Neural and ecological basis of pair bonding in butterflyfishes (F: Chaetodontidae)

Nowicki, Jessica Ploetz (2017) Neural and ecological basis of pair bonding in butterflyfishes (F: Chaetodontidae). PhD thesis, James Cook University.

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Abstract

Pair bonding has independently evolved in all major vertebrate lineages, where it represents a major defining feature of species-specific social structure. As such, proximate neural reasons for how, and adaptive reasons for why pair bonding occurs are fairly well established, at least for mammals and birds. In these later vertebrates, particularly mammals, there are four integral neurochemical systems involved: oxytocin, arginine vasotocin, dopamine, and opioid systems. Both oxytocin and arginine vasotocin systems facilitate partner attachment, presumably by mediating social memory. Meanwhile, dopamine and opioid systems appear to facilitate partner attachment by mediating partner reward learning and associated motivation/positive hedonics, respectively. Much less is known about the underlying neural or adaptive basis of pair bonding among reptiles, amphibians, and fishes. This is nonetheless very important, mainly because these lineages possess specific qualities, such as the general lack of bi-parental care, that facilitate improved understanding neurobiological systems that independently underpin pair bonding. Moreover, these lineages provide insight into the early evolution and subsequent evolutionary history of vertebrate pair bonding.

The overall objective of my thesis was to investigate the i) underlying neurobiological basis and ii) ecological benefits of pair bonding in fishes, and specifically, among coral reef butterflyfishes (f: Chaetodontidae). As a first step, I sought to establish a novel butterflyfish model system for conducting integrative, comparative and experimental neural research. By undertaking extensive in situ behavioural observations on wild fishes, I show that pair bonding vs. non-pair bonding sociality varies markedly among adults of Chaetodon lunulatus (84% are pair bonding, whereas 16% are solitary), and among six congeners (84% of C. lunulatus, 78% of C. baronessa, and 71% of C. vagabundus adults are pair bonded, whereas 88% of C. rainfordi, 90% of C. plebeius, and 80% of C. trifascialis adults are solitary). Interestingly, several key attributes, including parental care, do not co-vary with these species differences in sociality. I also show that an ecologically relevant character of Chaetodon pair bonding, namely preferential affiliation with partner, is reliably elicited in C. lunulatus males using the laboratory "two-choice proximity" assay. When given a choice to affiliate with either their partner or a non-partner female conspecific, the majority of males spent on average 54/60min affiliating with their partner, and only 8/60min affiliating with a non-partner female. These findings reaffirm previous assumptions of the sociality of these species, and validate that the proposed butterflyfish systems are amenable for undertaking highly controlled comparative, and reliable experimental research into fish pair boding.

I then used the established C. lunulatus model system for conducting integrative neural research, testing the hypothesis that regulatory neuro-chemical and –anatomical substrates may be similar to the mammalian model, Microtus ochrogaster. Peripheral administration of isotocin (IT, teleost homologue of oxytocin), arginine vasotocin (AVT, teleost homologue of arginine vasopressin) V1a receptor antagonists attenuates partner preference in males, indicating their functional involvement in pair bonding; however, administering dopamine D1 or mu-opioid receptor antagonists has no significant effect. Comparisons of gene expression of ITR, V1aR, D1R, D2R, and MORs within eight brain regions between pair bonded and solitary individuals showed that for females, differences in IT and V1a nonapeptide receptor expression within the lateral septum-like region (the ventral and lateral regions of the ventral telencephalon, Vv/Vl) is associated with differences in pairing phenotype. It further revealed that for both sexes, differences in dopamine D1, D2, and mu-opioid receptor expression within several regions of the mesolimbic reward system, including the striatum-like region (the central nucleus of the ventral telencephalon, Vc), is associated with differences in pairing phenotype.

Finally, to explore the ecological basis of butterflyfish pair bonding, I tested the assisted resource defence hypothesis (ARDH) for pair bonding in two strongly pair bonding Chaetodon species. In situ observations of wild individuals suggest that paired individuals assist their partners while defending feeding territories in a species-specific manner, such that C. lunulatus displays mutual partner assistance, whereas C. baronessa displays male-prioritized partner assistance. In both species, partner assistance appears to confer gains in feeding and energy reserves to partners over their solitary counterparts. Experimentally inducing new partnerships in situ immediately evoked marked declines in relations between partners of the new pair and between the new pair and their neighbouring pairs, leading to severe declines in feeding rate that eventually recovered with subsequent partner fidelity. Taken together, these findings corroborate with previous findings in butterflyfishes, further supporting ARDH for pair bonding in these organisms, and furthermore suggests that partner fidelity is critical for promoting assisted resource defence.

Overall, the results of this thesis demonstrate that in butterflyfishes, nonapeptide, dopamine, and opioid systems acting within specific nodes of the vertebrate social decision making network regulate pair bonding, in order to provide social assistance during defense of food resources. Based on the broader comparison of these results with those of mammals and birds, I furthermore conclude that in at least very selective cases, the convergence of pair bonding across exceptionally wide evolutionary distances is a consequence of pair bonding repeatedly serving an analogous ecological function through the repeated co-option of homologous neural structures. In order to determine the extent to which this has occurred, however, complementary studies in more vertebrates (most urgently amphibians and reptiles) are now needed.

Item ID: 52710
Item Type: Thesis (PhD)
Keywords: butterflyfish; butterflyfishes; Chaetodontidae; coral reef fishes; ecology; fish behavior; fish behavior; monogamy; neural mechanisms; neurobiology; pair bonding; pair bonds
Date Deposited: 28 Feb 2018 01:46
FoR Codes: 06 BIOLOGICAL SCIENCES > 0602 Ecology > 060201 Behavioural Ecology @ 30%
06 BIOLOGICAL SCIENCES > 0602 Ecology > 060205 Marine and Estuarine Ecology (incl Marine Ichthyology) @ 40%
06 BIOLOGICAL SCIENCES > 0603 Evolutionary Biology > 060304 Ethology and Sociobiology @ 30%
SEO Codes: 97 EXPANDING KNOWLEDGE > 970106 Expanding Knowledge in the Biological Sciences @ 100%
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