TY - JOUR
T1 - A Conserved Role for Serotonergic Neurotransmission in Mediating Social Behavior in Octopus
AU - Edsinger, Eric
AU - Dölen, Gül
N1 - Funding Information:
We thank members of the Dölen laboratory, R. Caldwell, M. Kuba, and T. Gutnick for comments, as well as K. Peramba, M. Renard, K. Dever, D. Calzarette, L. Menlow, J. Simmons, J. Marvel-Zuccola, J. Miao, M. Cordeiro, P. Newstein, and T. Sakmar for guidance and assistance in octopus care and D. Mark Welch and M. Sogin for guidance in the phylogenetic analysis. MDMA was a gift of R. Doblin (Multidisciplinary Association for Psychedelic Studies, MAPS). This work was supported by grants from the Kinship Foundation , Hartwell Foundation , and Klingenstein-Simons Foundation (G.D.) and the Vetlesen Foundation (E.E.)
Publisher Copyright:
© 2018 Elsevier Ltd
PY - 2018/10/8
Y1 - 2018/10/8
N2 - Human and octopus lineages are separated by over 500 million years of evolution [1, 2] and show divergent anatomical patterns of brain organization [3, 4]. Despite these differences, growing evidence suggests that ancient neurotransmitter systems are shared across vertebrate and invertebrate species and in many cases enable overlapping functions [5]. Sociality is widespread across the animal kingdom, with numerous examples in both invertebrate (e.g., bees, ants, termites, and shrimps) and vertebrate (e.g., fishes, birds, rodents, and primates) lineages [6]. Serotonin is an evolutionarily ancient molecule [7] that has been implicated in regulating both invertebrate [8] and vertebrate [9] social behaviors, raising the possibility that this neurotransmitter's prosocial functions may be conserved across evolution. Members of the order Octopoda are predominantly asocial and solitary [10]. Although at this time it is unknown whether serotonergic signaling systems are functionally conserved in octopuses, ethological studies indicate that agonistic behaviors are suspended during mating [11–13], suggesting that neural mechanisms subserving social behaviors exist in octopuses but are suppressed outside the reproductive period. Here we provide evidence that, as in humans, the phenethylamine (+/−)-3,4-methylendioxymethamphetamine (MDMA) enhances acute prosocial behaviors in Octopus bimaculoides. This finding is paralleled by the evolutionary conservation of the serotonin transporter (SERT, encoded by the Slc6A4 gene) binding site of MDMA in the O. bimaculoides genome. Taken together, these data provide evidence that the neural mechanisms subserving social behaviors exist in O. bimaculoides and indicate that the role of serotonergic neurotransmission in regulating social behaviors is evolutionarily conserved. Edsinger and Dölen identify clear octopus orthologs of the human serotonin transporter gene, SLC6A4. This finding is paralleled by conservation of the SLC6A4 binding site and acute prosocial functions of MDMA in octopuses. These data provide evidence for the evolutionary conservation of serotonergic signaling in the regulation of social behaviors.
AB - Human and octopus lineages are separated by over 500 million years of evolution [1, 2] and show divergent anatomical patterns of brain organization [3, 4]. Despite these differences, growing evidence suggests that ancient neurotransmitter systems are shared across vertebrate and invertebrate species and in many cases enable overlapping functions [5]. Sociality is widespread across the animal kingdom, with numerous examples in both invertebrate (e.g., bees, ants, termites, and shrimps) and vertebrate (e.g., fishes, birds, rodents, and primates) lineages [6]. Serotonin is an evolutionarily ancient molecule [7] that has been implicated in regulating both invertebrate [8] and vertebrate [9] social behaviors, raising the possibility that this neurotransmitter's prosocial functions may be conserved across evolution. Members of the order Octopoda are predominantly asocial and solitary [10]. Although at this time it is unknown whether serotonergic signaling systems are functionally conserved in octopuses, ethological studies indicate that agonistic behaviors are suspended during mating [11–13], suggesting that neural mechanisms subserving social behaviors exist in octopuses but are suppressed outside the reproductive period. Here we provide evidence that, as in humans, the phenethylamine (+/−)-3,4-methylendioxymethamphetamine (MDMA) enhances acute prosocial behaviors in Octopus bimaculoides. This finding is paralleled by the evolutionary conservation of the serotonin transporter (SERT, encoded by the Slc6A4 gene) binding site of MDMA in the O. bimaculoides genome. Taken together, these data provide evidence that the neural mechanisms subserving social behaviors exist in O. bimaculoides and indicate that the role of serotonergic neurotransmission in regulating social behaviors is evolutionarily conserved. Edsinger and Dölen identify clear octopus orthologs of the human serotonin transporter gene, SLC6A4. This finding is paralleled by conservation of the SLC6A4 binding site and acute prosocial functions of MDMA in octopuses. These data provide evidence for the evolutionary conservation of serotonergic signaling in the regulation of social behaviors.
KW - (+/−)-3,4-methylenedioxymethamphetamine
KW - 5-HT
KW - MDMA
KW - SERT
KW - SLC6A4
KW - evolution
KW - octopus
KW - phenethylamine
KW - serotonin
KW - social
UR - http://www.scopus.com/inward/record.url?scp=85054249526&partnerID=8YFLogxK
UR - http://www.scopus.com/inward/citedby.url?scp=85054249526&partnerID=8YFLogxK
U2 - 10.1016/j.cub.2018.07.061
DO - 10.1016/j.cub.2018.07.061
M3 - Article
C2 - 30245101
AN - SCOPUS:85054249526
SN - 0960-9822
VL - 28
SP - 3136-3142.e4
JO - Current Biology
JF - Current Biology
IS - 19
ER -