Reconstruction of paternal genotypes over multiple breeding seasons reveals male green turtles do not breed annually (original) (raw)
Related papers
Frontiers in Marine Science, 2014
The implications of climate change for global biodiversity may be profound with those species with little capacity for adaptation being thought to be particularly vulnerable to warming. A classic case of groups for concern are those animals exhibiting temperature-dependent sex-determination (TSD), such as sea turtles, where climate warming may produce single sex populations and hence extinction. We show that, globally, female biased hatchling sex ratios dominate sea turtle populations (exceeding 3:1 in >50% records), which, at-a-glance, reiterates concerns for extinction. However, we also demonstrate that more frequent breeding by males, empirically shown by satellite tracking 23 individuals and supported by a generalized bio-energetic life history model, generates more balanced operational sex ratios (OSRs). Hence, concerns of increasingly skewed hatchling sex ratios and reduced population viability are less acute than previously thought for sea turtles. In fact, in some scenarios skewed hatchling sex ratios in groups with TSD may be adaptive to ensure optimum OSRs.
2010
Species that have temperature-dependent sex determination (TSD) often produce highly skewed offspring sex ratios contrary to long-standing theoretical predictions. This ecological enigma has provoked concern that climate change may induce the production of single-sex generations and hence lead to population extirpation. All species of sea turtles exhibit TSD, many are already endangered, and most already produce sex ratios skewed to the sex produced at warmer temperatures (females). We tracked male loggerhead turtles ( Caretta caretta) from Zakynthos, Greece, throughout the entire interval between successive breeding seasons and identified individuals on their breeding grounds, using photoidentification, to determine breeding periodicity and operational sex ratios. Males returned to breed at least twice as frequently as females. We estimated that the hatchling sex ratio of 70:30 female to male for this rookery will translate into an overall operational sex ratio (OSR) (i.e., ratio of total number of males vs females breeding each year) of close to 50:50 female to male. We followed three male turtles for between 10 and 12 months during which time they all traveled back to the breeding grounds. Flipper tagging revealed the proportion of females returning to nest after intervals of 1, 2, 3, and 4 years were 0. 21, 0.38, 0.29, and 0.12, respectively (mean interval 2.3 years). A further nine male turtles were tracked for short periods to determine their departure date from the breeding grounds. These departure dates were combined with a photoidentification data set of 165 individuals identified on in-water transect surveys at the start of the breeding season to develop a statistical model of the population dynamics. This model produced a maximum likelihood estimate that males visit the breeding site 2.6 times more often than females (95%CI 2.1, 3.1), which was consistent with the data from satellite tracking and flipper tagging. Increased frequency of male breeding will help ameliorate female-biased hatchling sex ratios. Combined with the ability of males to fertilize the eggs of many females and for females to store sperm to fertilize many clutches, our results imply that effects of climate change on the viability of sea turtle populations are likely to be less acute than previously suspected.
Female sea turtles are promiscuous, with clutches of eggs often sired by multiple males and rates of multiple paternity varying greatly within and across species. We investigated levels of multiple paternity in loggerhead sea turtles (Caretta caretta) from three rookeries in Western Australia by analysing polymorphic species-specific genetic markers. We predicted that the level of multiple paternity would be related to female population size and hence the large rookery at Dirk Hartog Island would have higher rates of multiple paternity than two smaller mainland rookeries at Gnaraloo Bay and Bungelup Beach. Contrary to our prediction, we found highly variable rates of multiple paternity among the rookeries that we sampled, which was unrelated to female population size (25% at Bungelup Beach, 86% at Gnaraloo Bay, and 36% at Dirk Hartog Island). Approximately 45 different males sired 25 clutches and the average number of sires per clutch ranged from 1.2 to 2.1, depending on the rookery sampled. The variance in rates of multiple paternity among rookeries suggests that operational sex ratios are variable in Western Australia. Periodic monitoring would show whether the observed patterns of multiple paternity for these three rookeries are stable over time, and our data provide a baseline for detecting shifts in operational sex ratios.
Marine Biology
In a warming climate, male sea turtles may become increasingly rare due to temperature-dependent sex determination with females being produced at warmer temperatures. Hence there is widespread concern that a lack of adult males may impact population viability. However, there is controversy over this scenario and here we review aspects of the biology of male sea turtles that will help mitigate female-biased hatchling sex ratios. In particular, there is strong evidence that males generally breed more frequently than females (i.e. have a shorter remigration interval) and that individual breeding males actively search for females and may mate with multiple females from different nesting sites. These aspects of the biology of male turtles will cause female-biased hatchling sex ratios to translate into more balanced adult sex ratios on the breeding grounds (i.e. operational sex ratios). Sexual dimorphism is widespread with adult male turtles generally being smaller than females. In freshw...
Within-season shifts in multiple paternity patterns in mass-nesting olive ridley sea turtles
Endangered Species Research, 2021
ABSTRACT: Multiple paternity is common to all sea turtle species, but its causes and consequences are hard to ascertain and the behaviors and success of males difficult to observe. This study aims to describe patterns of multiple paternity for olive ridley turtles Lepidochelys olivacea at Playa de Escobilla, an ‘arribada’ (mass-nesting) site on the Mexican Pacific coast with over a million clutches laid each reproductive season. A total of 15 females and their hatchlings were sampled during 3 arribada events which occurred over the 2016−2017 nesting season. Females and hatchlings (N = 329) were genotyped at 5 microsatellite loci, from which we inferred the alleles of 46 contributing males. multiple paternity was detected in 60% of the analyzed clutches, which were sired by a range of 2 to 7 males. Multiple paternity rates differed significantly across arribada events, suggesting more males achieved fertilizations earlier in the breeding season. Paternal contribution in 6 of the clutches with multiple paternity was skewed towards a single male; the remaining clutches had a homogeneous male contribution. However, our results are based on relatively small within-arribada sample sizes. The frequency of multiple paternity among turtle clutches laid on this arribada beach could be related to the density of breeding individuals in the reproductive patch off Playa de Escobilla, rather than to the nesting population size or female size
Animal Conservation, 2012
The long-term survival of species with temperature-dependant sex determination requires a sufficient range of incubation temperatures to ensure that both males and females are produced. The primary sex ratio of sea turtles is determined by the temperature experienced by eggs during the middle third of incubation. Here, we investigated the variability in the production of male and female offspring by loggerhead sea turtles Caretta caretta at six nesting beaches in the temperate breeding area of Zakynthos, Greece. Hatchling sex ratios were estimated using incubation durations and sand temperatures for
Conservation Biology, 2010
Abstract: Species that have temperature-dependent sex determination (TSD) often produce highly skewed offspring sex ratios contrary to long-standing theoretical predictions. This ecological enigma has provoked concern that climate change may induce the production of single-sex generations and hence lead to population extirpation. All species of sea turtles exhibit TSD, many are already endangered, and most already produce sex ratios skewed to the sex produced at warmer temperatures (females). We tracked male loggerhead turtles (Caretta caretta) from Zakynthos, Greece, throughout the entire interval between successive breeding seasons and identified individuals on their breeding grounds, using photoidentification, to determine breeding periodicity and operational sex ratios. Males returned to breed at least twice as frequently as females. We estimated that the hatchling sex ratio of 70:30 female to male for this rookery will translate into an overall operational sex ratio (OSR) (i.e., ratio of total number of males vs females breeding each year) of close to 50:50 female to male. We followed three male turtles for between 10 and 12 months during which time they all traveled back to the breeding grounds. Flipper tagging revealed the proportion of females returning to nest after intervals of 1, 2, 3, and 4 years were 0.21, 0.38, 0.29, and 0.12, respectively (mean interval 2.3 years). A further nine male turtles were tracked for short periods to determine their departure date from the breeding grounds. These departure dates were combined with a photoidentification data set of 165 individuals identified on in-water transect surveys at the start of the breeding season to develop a statistical model of the population dynamics. This model produced a maximum likelihood estimate that males visit the breeding site 2.6 times more often than females (95%CI 2.1, 3.1), which was consistent with the data from satellite tracking and flipper tagging. Increased frequency of male breeding will help ameliorate female-biased hatchling sex ratios. Combined with the ability of males to fertilize the eggs of many females and for females to store sperm to fertilize many clutches, our results imply that effects of climate change on the viability of sea turtle populations are likely to be less acute than previously suspected.Resumen: Las especies que tienen determinación de sexo dependiente de la temperatura (DST) a menudo producen proporciones de sexo en su descendencia muy sesgadas contrarias las predicciones teóricas prevalecientes. Este enigma ecológico ha motivado preocupación de que el cambio climático puede inducir la producción de generaciones de un solo sexo y por lo tanto conducir a la extirpación de la población. Todas las especies de tortugas marinas presentan DST, muchas ya están en peligro y la mayoría ya producen proporciones de sexos sesgados hacia el sexo producido a temperaturas más cálidas (hembras). Rastreamos tortugas de carey machos (Caretta caretta) de Zakynthos, Grecia, a lo largo de todo el intervalo entre épocas reproductivas sucesivas e identificamos individuos en sus áreas reproductivas, utilizando fotoidentificación, para determinar la periodicidad reproductiva y las proporciones de sexo operacionales. Los machos retornaron para reproducirse por lo menos dos veces más frecuentemente que las hembras. Estimamos que la proporción de sexos de crías de 70:30 hembras a machos en esta colonia se traducirá en una proporción de sexos operacional (PSO) (i.e., la proporción del número total de machos versus hembras en reproducción cada año) cerca de 50:50 hembras a machos. Seguimos a 3 tortugas machos entre 10 y 12 meses durante los cuales todos retornaron al área reproductiva. El marcaje en aletas reveló que la proporción de hembras que retornaron a anidar después de intervalos de 1, 2, 3 y 4 años fue 0.21, 0.38, 0.29 y 0.12, respectivamente (intervalo promedio 2.3 años). Otros 9 machos fueron rastreados por períodos cortos para determinar su fecha de partida del área reproductiva. Esas fechas de partida fueron combinadas con un conjunto datos de la fotoidentificación de 165 individuos identificados en transectos realizados al inicio de la época reproductiva para desarrollar un modelo estadístico de la dinámica poblacional. Este modelo produjo una probabilidad máxima estimada de que los machos visitan el área reproductiva 2.6 veces más a menudo que las hembras (95%IC 2.1, 3.1), que fue consistente con los datos de rastreo por satélite y marcaje de aletas. Una mayor frecuencia de la reproducción de machos ayudará a mejorar las proporciones de sexo de crías sesgadas hacia hembras. En combinación con la habilidad de los machos para fertilizar los huevos de muchas hembras y de las hembras para almacenar esperma para fertilizar muchas puestas, nuestros resultados implican que es probable que los efectos del cambio climático sobre la viabilidad de las poblaciones de tortugas marinas sean menos agudos que lo sospechado previamente.Resumen: Las especies que tienen determinación de sexo dependiente de la temperatura (DST) a menudo producen proporciones de sexo en su descendencia muy sesgadas contrarias las predicciones teóricas prevalecientes. Este enigma ecológico ha motivado preocupación de que el cambio climático puede inducir la producción de generaciones de un solo sexo y por lo tanto conducir a la extirpación de la población. Todas las especies de tortugas marinas presentan DST, muchas ya están en peligro y la mayoría ya producen proporciones de sexos sesgados hacia el sexo producido a temperaturas más cálidas (hembras). Rastreamos tortugas de carey machos (Caretta caretta) de Zakynthos, Grecia, a lo largo de todo el intervalo entre épocas reproductivas sucesivas e identificamos individuos en sus áreas reproductivas, utilizando fotoidentificación, para determinar la periodicidad reproductiva y las proporciones de sexo operacionales. Los machos retornaron para reproducirse por lo menos dos veces más frecuentemente que las hembras. Estimamos que la proporción de sexos de crías de 70:30 hembras a machos en esta colonia se traducirá en una proporción de sexos operacional (PSO) (i.e., la proporción del número total de machos versus hembras en reproducción cada año) cerca de 50:50 hembras a machos. Seguimos a 3 tortugas machos entre 10 y 12 meses durante los cuales todos retornaron al área reproductiva. El marcaje en aletas reveló que la proporción de hembras que retornaron a anidar después de intervalos de 1, 2, 3 y 4 años fue 0.21, 0.38, 0.29 y 0.12, respectivamente (intervalo promedio 2.3 años). Otros 9 machos fueron rastreados por períodos cortos para determinar su fecha de partida del área reproductiva. Esas fechas de partida fueron combinadas con un conjunto datos de la fotoidentificación de 165 individuos identificados en transectos realizados al inicio de la época reproductiva para desarrollar un modelo estadístico de la dinámica poblacional. Este modelo produjo una probabilidad máxima estimada de que los machos visitan el área reproductiva 2.6 veces más a menudo que las hembras (95%IC 2.1, 3.1), que fue consistente con los datos de rastreo por satélite y marcaje de aletas. Una mayor frecuencia de la reproducción de machos ayudará a mejorar las proporciones de sexo de crías sesgadas hacia hembras. En combinación con la habilidad de los machos para fertilizar los huevos de muchas hembras y de las hembras para almacenar esperma para fertilizar muchas puestas, nuestros resultados implican que es probable que los efectos del cambio climático sobre la viabilidad de las poblaciones de tortugas marinas sean menos agudos que lo sospechado previamente.
The Maternal Legacy: Female Identity Predicts Offspring Sex Ratio in the Loggerhead Sea Turtle
Scientific Reports, 2016
In organisms with temperature-dependent sex determination, the incubation environment plays a key role in determining offspring sex ratios. Given that global temperatures have warmed approximately 0.6 °C in the last century, it is necessary to consider how organisms will adjust to climate change. To better understand the degree to which mothers influence the sex ratios of their offspring, we use 24 years of nesting data for individual female loggerhead sea turtles (Caretta caretta) observed on Bald Head Island, North Carolina. We find that maternal identity is the best predictor of nest sex ratio in univariate and multivariate predictive models. We find significant variability in estimated nest sex ratios among mothers, but a high degree of consistency within mothers, despite substantial spatial and temporal thermal variation. Our results suggest that individual differences in nesting preferences are the main driver behind divergences in nest sex ratios. As such, a female's ability to plastically adjust her nest sex ratios in response to environmental conditions is constrained, potentially limiting how individuals behaviorally mitigate the effects of environmental change. Given that many loggerhead populations already show female-biased offspring sex ratios, understanding maternal behavioral responses is critical for predicting the future of long-lived species vulnerable to extinction.
Molecular Ecology, 2013
Postcopulatory sperm storage can serve a range of functions, including ensuring fertility, allowing delayed fertilization and facilitating sexual selection. Sperm storage is likely to be particularly important in wide-ranging animals with low population densities, but its prevalence and importance in such taxa, and its role in promoting sexual selection, are poorly known. Here, we use a powerful microsatellite array and paternal genotype reconstruction to assess the prevalence of sperm storage and test sexual selection hypotheses of genetic biases to paternity in one such species, the critically endangered hawksbill turtle, Eretmochelys imbricata. In the majority of females (90.7%, N = 43), all offspring were sired by a single male. In the few cases of multiple paternity (9.3%), two males fertilized each female. Importantly, the identity and proportional fertilization success of males were consistent across all sequential nests laid by individual females over the breeding season (up to five nests over 75 days). No males were identified as having fertilized more than one female, suggesting that a large number of males are available to females. No evidence for biases to paternity based on heterozygosity or relatedness was found. These results indicate that female hawksbill turtles are predominantly monogamous within a season, store sperm for the duration of the nesting season and do not re-mate between nests. Furthermore, females do not appear to be using sperm storage to facilitate sexual selection. Consequently, the primary value of storing sperm in marine turtles may be to uncouple mating and fertilization in time and avoid costly re-mating.
High frequency of multiple paternity in the largest rookery of Mediterranean loggerhead sea turtles
2007
Mating systems are a central component in the evolution of animal life histories and in conservation genetics. The patterns of male reproductive skew and of paternal shares in batches of offspring, for example, affect genetic effective population size. A prominent characteristic of mating systems of sea turtles seem to be a considerable intra-and interspecific variability in the degree of polyandry. Because of the difficulty of observing the mating behaviour of sea turtles directly in the open sea, genetic paternity analysis is particularly useful for gaining insights into this aspect of their reproductive behaviour. We investigated patterns of multiple paternity in clutches of loggerhead sea turtles in the largest Mediterranean rookery using four highly variable microsatellite loci. Furthermore, we tested for a relationship between the number of fathers detected in clutches and body size of females. More than one father was detected in the clutches of 14 out of 15 females, with two clutches revealing the contribution of at least five males. In more than half the cases, the contributions of different fathers to a clutch did not depart from equality. The number of detected fathers significantly increased with increasing female body size. This relationship indicates that males may prefer to mate with large, and therefore productive, females. Our results suggest that polyandry is likely to increase effective population size compared to a population in which females would mate with only one male; male reproductive contributions being equal.