The influence of increased water temperature on the duration of spermatogenesis in a neotropical fish, Astyanax altiparanae (Characiformes, Characidae)

Quirino, Patrícia Postingel; Rodrigues, Maira da Silva; Cabral, Elis Marina da Silva; Siqueira‐Silva, Diógenes Henrique de; Mori, Ricardo; Butzge, Arno Juliano; Nóbrega, Rafael Henrique; Ninhaus‐Silveira, Alexandre; Veríssimo‐Silveira, Rosicleire

doi:10.1007/s10695-020-00869-7

Cited by 14 publications

(5 citation statements)

References 39 publications

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“…This phase is characterized by a rapid mitotic proliferation of germ and Sertoli cells [37] through a fixed number of mitotic divisions (6-8 in Salmoniformes according to [53]), before formation of the spermatocytes that enter meiosis. The speed of this mitotic proliferation as well as the following meiotic phase has been found dependent upon temperature in tilapia Oreochromis niloticus [54] and in the tropical fish Astyanax altiparanae [55]. Similarly, our study also documents an advanced rate of spermatogenesis in response to high temperature but in a temperate species.…”

Section: High Temperature Stimulated the Early Presence Of Type B Spe...supporting

confidence: 79%

“…As ectothermic organisms, fish experience remarkable physiological, endocrine, and metabolic changes when exposed to different water temperatures, and this includes adaptations in the reproductive axis [13,22]. For example, the duration of spermatogenesis in fish depends on the water temperature, with high temperatures within the normal thermal tolerance range of the species accelerating the process and reducing its duration [53][54][55]. In Atlantic salmon, initiation of spermatogenesis is concomitant with increases in the water temperature and photoperiod occurring in the spring/summer [28], and thus it is likely that exposure to a sustained high temperature in our study stimulated entering the first phase of spermatogenesis.…”

Section: High Temperature Stimulated the Early Presence Of Type B Spe...mentioning

confidence: 99%

“…However, the effects of these conditions on regulation of spermatogenesis were not analyzed. High temperature is believed to accelerate spermatogenesis, although studies on testis development at different temperatures have been performed mostly on warm water species such as Nile tilapia Oreochromis niloticus [53,54] or Astyanax altiparanae [55]. Thus, further research on changes occurring during spermatogenesis in response to different temperatures in temperate species such as Atlantic salmon is needed.…”

Section: Introductionmentioning

confidence: 99%

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Constant High Temperature Promotes Early Changes in Testis Development Associated with Sexual Maturation in Male Atlantic Salmon (Salmo salar L.) Post-Smolts

Martinez

Braanaas

Balseiro

et al. 2022

Fishes

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Sexual maturation of post-smolts is a concern for Atlantic salmon producers, and its occurrence is dependent upon factors such as water temperature and energy availability, among others. The present study was designed to investigate the effect of different temperatures and feeding regimes on testis development and local regulation of spermatogenesis in salmon post-smolts. A 3 × 2 factorial design was used, with three temperatures (8 °C, 12.5 °C, and 18 °C) and two feed regimes (100% and 67% ration). Salmon (1800 parr, initial mean weight 23.1 ± 7.2 g) were reared from 28 October 2018 to 30 May 2019 in a freshwater flow-through system under continuous light (LD24:0), except for a 5-week winter signal (LD12:12) introduced on 4 February 2019. Testis histology, transcription of follicle-stimulating hormone receptor (fshr) and luteinizing hormone receptor (lhr), and transcription of testis proteins involved in spermatogenesis regulation such as gonadal-soma-derived factors 1 (gsdf1) and 2 (gsdf2), anti-Müllerian hormone (amh), and insulin-like growth factor-3 (igf3), were analyzed. Results showed that high temperature alone (18 °C), irrespective of the feed regime, promoted early presence of type B spermatogonia and reduced transcript levels of the proliferation-inhibitory factor amh in males still considered immature, of groups 18–100% and 18–67% that later matured in high proportion (~100%). This effect was also present to some degree in the group 12.5–100% (40% maturation), and absent in 12.5–67%, 8–100%, and 8–67% (groups with little or no maturation). Later, at onset of rapid testis growth, high temperature was linked to a pronounced downregulation of amh and of the self-renewal factors gsdf1 and gsdf2, as well as to a pronounced upregulation of the proliferation-stimulating factor igf3. Overall, the present findings demonstrate that rearing salmon at high temperatures can stimulate an early activation of the brain–pituitary–gonad axis before actual onset of rapid testis growth, enhancing and accelerating the mechanisms that control initiation and progression of maturation, while the feed regime has a minor impact. This poses a challenge for current salmon aquaculture practices that use sustained high temperature to maximize growth, since these practices increase the risk of early post-smolt maturation.

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Section: High Temperature Stimulated the Early Presence Of Type B Spe...supporting

confidence: 79%

Section: High Temperature Stimulated the Early Presence Of Type B Spe...mentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

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Constant High Temperature Promotes Early Changes in Testis Development Associated with Sexual Maturation in Male Atlantic Salmon (Salmo salar L.) Post-Smolts

Martinez

Braanaas

Balseiro

et al. 2022

Fishes

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“…Another effect of temperature on reproduction occurs through regulation of the reproductive cycle, either by promoting 7 , 8 or suppressing gametogenesis 9 . However, chronic exposure at those temperatures or acute thermal stress at even higher temperatures can cause opposite inhibitory effects on spermatogenesis 10 , 11 .…”

mentioning

confidence: 99%

Early warming stress on rainbow trout juveniles impairs male reproduction but contrastingly elicits intergenerational thermotolerance

Butzge

Yoshinaga

Acosta

et al. 2021

Sci Rep

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The exposure of adult fish to warm or high temperatures is known to impair reproduction, yet the long-term reproductive impacts for treatments at early life are not well clarified. This study aimed to evaluate the effects of warm temperature (WT) during juvenile stage on gonad maturation, gamete quality, and offspring thermotolerance in rainbow trout. While the comparison of basic reproductive parameters in WT females did not reveal any kind of impairment, many WT males showed an atrophied, undeveloped gonad, or a smaller testis with lower milt volume; sperm quality parameters in WT males and deformity rates in the respective progeny were also highly affected. However, despite of such negative effects, many of the remaining progeny presented better rates of survival and growth when exposed to the same conditions as those of parental fish (WT), suggesting that thermal stress in parr stage males elicited intergenerational thermotolerance after a single generation. The present results support that prolonged warming stress during early life stages can adversely affect key reproductive aspects, but contrastingly increase offspring performance at upper thermal ranges. These findings have implications on the capacity of fish to adapt and to cope with global warming.

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“…Strikingly, heatwave males showed an increase in sperm number after the treatment, which was not the case in control males. The increase in number of spermatozoa produced likely resulted from an elevated rate of metabolism and associated accelerated spermatogenesis under the higher temperature, as observed in some other fishes (Nóbrega et al, 2009;Postingel Quirino et al, 2021). However, the heatwave had negative effects on sperm quality, since sperm velocity was lower in the heatwave males compared to the control males after the treatment.…”

Section: Heatwaves At Population Levelmentioning

confidence: 82%

Reproducing in hot water: Experimental heatwaves deteriorate multiple reproductive traits in a freshwater ectotherm

et al. 2023

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The influence of increased water temperature on the duration of spermatogenesis in a neotropical fish, Astyanax altiparanae (Characiformes, Characidae)

Cited by 14 publications

References 39 publications

Constant High Temperature Promotes Early Changes in Testis Development Associated with Sexual Maturation in Male Atlantic Salmon (Salmo salar L.) Post-Smolts

Constant High Temperature Promotes Early Changes in Testis Development Associated with Sexual Maturation in Male Atlantic Salmon (Salmo salar L.) Post-Smolts

Early warming stress on rainbow trout juveniles impairs male reproduction but contrastingly elicits intergenerational thermotolerance

Reproducing in hot water: Experimental heatwaves deteriorate multiple reproductive traits in a freshwater ectotherm

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