Preoptic galanin neuron activation is specific to courtship reproductive tactic in fish with two male morphs

AbstractSpecies exhibiting alternative reproductive tactics (ARTs) provide ideal models for investigating neural mechanisms underlying robust and consistent differences in social behavioral phenotypes between individuals within a single sex. Using phospho-S6 protein (pS6), a neural activity marker, we investigate the activation of galanin-expressing neurons in the preoptic area-anterior hypothalamus (POA-AH) during ARTs in midshipman fish (Porichthys notatus) that have two adult male morphs: type I’s that reproduce using an acoustic-dependent courtship tactic or a cuckolding tactic, and type II’s that only cuckold. The proportion of pS6-labelled galanin neurons increases during mating by courting type I males, but not cuckolders of either male morph or females, and is not explained by vocalization, eggs in the nest, or cuckolders present during mating. These differences within the same behavioral context indicate a male phenotype-specific role for galanin neurons in mating interactions, providing the most direct evidence to date for the role of a specific neuronal population in the differential activation of one mating behavior over the other in species exhibiting ARTs. More broadly, together with their known role in mammalian mating, the results suggest a deep-rooted, phylogenetically shared function for POA-AH galanin neurons in reproductive behavior. As such, these findings also provide new insights into the evolutionary relationship between POA-AH populations involved in social behavior regulation in teleosts, the most species-rich vertebrate group, with those in the more highly differentiated POA-AH of mammals.Significance StatementGalanin-expressing neurons in the preoptic area-anterior hypothalamus (POA-AH) are associated with mating and parental care in mammals. Here, we show that POA-AH galanin neurons are also active in a teleost fish during mating in a social context specific to one of two male morphs of a species with alternative reproductive tactics (ARTs). Together, the results suggest a key role for galanin-expressing neurons in the performance of reproductive-related social behaviors that is shared between distantly related vertebrate lineages and for galanin neuron activation in the evolution of ARTs. The results also help to clarify the relationship between molecularly-defined populations in the teleost POA-AH with the more highly differentiated mammalian POA-AH.

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Kin-Mediated Male Choice and Alternative Reproductive Tactics in Spider Mites

Biology ◽

10.3390/biology9110360 ◽

2020 ◽

Vol 9 (11) ◽

pp. 360

Author(s):

Peter Schausberger ◽

Yukie Sato

Keyword(s):

Random Mating ◽

Reproductive Potential ◽

Spider Mites ◽

Alternative Reproductive Tactics ◽

Male Choice ◽

Reproductive Tactics ◽

Kin Competition ◽

Context Specific ◽

Two Populations

Optimal outbreeding and kin selection theories state that the degree of kinship is a fundamental determinant in any mating system. However, the role of kinship in male choice and alternative reproductive tactics (ARTs) is poorly known. We assessed the influence of kinship on male choice and expression of ARTs in two populations of two-spotted spider mites Tetranychus urticae. Male spider mites guard premature females, which is an indicator of mate choice, and may conditionally adopt fighting or sneaking tactics to secure access to females. Males competing with kin or non-kin were offered one kin or non-kin female (experiment 1) and single males were presented a choice of kin and non-kin females (experiment 2). Under kin competition, males of both populations were more prone to guard non-kin than kin females at a 3:1 fighter:sneaker ratio. Under non-kin competition, all males were fighters. Under no-choice, males used novelty as indicator of genetic dissimilarity, serving as absolute decision rule for outbreeding. Under choice, comparative evaluation allowed males to preferentially guard females with higher reproductive potential. Overall, our study suggests that male spider mites can assess kinship of rivals and prospective mates. Kin discrimination allows adaptive, context-specific non-random mating preference and adjustment of ARTs.

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Alternative Reproductive Tactics

Reproductive Biology ◽

10.1093/oso/9780190688554.003.0015 ◽

2020 ◽

pp. 429-446

Author(s):

Shawn Garner ◽

Bryan Neff

Keyword(s):

Body Size ◽

Small Body ◽

Large Body ◽

Morphological Differentiation ◽

Alternative Reproductive Tactics ◽

Reproductive Tactics ◽

Aggressive Interactions ◽

Single Sex ◽

Female Mimicry ◽

Mating Opportunities

Alternative reproductive tactics (ARTs) describe variation among individuals of a single sex in the tactics used to obtain mating opportunities. In crustaceans, ARTs have been observed in multiple taxa and take a variety of forms. ARTs are most commonly observed in males and are generally associated with intense competition among males to monopolize access to breeding females. ARTs frequently involve a guard tactic that competes with other males to monopolize access to females, while a second usurper tactic foregos competition with other males and instead obtains mating opportunities through sneaking behavior. Guard and usurper tactics may be expressed conditionally based on a male’s ability to guard a female (e.g. his body size, the abundance of competitors), or may be expressed as discrete phenotypes that can also include morphological differentiation. For example, in Jassa amphipods the guard tactic is associated with large body size and an enlarged “thumb” on the claw that is used in aggressive interactions with other males, while the usurper tactic is associated with small body size and a reduced thumb. The usurper tactic can take two forms in a marine isopod: small males (gamma) use sneaking behavior to avoid competition with large males (alpha), whereas intermediate-sized males (beta) use female mimicry to avoid competition. Overall, ARTs are well-represented in crustaceans, with many opportunities for continued study to better characterize these unique adaptations.

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Behavioural tactic predicts preoptic-hypothalamic gene expression more strongly than developmental morph in fish with alternative reproductive tactics

Proceedings of The Royal Society B Biological Sciences ◽

10.1098/rspb.2017.2742 ◽

2018 ◽

Vol 285 (1871) ◽

pp. 20172742 ◽

Cited By ~ 10

Author(s):

Joel A. Tripp ◽

Ni Y. Feng ◽

Andrew H. Bass

Keyword(s):

Gene Expression ◽

Social Behaviour ◽

Hormonal Regulation ◽

Paternal Care ◽

Expression Patterns ◽

Alternative Reproductive Tactics ◽

Type I ◽

Type Ii ◽

Reproductive Tactics ◽

Territory Defence

Reproductive success relies on the coordination of social behaviours, such as territory defence, courtship and mating. Species with extreme variation in reproductive tactics are useful models for identifying the neural mechanisms underlying social behaviour plasticity. The plainfin midshipman ( Porichthys notatus ) is a teleost fish with two male reproductive morphs that follow widely divergent developmental trajectories and display alternative reproductive tactics (ARTs). Type I males defend territories, court females and provide paternal care, but will resort to cuckoldry if they cannot maintain a territory. Type II males reproduce only through cuckoldry. We sought to disentangle gene expression patterns underlying behavioural tactic, in this case ARTs, from those solely reflective of developmental morph. Using RNA-sequencing, we investigated differential transcript expression in the preoptic area-anterior hypothalamus (POA-AH) of courting type I males, cuckolding type I males and cuckolding type II males. Unexpectedly, POA-AH differential expression was more strongly coupled to behavioural tactic than morph. This included a suite of transcripts implicated in hormonal regulation of vertebrate social behaviour. Our results reveal that divergent expression patterns in a conserved neuroendocrine centre known to regulate social-reproductive behaviours across vertebrate lineages may be uncoupled from developmental history to enable plasticity in the performance of reproductive tactics.

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Competition and cuckoldry: estimating fitness of alternative reproductive tactics in plainfin midshipman

Behaviour ◽

10.1163/1568539x-00003180 ◽

2014 ◽

Vol 151 (8) ◽

pp. 1209-1227 ◽

Cited By ~ 18

Author(s):

Karen M. Cogliati ◽

Sigal Balshine ◽

Bryan D. Neff

Keyword(s):

Alternative Reproductive Tactics ◽

Type I ◽

Type Ii ◽

Reproductive Tactics ◽

System A ◽

Porichthys Notatus ◽

Gene By Environment Interactions ◽

Sampling Locations ◽

Plainfin Midshipman ◽

Reproductive Tactic

There has been much debate about how male alternative reproductive tactics (ARTs) evolve. In particular, researchers question whether ARTs have evolved as a conditional, ‘best of a bad job’ strategy where one tactic has higher fitness than the other, or whether they have evolved as a result of a genetic polymorphism where both tactics have equal fitness. Despite the large number of species known to have ARTs, tests of equal fitness between tactics have only been conducted in a handful of species. We tested the prediction of equal fitness using the plainfin midshipman (Porichthys notatus), a species with two well characterized male ARTs: guarding type I males and cuckolding type II males. We collected data across three years and three sampling locations to determine the proportion of each reproductive tactic, as well as the proportion of offspring sired by each male type using microsatellite markers. Our analysis suggests that males adopting the conventional guarding tactic likely have higher fitness compared to males adopting the cuckolder type II tactic. Also, we show that the guarding male tactic is able to gain paternity through cuckoldry, and that these males, who sometimes guard and sometimes cuckold, are responsible for the majority of paternity lost within nests. Indeed, the classic cuckolding type II males were responsible for only a small fraction of the paternity lost. These results highlight the degree of flexibility in male behaviour even among individuals adopting the same male tactic. Taken together, our results provide the first exploration of the evolution of male ARTs in plainfin midshipman and, given the tractability of midshipman system, a valuable next step will be to look for gene-by-environment interactions on tactic development and expression.

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Neuroanatomical differentiation associated with alternative reproductive tactics in male arid land bees, Centris pallida and Amegilla dawsoni

Journal of Comparative Physiology A ◽

10.1007/s00359-021-01492-4 ◽

2021 ◽

Author(s):

Meghan Barrett ◽

Sophi Schneider ◽

Purnima Sachdeva ◽

Angelina Gomez ◽

Stephen Buchmann ◽

...

Keyword(s):

Alternative Reproductive Tactics ◽

Arid Land ◽

Reproductive Tactics

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Alternative reproductive tactics and status-dependent selection

Behavioral Ecology ◽

10.1093/beheco/ari030 ◽

2005 ◽

Vol 16 (3) ◽

pp. 566-570 ◽

Cited By ~ 16

Author(s):

Jonathan S.F. Lee

Keyword(s):

Alternative Reproductive Tactics ◽

Reproductive Tactics

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Catecholaminergic Fiber Innervation of the Vocal Motor System Is Intrasexually Dimorphic in a Teleost with Alternative Reproductive Tactics

Brain Behavior and Evolution ◽

10.1159/000438720 ◽

2015 ◽

Vol 86 (2) ◽

pp. 131-144 ◽

Cited By ~ 6

Author(s):

Zachary N. Ghahramani ◽

Miky Timothy ◽

Gurpreet Kaur ◽

Michelle Gorbonosov ◽

Alena Chernenko ◽

...

Keyword(s):

Motor Neurons ◽

Motor System ◽

Advertisement Call ◽

Motor Nucleus ◽

Type I ◽

Type Ii ◽

Fiber Density ◽

Reproductive Tactics ◽

Long Duration ◽

Behavioral Divergence

Catecholamines, which include the neurotransmitters dopamine and noradrenaline, are known modulators of sensorimotor function, reproduction, and sexually motivated behaviors across vertebrates, including vocal-acoustic communication. Recently, we demonstrated robust catecholaminergic (CA) innervation throughout the vocal motor system in the plainfin midshipman fish Porichthys notatus, a seasonal breeding marine teleost that produces vocal signals for social communication. There are 2 distinct male reproductive morphs in this species: type I males establish nests and court females with a long-duration advertisement call, while type II males sneak spawn to steal fertilizations from type I males. Like females, type II males can only produce brief, agonistic, grunt type vocalizations. Here, we tested the hypothesis that intrasexual differences in the number of CA neurons and their fiber innervation patterns throughout the vocal motor pathway may provide neural substrates underlying divergence in reproductive behavior between morphs. We employed immunofluorescence (-ir) histochemistry to measure tyrosine hydroxylase (TH; a rate-limiting enzyme in catecholamine synthesis) neuron numbers in several forebrain and hindbrain nuclei as well as TH-ir fiber innervation throughout the vocal pathway in type I and type II males collected from nests during the summer reproductive season. After controlling for differences in body size, only one group of CA neurons displayed an unequivocal difference between male morphs: the extraventricular vagal-associated TH-ir neurons, located just lateral to the dimorphic vocal motor nucleus (VMN), were significantly greater in number in type II males. In addition, type II males exhibited greater TH-ir fiber density within the VMN and greater numbers of TH-ir varicosities with putative contacts on vocal motor neurons. This strong inverse relationship between the predominant vocal morphotype and the CA innervation of vocal motor neurons suggests that catecholamines may function to inhibit vocal output in midshipman. These findings support catecholamines as direct modulators of vocal behavior, and differential CA input appears reflective of social and reproductive behavioral divergence between male midshipman morphs.

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