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The role of juvenile hormone in regulating reproductive physiology and dominance in Dinoponera quadriceps ants.

ABSTRACT: Unequal reproductive output among members of the same sex (reproductive skew) is a common phenomenon in a wide range of communally breeding animals. In such species, reproductive dominance is often acquired during antagonistic interactions between group members that establish a reproductive hierarchy in which only a few individuals reproduce. Rank-specific syndromes of behavioural and physiological traits characterize such hierarchies, but how antagonistic behavioural interactions translate into stable rank-specific syndromes remains poorly understood. The pleiotropic nature of hormones makes them prime candidates for generating such syndromes as they physiologically integrate environmental (social) information, and often affect reproduction and behaviour simultaneously. Juvenile hormone (JH) is one of several hormones that occupy such a central regulatory role in insects and has been suggested to regulate reproductive hierarchies in a wide range of social insects including ants. Here we use experimental manipulation to investigate the effect of JH levels on reproductive physiology and social dominance in high-ranked workers of the eusocial ant Dinoponera quadriceps, a species that has secondarily reverted to queenless, simple societies. We show that JH regulated reproductive physiology, with ants in which JH levels were experimentally elevated having more regressed ovaries. In contrast, we found no evidence of JH levels affecting dominance in social interactions. This could indicate that JH and ovary development are decoupled from dominance in this species, however only high-ranked workers were investigated. The results therefore confirm that the regulatory role of JH in reproductive physiology in this ant species is in keeping with its highly eusocial ancestors rather than its secondary reversion to simple societies, but more investigation is needed to disentangle the relationships between hormones, behaviour and hierarchies.

SUBMITTER: Norman VC

PROVIDER: S-EPMC6398374 | biostudies-literature | 2019

REPOSITORIES: biostudies-literature

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The role of juvenile hormone in regulating reproductive physiology and dominance in <i>Dinoponera quadriceps</i> ants.

Norman Victoria C VC Pamminger Tobias T Nascimento Fabio F Hughes William O H WOH

PeerJ 20190301

Unequal reproductive output among members of the same sex (reproductive skew) is a common phenomenon in a wide range of communally breeding animals. In such species, reproductive dominance is often acquired during antagonistic interactions between group members that establish a reproductive hierarchy in which only a few individuals reproduce. Rank-specific syndromes of behavioural and physiological traits characterize such hierarchies, but how antagonistic behavioural interactions translate into ...[more]

PMID: 30842903

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Project description:Gonadotropin-releasing hormone (GnRH) controls the reproductive physiology and behavior of vertebrates by stimulating synthesis and release of gonadotropin from the pituitary gland. In 2000, another hypothalamic neuropeptide, gonadotropin-inhibitory hormone (GnIH), was discovered in quail and found to be an inhibiting factor for gonadotropin release. GnIH homologs are present in the brains of vertebrates, including birds, mammals, amphibians, and fish. These peptides, categorized as RF amide-related peptides (RFRPs), possess a characteristic LPXRF-amide (X = L or Q) motif at their C-termini. GnIH/RFRP precursor mRNA encodes a polypeptide that is possibly cleaved into three mature peptides in birds and two in mammals. The names of these peptides are GnIH, GnIH-related peptide-1 (GnIH-RP-1) and GnIH-RP-2 in birds, and RFRP-1 and RFRP-3 in mammals. GnIH/RFRP is synthesized in neurons of the paraventricular nucleus of the hypothalamus in birds and the dorsomedial hypothalamic area in mammals. GnIH neurons project to the median eminence, thus providing a functional neuroanatomical infrastructure to regulate anterior pituitary function. In quail, GnIH inhibits gonadal activity by decreasing synthesis and release of gonadotropin. The widespread distribution of GnIH/RFRP immunoreactive fibers in all animals tested suggests various actions within the brain. In accordance, GnIH/RFRP receptor mRNA is also expressed widely in the brain and the pituitary. GnIH/RFRP immunoreactive axon terminals are in probable contact with GnRH neurons in birds and mammals, and we recently demonstrated expression of GnIH receptor mRNA in GnRH-I and GnRH-II neurons in European starlings. Thus, GnIH/RFRP may also inhibit gonadotropin synthesis and release by inhibiting GnRH neurons in addition to having direct actions on the pituitary gland. Intracerebroventricular administration of GnIH/RFRP further inhibits reproductive behaviors in songbirds and rodents, possibly via direct actions on the GnRH system. The expression of GnIH/RFRP is regulated by melatonin which is an internal indicator of day length in vertebrates. Stress stimuli also regulate the expression of GnIH/RFRP in songbirds and rodents. Accordingly, GnIH/RFRP may serve as a transducer of environmental information and social interactions into endogenous physiology and behavior of the animal. Recently, it was shown that GnIH/RFRP and its receptor are also expressed in the gonads of birds, rodents and primates. In sum, the existing data suggest that GnIH/RFRP is an important mediator of reproductive function acting at the level of the brain, pituitary, and the gonad in birds and mammals.

Dataset Information

The role of juvenile hormone in regulating reproductive physiology and dominance in Dinoponera quadriceps ants.

Publications

The role of juvenile hormone in regulating reproductive physiology and dominance in <i>Dinoponera quadriceps</i> ants.

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