A Novel Body Plan Alters Diversification of Body Shape and Genitalia in Live-Bearing Fish

Langerhans, R. Brian; Rosa‐Molinar, Eduardo

doi:10.3389/fevo.2021.619232

Cited by 4 publications

(3 citation statements)

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“…Major evolutionary transitions, such as changes in body plan, invading novel environments, and evolution of novel traits, can cause rapid adaptive diversification and lead to new evolutionary routes because evolutionary change is contingent on past evolutionary history (Gould, 2002 ; McLennan, 2008 ; Losos, 2009 ; Wellborn and Langerhans, 2015 ). Subsequent to the evolution of the novel three-part body plan of poeciliid fishes, recent work has suggested that traits within the gonopodial complex have been co-opted for new evolutionary functions (Langerhans and Rosa-Molinar, 2021 ; and references therein). Similarly, we propose that Poeciliids may have remodeled or co-opted some sensory structures to adapt to changes in the novel ano-urogenital region and associated mating behaviors to fulfill the new copulatory function.…”

Section: Discussionmentioning

confidence: 99%

“…Observations and quantification analyses of labeled superficial neuromasts in this study for both males and females were focused on two of three anatomical regions previously described in Gambusia (Rosa-Molinar et al, 1994 , 1998 ; Rosa-Molinar, 2005 ): the ano-urogenital and caudal regions (see diagram in Figures 2C,D ). In male Gambusia, the ano-genital region is specifically defined as the region between the 8th and 14th spinal vertebral segments where the 8th vertebra is aligned with the base of the anal fin (Rosa-Molinar et al, 1994 , 1998 ; Rivera-Rivera et al, 2010 ; Langerhans and Rosa-Molinar, 2021 for better visual reference). Two-tailed t -tests were conducted to determine whether the sexes differed in the number of labeled superficial neuromasts.…”

Section: Methodsmentioning

confidence: 99%

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Are superficial neuromasts proprioceptors underlying fast copulatory behavior?

Martínez-Rivera

Serrano-Vélez²,

Torres-Vazquez³

et al. 2022

Front. Neural Circuits

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In male Poeciliid fishes, the modified anal fin (i.e., gonopodium) and its axial and appendicular support are repositioned within the axial skeleton, creating a novel sexually dimorphic ano-urogenital region. During copulation, the relative location of the gonopodium is crucial for successful insemination. Therefore, the repositioning of these structures and organ relied on the reorganization of the efferent circuitry that controls spinal motor neurons innervating appendicular muscles critical for the movement of the gonopodium, including the fast and synchronous torque-trust motion during insemination attempts. Copulation occurs when a male positions himself largely outside a female’s field of view, circumducts his gonopodium, and performs a rapid, complex maneuver to properly contact the female urogenital sinus with the distal tip of the gonopodium and transfers sperm. Although understanding of the efferent circuitry has significantly increased in the last 24 years, nothing is known about the cutaneous receptors involved in gonopodium movement, or how the afferent signals are processed to determine the location of this organ during copulation. Using Western mosquitofish, Gambusia affinis, as our model, we attempt to fill this gap in knowledge. Preliminary data showed cutaneous nerves and sensory neurons innervating superficial neuromasts surrounding the base of adult male gonopodium; those cutaneous nerves projected ventrally from the spinal cord through the 14th dorsal root ganglion and its corresponding ventral root towards the base and fin rays of the gonopodium. We asked what role the cutaneous superficial neuromasts play in controlling the positioning and timing of the gonopodium’s fast and synchronous movements for effective sperm transfer. First, we found a greater number of superficial neuromasts surrounding the base of the male’s gonopodium compared to the base of the female’s anal fin. Second, we systemically removed superficial neuromasts surrounding the gonopodium base and observed significant impairment of the positioning and timing of gonopodial movements. Our findings provide a first step to supporting the following hypothesis: during radical reorganization of the Poeciliid body plan, superficial neuromasts have been partially co-opted as proprioceptors that allow the gonopodium to control precise positioning and timing during copulatory attempts.

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Section: Discussionmentioning

confidence: 99%

Section: Methodsmentioning

confidence: 99%

Are superficial neuromasts proprioceptors underlying fast copulatory behavior?

Martínez-Rivera

Serrano-Vélez²,

Torres-Vazquez³

et al. 2022

Front. Neural Circuits

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“…Blue holes were selected a priori as representative of the larger set of blue holes on Andros Island and are characterized by independent colonization events and low gene flow between mosquitofish populations (e.g. Heinen‐Kay & Langerhans, 2013; Langerhans, 2017; Langerhans et al, 2007; Langerhans & Rosa‐Molinar, 2021; Riesch et al, 2013). Despite varying resource availability (e.g.…”

Section: Methodsmentioning

confidence: 99%

Predation risk and the evolution of a vertebrate stress response: Parallel evolution of stress reactivity and sexual dimorphism

Vinterstare

Ugge

Hegg

et al. 2021

J of Evolutionary Biology

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Predation risk is often invoked to explain variation in stress responses. Yet, the answers to several key questions remain elusive, including the following: (1) how predation risk influences the evolution of stress phenotypes, (2) the relative importance of environmental versus genetic factors in stress reactivity and (3) sexual dimorphism in stress physiology. To address these questions, we explored variation in stress reactivity (ventilation frequency) in a post‐Pleistocene radiation of live‐bearing fish, where Bahamas mosquitofish (Gambusia hubbsi) inhabit isolated blue holes that differ in predation risk. Individuals of populations coexisting with predators exhibited similar, relatively low stress reactivity as compared to low‐predation populations. We suggest that this dampened stress reactivity has evolved to reduce energy expenditure in environments with frequent and intense stressors, such as piscivorous fish. Importantly, the magnitude of stress responses exhibited by fish from high‐predation sites in the wild changed very little after two generations of laboratory rearing in the absence of predators. By comparison, low‐predation populations exhibited greater among‐population variation and larger changes subsequent to laboratory rearing. These low‐predation populations appear to have evolved more dampened stress responses in blue holes with lower food availability. Moreover, females showed a lower ventilation frequency, and this sexual dimorphism was stronger in high‐predation populations. This may reflect a greater premium placed on energy efficiency in live‐bearing females, especially under high‐predation risk where females show higher fecundities. Altogether, by demonstrating parallel adaptive divergence in stress reactivity, we highlight how energetic trade‐offs may mould the evolution of the vertebrate stress response under varying predation risk and resource availability.

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