared to single wasps and pairs of wasps meeting for the first time. These candidate genes are related to calcium signaling, therefore, we treated wasps with lithium chloride, a pharmacological agent that inhibits calcium signaling in neurons. This treatment decreased aggression in paper wasps, but did not affect expression of genes related to calcium signaling. The results suggest calcium signaling differences may be related to individual memory recall in wasps, and we present four promising candidate genes for future study. These data suggest genes associated with dominance behavior may be co-opted for individual recognition, but further work is needed to establish a causal association with the behavior.

Tài liệu tham khảo

Barron AB, Maleszka J, Vander Meer RK, Robinson GE, Maleszka R (2007) Comparing injection, feeding and topical application methods for treatment of honeybees with octopamine. J Insect Physiol 53:187–194 Berens AJ, Hunt JH, Toth AL (2015) Comparative transcriptomics of convergent evolution: different genes but conserved pathways underlie caste phenotypes across lineages of eusocial insects. Mol Biol Evol 32:690–703 Berridge MJ (1993) Inositol trisphosphate and calcium signaling. Nature 361:315–325. doi:10.1038/361315a0 Boeckle M, Bugnyar T (2012) Long-term memory for affiliates in ravens. Curr Biol 22:801–806. doi:10.1016/j.cub.2012.03.023 Bolduc FV, Bell K, Cox H, Broadie KS, Tully T (2008) Excess protein synthesis in Drosophila fragile × mutants impairs long-term memory. Nat Neurosci 11:1143–1145. doi:10.1038/Nn.2175 Bond AB, Kamil AC, Balda RP (2003) Social complexity and transitive inference in corvids. Anim Behav 65:479–487. doi:10.1006/anbe.2003.2101 Boughman JW, Moss CF (2003) Social sounds: vocal learning and development of mammal and bird calls. In: Simmons AM, Popper AN, Fay RR (eds) Springer handbook of auditory research, vol 16., Acoustic Communication Springer, New York, pp 138–224 Boysen ST, Berntson GG (1989) Conspecific recognition in the chimpanzee (Pan troglodytes)—cardiac responses to significant others. J Comp Psychol 103:215–220. doi:10.1037//0735-7036.103.3.215 Brennan PA, Kendrick KM (2006) Mammalian social odours: attraction and individual recognition. Philos Trans R Soc B 361:2061–2078. doi:10.1098/rstb.2006.1931 Bruck JN (2013) Decades-long social memory in bottlenose dolphins. Proc R Soc B 280:20131726. doi:10.1098/rspb.2013.1726 Byrne RW, Whiten A (1988) Machiavellian intelligence: social expertise and the evolution of intellect in monkeys, apes, and humans. Oxford science publications, Clarendon Press, Oxford Chen CC et al (2012) Visualizing long-term memory formation in two neurons of the Drosophila brain. Science 335:678–685. doi:10.1126/science.1212735 Chorna T, Hasan G (2012) The genetics of calcium signaling in Drosophila melanogaster. Biochim Biophys Acta Gen Subj 1820:1269–1282. doi:10.1016/j.bbagen.2011.11.002 Daugherty THF, Toth AL, Robinson GE (2011) Nutrition and division of labor: effects on foraging and brain gene expression in the paper wasp Polistes metricus. Mol Ecol 20:5337–5347. doi:10.1111/j.1365-294X.2011.05344.x D’Ettorre P, Heinze J (2005) Individual recognition in ant queens. Curr Biol 15:2170–2174. doi:10.1016/j.cub.2005.10.067 Dreier S, D’Ettorre P (2009) Social context predicts recognition systems in ant queens. J Evol Biol 22:644–649. doi:10.1111/j.1420-9101.2008.01668.x Dreier S, van Zweden JS, D’Ettorre P (2007) Long-term memory of individual identity in ant queens. Biol Lett (London) 3:459–462. doi:10.1098/rsb1.2007.0224 Dubnau J et al (2003) The staufen/pumilio pathway is involved in Drosophila long-term memory. Curr Biol 13:286–296 Ellen CW, Mercer AR (2012) Modulatory actions of dopamine and serotonin on insect antennal lobe neurons: insights from studies in vitro. J Mol Histol 43:401–404. doi:10.1007/s10735-012-9401-7 Ferreira PG, Patalano S, Chauhan R, Ffrench-Constant R, Gabaldon T, Guigo R, Sumner S (2013) Transcriptome analyses of primitively eusocial wasps reveal novel insights into the evolution of sociality and the origin of alternative phenotypes. Genome Biol. doi:10.1186/Gb-2013-14-2-R20 Fitch WT, Hauser MD (2003) Unpacking “honesty”: vertebrate vocal production and the evolution of acoustic signals. In: Simmons AM, Popper AN, Fay RR (eds) Springer handbook of auditory research, vol 16., Acoustic communication Springer, New York, pp 65–137 Ge XC et al (2004) Notch signaling in Drosophila long-term memory formation. P Natl Acad Sci USA 101:10172-10176 Godard R (1991) Long-term-memory of individual neighbors in a migratory songbird. Nature 350:228–229. doi:10.1038/350228a0 Gouzoules S (1984) Primate mating systems, kin associations, and cooperative behavior—evidence for kin recognition. Am J Phys Anthropol 27:99–134 Haug-Collet K, Pearson B, Webel R, Szerencsei RT, Winkfein RJ, Schnetkamp PP, Colley NJ (1999) Cloning and characterization of a potassium-dependent sodium/calcium exchanger in Drosophila. J Cell Biol 147:659–670 Hölldobler B, Wilson EO (1990) Host tree selection by the neotropical ant Paraponera clavata (hymenoptera, formicidae). Biotropica 22:213–214. doi:10.2307/2388416 Humphrey NK (1976) The social function of intellect. In: Bateson PPG, Hinde RA, St. John’s College (University of Cambridge), King’s College (University of Cambridge) (eds) Growing points in ethology: based on a conference sponsored by St. John’s College and King’s College, Cambridge. Cambridge University Press, Cambridge Eng., New York, pp 303–317 Injaian A, Tibbetts EA (2014) Cognition across castes: individual recognition in worker Polistes fuscatus wasps. Anim Behav 87:91–96. doi:10.1016/j.anbehav.2013.10.014 Jandt JM, Thomson JL, Geffre AC, Toth AL (2015) Lab rearing environment perturbs social traits: a case study with Polistes wasps. Behav Ecol Sociobiol. doi:10.1093/beheco/arv082 Jolly A (1966) Lemur social behavior and primate intelligence—step from prosimian to monkey intelligence probably took place in a social context. Science 153:501–506. doi:10.1126/science.153.3735.501 Komdeur J, Hatchwell BJ (1999) Kin recognition: function and mechanism in avian societies. Trends Ecol Evol 14:237–241. doi:10.1016/S0169-5347(98)01573-0 Leopold DA, Rhodes G (2010) A comparative view of face perception. J Comp Psychol 124:233–251. doi:10.1037/A0019460 Mateo JM (2006) The nature and representation of individual recognition odours in belding’s ground squirrels. Anim Behav 71:141–154. doi:10.1016/j.anbehav.2005.04.006 Matsuno M, Horiuchi J, Tully T, Saitoe M (2009) The Drosophila cell adnesion molecule klingon is required for long-term memory formation and is regulated by notch. P Natl Acad Sci USA 106:310–315 Matthews S, Snowdon CT (2011) Long-term memory for calls of relatives in cotton-top tamarins (Saguinus oedipus). J Comp Psychol 125:366–369. doi:10.1037/A0023149 McBride SMJ et al (2005) Pharmacological rescue of synaptic plasticity, courtship behavior, and mushroom body defects in a Drosophila model of fragile x syndrome. Neuron 45:753–764. doi:10.1016/j.neuron.2005.01.038 McBride SMJ et al (2010) Pharmacological and genetic reversal of age-dependent cognitive deficits attributable to decreased presenilin function. J Neurosci 30:9510–9522. doi:10.1523/Jneurosci.1017-10.2010 McComb K, Moss C, Sayialel S, Baker L (2000) Unusually extensive networks of vocal recognition in African elephants. Anim Behav 59:1103–1109. doi:10.1006/anbe.2000.1406 Miyashita T, Oda Y, Horiuchi J, Yin JCP, Morimoto T, Saitoe M (2012) Mg2+ block of Drosophila nmda receptors is eequired for long-term memory formation and creb-dependent gene expression. Neuron 74:887–898. doi:10.1016/j.neuron.2012.03.039 Murai C, Tanaka M, Tomonaga M, Sakagami M (2011) Long-term visual recognition of familiar persons, peers, and places by young monkeys (Macaca fuscata). Dev Psychobiol 53:732–737. doi:10.1002/Dev.20548 Ng FS, Tangredi MM, Jackson FR (2011) Glial cells physiologically modulate clock neurons and circadian behavior in a calcium-dependent manner. Curr Biol 21:625–634. doi:10.1016/j.cub.2011.03.027 Pan L, Woodruff E, Liang P, Broadie K (2008) Mechanistic relationships between Drosophila fragile × mental retardation protein and metabotropic glutamate receptor a signaling. Mol Cell Neurosci 37:747–760. doi:10.1016/j.mcn.2008.01.003 Perisse E, Raymond-Delpech V, Neant I, Matsumoto Y, Leclerc C, Moreau M, Sandoz JC (2009) Early calcium increase triggers the formation of olfactory long-term memory in honeybees. BMC Biol 7:30. doi:10.1186/1741-7007-7-30 Pusey A, Wolf M (1996) Inbreeding avoidance in animals. Trends Ecol Evol 11:201–206. doi:10.1016/0169-5347(96)10028-8 Qin H, Dubnau J (2010) Genetic disruptions of Drosophila pavlovian learning leave extinction learning intact. Genes Brain Behav 9:203–212. doi:10.1111/j.1601-183X.2009.00548.x Rand MD, Grimm M, Artavanis-Tsakonas S, Patriub V, Blacklow SC, Sklar J, Aster JC (2000) Calcium depletion dissociates and activates heterodimeric notch receptors. Mol Cell Biol 20:1825–1835 Rasmussen LEL (1995) Evidence for long-term chemical memory in elephants. Chem Senses 20:237 Reeve HK (1991) Polistes. In: Ross KG, Matthews RW (eds) The Social biology of wasps, 1st edn. Comstock Pub. Associates, Ithaca, pp 99–148 Rimmele U, Hediger K, Heinrichs M, Klaver P (2009) Oxytocin makes a face in memory familiar. J Neurosci 29:38–42. doi:10.1523/Jneurosci.4260-08.2009 Ross HE, Young LJ (2009) Oxytocin and the neural mechanisms regulating social cognition and affiliative behavior. Front Neuroendocrin 30:534–547. doi:10.1016/j.yfrne.2009.05.004 Sayigh LS, Tyack PL, Wells RS, Solow AR, Scott MD, Irvine AB (1999) Individual recognition in wild bottlenose dolphins: a field test using playback experiments. Anim Behav 57:41–50. doi:10.1006/anbe.1998.0961 Schoenfeld BP et al (2013) The Drosophila dmglura is required for social interaction and memory. Front Pharmacol. doi:10.3389/Fphar.2013.00064 Sheehan MJ, Tibbetts EA (2008) Robust long-term social memories in a paper wasp. Curr Biol 18:R851–R852. doi:10.1016/j.cub.2008.07.032 Sheehan MJ, Tibbetts EA (2010) Selection for individual recognition and the evolution of polymorphic identity signals in Polistes paper wasps. J Evol Biol 23:570–577. doi:10.1111/j.1420-9101.2009.01923.x Sheehan MJ, Tibbetts EA (2011) Specialized face learning is associated with individual recognition in paper wasps. Science 334:1272–1275. doi:10.1126/science.1211334 Skuse DH et al (2014) Common polymorphism in the oxytocin receptor gene (oxtr) is associated with human social recognition skills. Proc Natl Acad Sci USA 111:1987–1992. doi:10.1073/pnas.1302985111 Smuts BB (1987) Primate societies. University of Chicago Press, Chicago Sofola O et al (2010) Inhibition of gsk-3 ameliorates a beta pathology in an adult-onset Drosophila model of Alzheimer’s disease. PLoS Genet. doi:10.1371/journal.pgen.1001087 Sofola-Adesakin O et al (2014) Lithium suppresses a beta pathology by inhibiting translation in an adult Drosophila model of Alzheimer’s disease. Front Aging Neurosci. doi:10.3389/Fnagi.2014.00190 Tibbetts EA (2002) Visual signals of individual identity in the wasp Polistes fuscatus. Proc R Soc Lond Ser B 269:1423–1428. doi:10.1098/rspb.2002.2031 Tibbetts EA (2004) Complex social behaviour can select for variability in visual features: a case study in Polistes wasps. Proc R Soc Lond Ser B 271:1955–1960. doi:10.1098/rspb.2004.2784 Tibbetts EA, Dale J (2004) A socially enforced signal of quality in a paper wasp. Nature 432:218–222. doi:10.1038/Nature02949 Tibbetts EA, Dale J (2007) Individual recognition: it is good to be different. Trends Ecol Evol 22:529–537. doi:10.1016/j.tree.2007.09.001 Tibbetts EA, Sheehan MJ (2013) Individual recognition and the evolution of learning and memory in Polistes paper wasps. In: Menzel R, Benjamin PR (eds) Invertebrate learning and memory, vol 22. Academic Press, New York, pp 561–571 Toth AL et al (2007) Wasp gene expression supports an evolutionary link between maternal behavior and eusociality. Science 318:441–444. doi:10.1126/science.1146647 Toth AL, Tooker JF, Radhakrishnan S, Minard R, Henshaw MT, Grozinger CM (2014) Shared genes related to aggression, rather than chemical communication, are associated with reproductive dominance in paper wasps (Polistes metricus). BMC Genom 15:75. doi:10.1186/1471-2164-15-75 Wallace J (2014) Calcium dysregulation, and lithium treatment to forestall Alzheimer’s disease—a merging of hypotheses. Cell Calcium 55:175–181. doi:10.1016/j.ceca.2014.02.005 Webel R, Huag-Collet K, Pearson B, Szerencsei RT, Winkfein RJ, Schnetkamp PPM, Colley NJ (2002) Potassium-dependent sodium-calcium exchange through the eye of the fly. Ann Ny Acad Sci 976:300–314 Wilson EO (1971) The insect societies. Belknap Press of Harvard University Press, Cambridge, MA Wu CL et al (2007) Specific requirement of nmda receptors for long-term memory consolidation in Drosophila ellipsoid body. Nat Neurosci 10(12):1578-1586 Xia SZ et al (2005) NMDA receptors mediate olfactory learning and memory in Drosophila. Curr Biol 15:603–615. doi:10.1016/j.cub.2005.02.059 Zhang JB, Little CJ, Tremmel DM, Yin JCP, Wesley CS (2013) Notch-inducible hyperphosphorylated creb and its ultradian oscillation in long-term memory formation. J Neurosci 33:12825-12834