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

Behaviour ◽  
2014 ◽  
Vol 151 (8) ◽  
pp. 1209-1227 ◽  
Author(s):  
Karen M. Cogliati ◽  
Sigal Balshine ◽  
Bryan D. Neff

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.

2018 ◽  
Vol 285 (1871) ◽  
pp. 20172742 ◽  
Author(s):  
Joel A. Tripp ◽  
Ni Y. Feng ◽  
Andrew H. Bass

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.


2015 ◽  
Vol 86 (2) ◽  
pp. 131-144 ◽  
Author(s):  
Zachary N. Ghahramani ◽  
Miky Timothy ◽  
Gurpreet Kaur ◽  
Michelle Gorbonosov ◽  
Alena Chernenko ◽  
...  

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.


Behaviour ◽  
1994 ◽  
Vol 129 (3-4) ◽  
pp. 177-201 ◽  
Author(s):  
Peter Nurnberg ◽  
John D. Berard ◽  
Jorg T. Epplen ◽  
Jorg Schmidtke

AbstractMale rhesus macaques on Cayo Santiago use rank-dependent alternative reproductive tactics. High-ranking males can form long-term consorts and guard female mates while low-ranking males frequently resort to quick copulations under the cover of vegetation. No single reproductive tactic provided the Group S males with a definitive reproductive advantage during the one-year study. Males using the long-term tactic and the quick, stealth tactic sired five offspring each, but fewer males used the long-term consort tactic. Males using the long-term reproductive tactic have significantly greater mating success than males using the quick, sneaky tactic, and may have greater reproductive success. The highest-ranking males who form long-term consorts had the greatest degree of reproductive success. This indicates that for the highest-ranking males, forming long-term consorts is the most effective reproductive tactic. The effectiveness of alternative tactics for high-ranking males (i.e. consort disruption and possessive following) was equivocal. Consort disruption had no immediate effect on reproductive success. Possessive following may have resulted in the siring of two offspring by the alpha male, but was ineffective in other cases, where the females were inseminated by subordinate males. The effectiveness of the quick, furtive tactic was demonstrated by the siring of 45% of the infants by males who used this tactic.


2017 ◽  
Vol 203 (3) ◽  
pp. 211-222 ◽  
Author(s):  
Ashwin A. Bhandiwad ◽  
Elizabeth A. Whitchurch ◽  
Orphal Colleye ◽  
David G. Zeddies ◽  
Joseph A. Sisneros

2017 ◽  
Vol 284 (1868) ◽  
pp. 20172223 ◽  
Author(s):  
Armando Hernandez-Jimenez ◽  
Oscar Rios-Cardenas

There is extensive morphological variation of male genitalia across animals with internal fertilization, even among closely related species. Most studies attempting to explain this extraordinary diversity have focused on processes that occur post-copula (e.g. sperm competition, cryptic female choice). Only a few studies have focused on the pre-copula process of female preference. In addition, the extent to which this variation could be associated with the use of different reproductive tactics has yet to be explored. Here, we show that female preference for male genitalia length in two livebearing fishes depends on the type of reproductive tactic of the males being evaluated as well as the body condition of the female. In a species where all males coax females to acquire matings (courters), females preferred males with short genitalia. In a species with genetically influenced alternative reproductive tactics (courter males that only court and produce courter sons, sneaker males that use the coercive tactic of sneak chase and produce sneaker sons), female preference depended on an interaction between male tactic and female condition: females in good condition preferred courter males with short genitalia, and sneaker males with long genitalia. Our results suggest that female preference for male traits favourable to their sons may be an important factor contributing to the diversification of male genitalia. Despite the contrasting selection for genitalia length that our female preference tests suggest, we found no significant differences in genitalia length between coaxing (courters) and coercive (sneakers) males. Our study represents a starting point to more clearly understand the role of alternative reproductive tactics and variation in female mate preference in the evolution of male genitalia.


2019 ◽  
Author(s):  
Joel A. Tripp ◽  
Isabella Salas-Allende ◽  
Andrea Makowski ◽  
Andrew H. Bass

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.


2019 ◽  
Vol 65 (6) ◽  
pp. 609-616 ◽  
Author(s):  
Magali Meniri ◽  
Florence Gohon ◽  
Ophélie Gning ◽  
Gaétan Glauser ◽  
Armelle Vallat ◽  
...  

AbstractTo reproduce, males have to fertilize the female’s eggs, sometimes in competition with ejaculates of other males. In species where males display alternative reproductive tactics, whereby territorial males secure mating and non-territorial males have to sneak copulations, the latter might be expected to invest relatively more resources towards sperm quality compared with the territorial males. Sperm cells are especially vulnerable to oxidative stress, which reduces male fertility. Therefore, antioxidant resources are expected to modulate sperm quality, and might be allocated differently between reproductive tactics. To test the link between reproductive tactics, redox profile and sperm quality, we experimentally induced changes in the reproductive tactics of 39 captive males Seba’s short-tailed bats Carollia perspicillata. We monitored the blood and ejaculate oxidative balance, and the sperm quality before, 7 days and 21 days after the manipulation of reproductive tactic. Although ejaculates’ oxidative damage was negatively related to sperm velocity, males exhibited similar blood and ejaculates redox profiles and similar sperm quality, regardless of their reproductive tactic. Possibly, these results arise as a consequence of some constraints having been lifted during the experiment. Our results also suggest that, in Seba’s short-tailed bats, the expression of alternative reproductive tactics is not subjected to strong oxidative constraints. Furthermore, our results could reflect an absence of trade-off between pre- and post-copulatory traits in harem males, as they could be selected to invest both in female attraction and sperm quality, as a consequence of their inability to fully monopolize females.


2020 ◽  
Vol 223 (14) ◽  
pp. jeb225177
Author(s):  
Brooke J. Vetter ◽  
Joseph A. Sisneros

ABSTRACTThe plainfin midshipman fish (Porichthys notatus) is an established model for investigating acoustic communication because the reproductive success of this species is dependent on the production and reception of social acoustic signals. Previous work showed that female midshipman have swim bladders with rostral horn-like extensions that project close to the saccule and lagena, while nesting (type I) males lack such rostral swim bladder extensions. The relative close proximity of the swim bladder to the lagena should increase auditory sensitivity to sound pressure and higher frequencies. Here, we test the hypothesis that the swim bladder of female midshipman enhances lagenar sensitivity to sound pressure and higher frequencies. Evoked potentials were recorded from auditory hair cell receptors in the lagena in reproductive females with intact (control condition) and removed (treated condition) swim bladders while pure tone stimuli (85–1005 Hz) were presented by an underwater speaker. Females with intact swim bladders had auditory thresholds 3–6 dB lower than females without swim bladders over a range of frequencies from 85 to 405 Hz. At frequencies from 545 to 1005 Hz, only females with intact swim bladders had measurable auditory thresholds (150–153 dB re. 1 µPa). The higher percentage of evoked lagenar potentials recorded in control females at frequencies >505 Hz indicates that the swim bladder extends the bandwidth of detectable frequencies. These findings reveal that the swim bladders in female midshipman can enhance lagenar sensitivity to sound pressure and higher frequencies, which may be important for the detection of behaviorally relevant social signals.


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