"Bet hedging" against climate change in developing and adult animals: roles for stochastic gene expression, phenotypic plasticity, epigenetic inheritance and adaptation.

Animals from embryos to adults experiencing stress from climate change have numerous mechanisms available for enhancing their long-term survival. In this review we consider these options, and how viable they are in a world increasingly experiencing extreme weather associated with climate change. A deeply understood mechanism involves natural selection, leading to evolution of new adaptations that help cope with extreme and stochastic weather events associated with climate change. While potentially effective at staving off environmental challenges, such adaptations typically occur very slowly and incrementally over evolutionary time. Consequently, adaptation through natural selection is in most instances regarded as too slow to aid survival in rapidly changing environments, especially when considering the stochastic nature of extreme weather events associated with climate change. Alternative mechanisms operating in a much shorter time frame than adaptation involve the rapid creation of alternate phenotypes within a life cycle or a few generations. Stochastic gene expression creates multiple phenotypes from the same genotype even in the absence of environmental cues. In contrast, other mechanisms for phenotype change that are externally driven by environmental clues include well-understood developmental phenotypic plasticity (variation, flexibility), which can enable rapid, within-generation changes. Increasingly appreciated are epigenetic influences during development leading to rapid phenotypic changes that can also immediately be very widespread throughout a population, rather than confined to a few individuals as in the case of favorable gene mutations. Such epigenetically-induced phenotypic plasticity can arise rapidly in response to stressors within a generation or across a few generations and just as rapidly be "sunsetted" when the stressor dissipates, providing some capability to withstand environmental stressors emerging from climate change. Importantly, survival mechanisms resulting from adaptations and developmental phenotypic plasticity are not necessarily mutually exclusive, allowing for classic "bet hedging". Thus, the appearance of multiple phenotypes within a single population provides for a phenotype potentially optimal for some future environment. This enhances survival during stochastic extreme weather events associated with climate change. Finally, we end with recommendations for future physiological experiments, recommending in particular that experiments investigating phenotypic flexibility adopt more realistic protocols that reflect the stochastic nature of weather.

Metabolic rate and hypoxia tolerance in Girardinichthys multiradiatus (Pisces: Goodeidae), an endemic fish at high altitude in tropical Mexico.

The darkedged splitfin (Amarillo fish), Girardinichthys multiradiatus is a vulnerable endemic fish species inhabiting central Mexico's high altitude Upper Lerma Basin, where aquatic hypoxia is exacerbated by low barometric pressures (lower PO2s), large aquatic oxygen changes, poor aquatic systems management and urban, agricultural and industrial pollution. The respiratory physiology of G. multiradiatus under such challenging conditions is unknown - therefore the main goal of the present study was to determine metabolic rates and hypoxia tolerance to elucidate possible physiological adaptations allowing this fish to survive high altitude and increasingly eutrophic conditions. Fish came from two artificial reservoirs - San Elías and Ex Hacienda - considered refuges for this species. Both reservoirs showed high dial PO2 variation, with hypoxic conditions before midday and after 20:00 h, ~4 h of normoxia (15 kPa) from 16:00-20:00, and ~4 h of hyperoxia (16-33 kPa) from 12:00-16:00. Standard metabolic rate at 20 ±â€¯0.5 °C of larvae from Ex Hacienda was significantly higher than those from San Elías, but these differences disappeared in juveniles and adults. Metabolic rate at 20 ±â€¯0.5 °C for adults was 9.8 ±â€¯0.1 SEM µmol O2/g/h. The metabolic scaling exponent for adults was 0.58 for San Elías fish and 0.83 for Ex Hacienda fish, indicating possible ecological effects on this variable. Post-larval fish in Ex Hacienda and all stages in San Elias site showed considerable hypoxia tolerance, with PCrit mean values ranging from 1.9-3.1 kPa, lower than those of many tropical fish at comparable temperatures. Collectively, these data indicate that G. multiradiatus is well adapted for the hypoxia associated with their high-altitude habitat.

Metabolic physiology of the Mayan cichlid fish (Mayaheros uropthalmus): Re-examination of classification as an oxyconformer.

The Mayan cichlid (Mayaheros uropthalmus) is a freshwater fish inhabiting warm, potentially hypoxic and/or brackish waters, in Mexico and Central America. Despite its description as highly hypoxia tolerant, M. uropthalmus has been classified physiologically as an 'oxyconformer', which would place it in a very small (and shrinking) category of fishes that purportedly cannot maintain oxygen consumption (MO2) as ambient PO2 falls. However, hypoxia tolerance is often associated with strong oxyregulation, not oxyconformation as described for M. uropthalmus. To resolve these inconsistencies, we measured MO2, the ambient PO2 at which MO2 begins to decline as PO2 falls (PCrit), and gill ventilation rate (fG) in the Mayan cichlid. Variables were measured at 23o, 28 o and 33 °C and temperature sensitivity (Q10) calculated for each function. MO2 at air saturation was 2.9 ±â€¯0.2, 4.3 ±â€¯0.4, and 5.9 ±â€¯0.3 µmol O2/g/h at 23o, 28o and 33 °C, respectively. PCrits were low at 2.6 ±â€¯0.8 kPa, 3.2 ±â€¯0.8 kPa and 4.7 ±â€¯0.9 kPa at 23o, 28o and 33 °C, respectively. Q10 values for MO2 were 2.56 ±â€¯0.21 (23-28 °C), 1.89 ±â€¯0.15 (28-33 °C) and 2.2 ±â€¯0.1 (full temperature range of 23-33 °C), suggesting overall Q10s typical for tropical freshwater fish. fG was 39 ±â€¯3, 45 ±â€¯4, and 53 ±â€¯6 breaths/min at 23o, 28o and 33 °C, respectively, and increase 2-3 fold in severe hypoxia at each temperature. Experiments employing hyperoxia up to 35 kPa indicate a strong 'hypoxic drive' for gill ventilation. Collectively, these data show that, in contrast to a previous characterization, the Mayan cichlid is a strong oxyregulator exhibiting attributes (e.g. very low PCrit) typical of very hypoxia-tolerant fishes.

Hypoxia-induced developmental plasticity of larval growth, gill and labyrinth organ morphometrics in two anabantoid fish: The facultative air-breather Siamese fighting fish (Betta splendens) and the obligate air-breather the blue gourami (Trichopodus trichopterus).

Larval and juvenile air breathing fish may experience nocturnal and/or seasonal aquatic hypoxia. Yet, whether hypoxia induces respiratory developmental plasticity in larval air breathing fish is uncertain. This study predicted that larvae of two closely related anabantid fish-the facultative air breather the Siamese fighting fish (Betta splendens) and the obligate air breathing blue gourami (Trichopodus trichopterus)-show distinct differences in developmental changes in body, gill, and labyrinth morphology because of their differences in levels of dependency upon air breathing and habitat. Larval populations of both species were reared in normoxia or chronic nocturnal hypoxia from hatching through 35-38 days postfertilization. Gill and labyrinth variables were measured at the onset of air breathing. Betta splendens reared in normoxia possessed larger, more developed gills (~3× greater area) than T. trichopterus at comparable stages. Surface area of the emerging labyrinth, the air breathing organ, was ~ 85% larger in normoxic B. splendens compared to T. trichopterus. Rearing in mild hypoxia stimulated body growth in B. splendens, but neither mild nor severe hypoxia affected growth in T. trichopterus. Condition factor, K (~ 1.3 in B. splendens, 0.7 in T. trichopterus) was unaffected by mild hypoxia in either species, but was reduced by severe hypoxia to <0.9 only in B. splendens. Severe, but not mild, hypoxia decreased branchial surface area in B. splendens by ~40%, but neither hypoxia level affected Trichopodus branchial surface. Mild, but not severe, hypoxia increased labyrinth surface area by 30% in B. splendens. However, as for branchial surface area, labyrinth surface area was not affected in Trichopodus. These differential larval responses to hypoxic rearing suggest that different larval habitats and activity levels are greater factors influencing developmental plasticity than genetic closeness of the two species.

Developmental cardiovascular physiology of the olive ridley sea turtle (Lepidochelys olivacea).

Our understanding of reptilian cardiovascular development and regulation has increased substantially for two species the American alligator (Alligator mississippiensis) and the common snapping turtle (Chelydra serpentina) during the past two decades. However, what we know about cardiovascular maturation in many other species remains poorly understood or unknown. Embryonic sea turtles have been studied to understand the maturation of metabolic function, but these studies have not addressed the cardiovascular system. Although prior studies have been pivotal in characterizing development, and factors that influence it, the development of cardiovascular function, which supplies metabolic function, is unknown in sea turtles. During our investigation we focused on quantifying how cardiovascular morphological and functional parameters change, to provide basic knowledge of development in the olive ridley sea turtle (Lepidochelys olivacea). Embryonic mass, as well as mass of the heart, lungs, liver, kidney, and brain increased during turtle embryo development. Although heart rate was constant during this developmental period, arterial pressure approximately doubled. Further, while embryonic olive ridley sea turtles lacked cholinergic tone on heart rate, there was a pronounced beta adrenergic tone on heart rate that decreased in strength at 90% of incubation. This beta adrenergic tone may be partially originating from the sympathetic nervous system at 90% of incubation, with the majority originating from circulating catecholamines. Data indicates that olive ridley sea turtles share traits of embryonic functional cardiovascular maturation with the American alligator (Alligator mississippiensis) but not the common snapping turtle (Chelydra serpentina).

[Home range of Aspidoscelis cozumela (Squamata: Teiidae): a parthenogenetic lizard microendemic to Cozumel Island, México]. / Ámbito hogareño de Aspidoscelis cozumela (Squamata, Teiidae): una lagartija partenogenética microendémica de Isla Cozumel, México.

Home range is defined as the area within which an individual moves to acquire resources necessary to increase their fitness and may vary inter and intra-specifically with biotic and abiotic factors. This study details the home range of the parthenogenic lizard, Aspidoscelis cozumela, an active forager microendemic to Cozumel Island, México, with high preference for open sand beaches. The home range of A. cozumela was compared with other species of Aspidoscelis (gonochoric and parthenogenetic) and other lizards that occupy coastal habitats. Furthermore, the biotic and abiotic factors that may influence home range were analyzed. This study was conducted in the beach located on the East side of the island (area of 4,000 M2) that is composed primarily of halophyte vegetation with high levels of sunlight. From 1999 to 2001, nine samples were taken which included the dry, rainy, "nortes", and breeding seasons. During each sampling, capture-mark-recapture techniques were conducted and the date, time of day, and snout-vent length (SVL) were recorded to the nearest millimeter. Individuals were located in the study area using a bi-coordinate reference using 10 x 10 m subdivisions of the habitat. Home range and home range overlap were calculated using the convex polygon method in McPaal and home range/SVL correlation was tested using Pearson's correlation. To calculate females home range, three or more recaptures were considered. A total of 20 home ranges that averaged 45.1 ± 14.0 m2 were obtained and no correlation between SVL and home range size was detected (p = 0.9229, n = 20). However, removing individuals with outlier home ranges (females with home ranges > 100 m2, n = 2) resulted in a positive correlation with SVL (r = 0.61, p = 0.0072, n = 18). A 22.9 ± 5.7% overlap in home range was also detected. The small home range of A. cozumela represents the smallest home range within the Aspidoscelis genus recorded to date (including both parthenogenetic and gonochoric species) and contrasts the theoretical predictions of broad home ranges for widely foraging species. Thermoregulatory benefits and a high population density may explain the small home range of A. cozumela. Although this species is highly adapted to the environmental conditions present on the open sand beaches, anthropogenic effects on these habitats by the development of tourism infrastructure may jeopardize their existence on Cozumel Island.

Ámbito hogareño de Aspidoscelis cozumela(Squamata, Teiidae): una lagartija partenogenética microendémica de Isla Cozumel, México / Home range of Aspidoscelis cozumela (Squamata: Teiidae): a parthenogenetic lizard microen-demic to Cozumel Island, México

Home range is defined as the area within which an individual moves to acquire resources necessary to increase their fitness and may vary inter and intra-specifically with biotic and abiotic factors. This study details the home range of the parthenogenic lizard, Aspidoscelis cozumela,an active forager microendemic to Cozumel Island, México, with high preference for open sand beaches. The home range of A. cozumelawas compared with other species of Aspidoscelis(gonochoric and parthenogenetic) and other lizards that occupy coastal habitats. Furthermore, the biotic and abiotic factors that may influence home range were analyzed. This study was conducted in the beach located on the East side of the island (area of 4 000 m2) that is composed primarily of halophyte vegetation with high levels of sunlight. From 1999 to 2001, nine samples were taken which included the dry, rainy, "nortes", and breeding seasons. During each sampling, capture-mark-recapture techniques were conducted and the date, time of day, and snout-vent length (SVL) were recorded to the nearest millimeter. Individuals were located in the study area using a bi-coordinate reference using 10 x 10 m subdivisions of the habitat. Home range and home range overlap were calculated using the convex polygon method in McPaal and home range/SVL correlation was tested using Pearson's correlation. To calculate females home range, three or more recaptures were considered. A total of 20 home ranges that averaged 45.1 ± 14.0 m2 were obtained and no correlation between SVL and home range size was detected (p = 0.9229, n = 20). However, removing individuals with outlier home ranges (females with home ranges > 100 m2, n = 2) resulted in a positive correlation with SVL (r = 0.61, p = 0.0072, n = 18). A 22.9 ± 5.7% overlap in home range was also detected. The small home range of A. cozumelarepresents the smallest home range within the Aspidoscelisgenus recorded to date (including both parthenogenetic and gonochoric species) and contrasts the theoretical predictions of broad home ranges for widely foraging species. Thermoregulatory benefits and a high population density may explain the small home range of A. cozumela.Although this species is highly adapted to the environmental conditions present on the open sand beaches, anthropogenic effects on these habitats by the development of tourism infrastructure may jeopardize their existence on Cozumel Island.

El ámbito hogareño es el área dentro de la cual un individuo se mueve para adquirir recursos que incrementen su supervivencia. El ámbito hogareño puede variar, intra e interespecíficamente, por factores bióticos y abióticos. En este trabajo se estudió el ámbito hogareño de la lagartija partenogenética Aspidoscelis cozumela,una especie de forrajeo amplio, con alta preferencia por las playas y microendémica de Isla Cozumel, México. El ámbito hogareño de A. cozumelase comparó con otras especies de Aspidoscelis(gonocóricas y partenogenéticas) y con otras lagartijas que ocupan hábitats costeros. Además, se discuten los factores bióticos y abióticos que lo moldean. La zona de estudio fue una playa (con un área de 4 000 m2), que se encuentra al Este de la isla y que presenta vegetación halófita (expuesta a altos niveles de insolación). De 1999 al 2001 se realizaron nueve censos que cubrieron la época de sequía, de lluvias y la época de "nortes" de la zona y la temporada de reproducción de A. cozumela.Durante cada censo, se realizó captura-marcaje-recaptura y se registró: fecha, hora del día, longitud hocico-cloaca (LHC) al milímetro más cercano. Los individuos fueron ubicados en el área de estudio por bi-coordenadas usando estacas como referencia. El ámbito hogareño se calculó con el método del polígono convexo con el programa McPaal, adicional-mente se calculó el solapamiento del ámbito hogareño. Se relacionó la LHC con el ámbito hogareño. Para el cálculo del ámbito hogareño se consideraron las hembras con tres o más recapturas. Se obtuvieron 20 ámbitos hogareños, que promediaron 45.1 ± 14.0 m2. No se encontró relación de la LHC con el ámbito hogareño (p = 0.9229, n = 20). Sin embargo, un análisis que excluyó los individuos con los ámbitos hogareños extremos, mostró que el ámbito hogareño de A. cozumelase relacionó de manera positiva con la LHC (p = 0.0072, n = 18), las hembras más grandes tuvieron ámbitos hogareños más amplios. El solapamiento del ámbito hogareño fue de 22.9 ± 5.7%. El ámbito hogareño de A. cozumelaes el más pequeño que se ha documentado en el género Aspidoscelis(incluyendo especies partenoge-néticas y gonocóricas) y se contrapone con las predicciones teóricas que establecen ámbitos hogareños amplios para especies de forrajeo amplio. Beneficios térmicos y una elevada densidad poblacional pueden explicar la marcada residencia en las playas y ámbito hogareño reducido de A. cozumela.La lagartija partenogenética A. cozumelaestá bien adaptada a las condiciones ambientales en las playas, sin embargo las afectaciones severas en las playas por el desarrollo de la infraestructura turística pueden poner en riesgo su existencia en Isla Cozumel.