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Effects of Chronic Thermal Stress on the Reproductive Performance of Male

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Effects of Chronic Thermal Stress on the Reproductive Performance of Male bioRxiv preprint doi: https://doi.org/10.1101/267476; this version posted February 18, 2018. The copyright holder for this preprint (which was not certified by peer review) is the author/funder. All rights reserved. No reuse allowed without permission. 1 Effects of chronic thermal stress on the reproductive performance of male 2 Octopus maya 3 4 Runnig title: Male Octopus maya reproductive fitness under stress 5 6 Laura López-Galindo1, Clara Galindo-Sánchez1, Alberto Olivares2, Omar 7 Hernando Avila-Poveda3,4, Fernando Díaz1, Oscar E. Juárez1, Fabiola Lafarga5, 8 Jordi Pantoja-Pérez5, Claudia Caamal-Monsreal6, Carlos Rosas6,7 9 10 1 Departamento de Biotecnología Marina, Centro de Investigación Científica y 11 Educación Superior de Ensenada, Ensenada, Baja California, México 12 2 Facultad de Ciencias del Mar y Recursos Biológicos, Universidad de 13 Antofagasta, Departamento de Biotecnología, Antofagasta, Chile 14 3 Facultad de Ciencias del Mar, Universidad Autónoma de Sinaloa, Mazatlán, 15 Sinaloa, México 16 4 Dirección de Cátedras-CONACYT, Consejo Nacional de Ciencia y Tecnología 17 (CONACYT), Ciudad de México, México4 18 5 Departamento de Acuicultura, Centro de Investigación Científica y Educación 19 Superior de Ensenada, Ensenada, Baja California, México 20 6Unidad Multidisciplinaria de Docencia e Investigación, Facultad de Ciencias, 21 Universidad Nacional Autónoma de México, Sisal, Yucatán, México 22 7 Laboratorio Nacional de Resiliencia Costera, CONACYT, Sisal, Yucatán, 23 México 24 25 *corresponding author 26 E-mail: [email protected] (CR) 27 28 Keywords: sperm quality, testis damage, physiological condition, multiple 29 paternity, paternal contribution. 30 31 Summary statement 32 Temperature affects the physiology and the reproductive performance of male 33 Octopus maya, an important fishing resource in the Yucatan Peninsula. You created this PDF from an application that is not licensed to print to novaPDF printer (http://www.novapdf.com) bioRxiv preprint doi: https://doi.org/10.1101/267476; this version posted February 18, 2018. The copyright holder for this preprint (which was not certified by peer review) is the author/funder. All rights reserved. No reuse allowed without permission. 2 34 Abstract 35 36 In female Octopus maya the reproductive success has well-defined thermal 37 limits; beyond which, spawning, number of eggs, fecundity, and the viability of 38 the embryos are reduced. Observations of wild male O. maya suggest that 39 temperatures below 27°C favour their reproductive performance. From these 40 observations we hypothesize that, as in females, the temperature modulates 41 the reproductive performance of adult O. maya males. The study was directed 42 to evaluate the physiological condition, reproductive success, and histological 43 damage in testis of male O. maya exposed to thermal stress, to determine the 44 implications of ocean warming over their reproductive performance. High 45 temperatures (28-30°C) negatively affect the growth and health of male O. 46 maya. In octopuses maintained at 30°C, as a consequence of the thermal 47 stress we observed an increment in the haemocytes number, a reduction in the 48 oxygen consumption rate, and an inflammatory process in the testis. The 49 number of spermatozoa per spermatophore was not affected by temperature, 50 but higher spermatophores production was observed at 30°C. The paternity 51 analysis showed that the offspring had multiple paternity with an average of 10 52 males contributing in a single spawn. The paternal contribution was affected by 53 temperature with high, medium, or no paternal contribution in animals 54 maintained at 24°C (control group), 28°C, and 30°C, respectively. The 55 temperatures from 28°C to 30°C deeply affected the reproductive performance 56 of Octopus maya males. You created this PDF from an application that is not licensed to print to novaPDF printer (http://www.novapdf.com) bioRxiv preprint doi: https://doi.org/10.1101/267476; this version posted February 18, 2018. The copyright holder for this preprint (which was not certified by peer review) is the author/funder. All rights reserved. No reuse allowed without permission. 3 57 Introduction 58 59 Aquatic environments are thermally heterogeneous in time and space. 60 Organisms inhabiting these environments, specifically ectotherm organisms, 61 show morphological, behavioural, and physiological mechanisms (phenotypic 62 plasticity) that give them adaptive capabilities to cope with environmental 63 changes (Pigliucci, 1996; Somero, 2010; Bozinovic and Pörtner, 2015; Deutchs 64 et al., 2015; Piasečná et al., 2015). Animal physiology, ecology, and evolution 65 are affected by temperature, It is also expected that community structure will be 66 strongly influenced by global warming (Nguyen et al., 2011). For example, 67 temperature seemed to play the most important role in structuring the 68 distribution of cephalopod body size along the continental shelves of the 69 Atlantic Ocean, while resource availability, seasonality, or competition only 70 played a limited role in determining latitudinal body size patterns (Rosa et al., 71 2012). 72 In the eastern region of the continental shelf of Yucatan Peninsula (YP), 73 Mexico, a summer upwelling allows sub-superficial subtropical water from the 74 Caribbean (between 150 and 200 m deep) to enter the shelf with temperatures 75 between 16°C and 22ºC (Enriquez et al., 2013a). This cold water mass, besides 76 functioning as an external temperature control for the shelf, transports nutrients 77 which are used by primary producers (Enriquez et al., 2010). This upwelling 78 affects only the eastern portion of the YP continental shelf provoking a summer 79 thermal gradient that runs from the western to the eastern shelf from high to low 80 temperatures, offering different environments to aquatic species of the zone 81 (Zavala-Hidalgo et al., 2003; Zavala-Hidalgo et al., 2006; Ciencias de la 82 atmósfera, http://uniatmos.atmosfera.unam.mx/ACDM/ ). 83 Octopus maya is endemic to the YP continental shelf. This species is the most 84 important octopus fishery in the American continent, with an annual production 85 fluctuating between 8,000 and 20,000 Tons (SAGARPA, 2013; Galindo-Cortés 86 et al., 2014; Gamboa-Álvarez et al., 2015). O. maya is an ectotherm organism 87 particularly temperature-sensitive (Noyola et al., 2013a; Noyola et al., 2013b) 88 that can be affected in its morphology, behaviour, physiology and reproduction 89 by changes in ambient temperature with spatio-temporal fluctuations. 90 Predictions of the thermal processes on the YP shelf indicate that sea You created this PDF from an application that is not licensed to print to novaPDF printer (http://www.novapdf.com) bioRxiv preprint doi: https://doi.org/10.1101/267476; this version posted February 18, 2018. The copyright holder for this preprint (which was not certified by peer review) is the author/funder. All rights reserved. No reuse allowed without permission. 4 91 temperatures may rise between 2.5 to 3°C in the zone where upwelling has no 92 effect (Enriquez et al., 2013b; Saldívar-Lucio et al., 2015). This temperature 93 increase could be deleterious for this especies, affecting the regional fishing 94 economy. Gamboa-Álvarez et al., (2015) observed that during the August- 95 December fishing season, the greatest abundances of O. maya was found 96 along the Campeche coast (western zone, without upwelling influence), where 97 small octopus were fished; whereas, in the eastern zone, less abundances 98 were recorded, but octopus with higher biomass were caught. It was also 99 observed that the O. maya wild population reproduces year round in the YP 100 eastern zone, due to low temperatures maintained by the summer upwelling; 101 whereas in the western zone, reproduction occurs only during the winter storms 102 (‘nortes’ season, November–February), when low temperatures favour egg- 103 laying (Avila-Poveda et al., 2015; Markaida et al., 2016; Angeles-Gonzalez et 104 al., 2017). 105 In laboratory conditions, at 31°C the spawning of female O. maya was 106 significantly reduced and only 13% of the total females (n= 32) spawned, while 107 the few fertilized eggs (embryos) were not developed or died after two weeks 108 (Juárez et al., 2015). It was observed that females exposed to a temperature 109 decrease of 1°C every 5 days and starting at 31°C, only 87% spawned after 110 temperatures reached less than 27°C, and of these only 50% of the eggs laid 111 (mean 530 eggs per spawn) were fertilized (Juárez et al., 2015). Those results 112 suggested that temperature could be deleterious to sperm stored in the 113 spermathecae of the oviductal glands, which play a crucial role in octopus 114 reproduction (Olivares et al., 2017). At a later date, the performance of juveniles 115 hatched from those thermal stressed females was evaluated (Juarez et al., 116 2016). Results obtained in that study showed that juveniles from stressed 117 females had lower growth rate and twice the metabolic rate than hatchlings 118 coming from unstressed females, providing evidence that temperature stress 119 experienced by females has consequences on the performance of hatchlings, 120 with effects on the biomass production and survival. 121 To date, a small number of studies have investigated multiple paternity within 122 cephalopods by using microsatellite markers demonstrating that multiple 123 paternity could be a common characteristic in octopus species. Voight and 124 Feldheim (2009) sampled Granelodone boreopacifica juveniles and found at You created this PDF from an application that is not licensed to print to novaPDF printer (http://www.novapdf.com) bioRxiv preprint doi: https://doi.org/10.1101/267476; this version posted February 18, 2018. The copyright holder for this preprint (which was not certified by peer review) is the author/funder. All rights reserved. No reuse allowed without permission. 5 125 least two genetically distinct sires that contribute to the progeny. Quinteiro et al., 126 (2011) found evidence of between two to four siring males in egg clutches of O.
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