Temperature-dependent sex-biased embryo mortality in a bird

Sex ratios have important evolutionary consequences and are often biased by environmental factors. The effect of developmental temperature on offspring sex ratios has been widely documented across a diverse range of taxa but has rarely been investigated in birds and mammals. However, recent field observations and artificial incubation experiments have demonstrated that the hatching sex ratio of a megapode, the Australian brush-turkey (Alectura lathami), varied with incubation temperature; more females hatched at high incubation temperatures and more males hatched at low temperatures. Here, we investigated the causes of this temperature-dependent sex-biasing system. Molecular sexing of chicks and embryos confirmed that male embryo mortality was greater at high temperatures while female embryo mortality is greater at low temperatures, with mortality in both sexes similar at intermediate incubation temperatures. Temperature-dependent sex-biased embryo mortality represents a novel mechanism of altering sex ratios in birds. This novel mechanism, coupled with the unique breeding biology of the brush-turkey, offers a potentially unparalleled opportunity in which to investigate sex allocation theory in birds.     

Temperature affects male and female potential reproductive rates differently in the sex-role reversed pipefish, Syngnathus typhle

The differences in potential reproductive rate between the sexescan be used to predict the operational sex ratio and the patternsand intensity of mating competition and hence sexual selectionin a population. This article describes how one environmentalcomponent, temperature, affects potential reproductive ratesof the two sexes in the paternally brooding, sex-role reversedpipefish (Syngnathus typhle). Males brooded embryos much longer(on average 58 days) in cold water (about 10°C) than inwarmer water (35 days at about 15°C). As a consequence,the potential reproductive rate (number of eggs brooded perday) of males was significantly higher in warm water. In females,however, potential reproductive rate, i.e., number of eggs producedper day given an unlimited access to mates, was not significantlydifferent between temperatures. In both sexes, potential reproductiverate was positively related to body size. At both temperatures,females had the potential to reproduce faster than males. Asa result, the operational sex ratio will become female biasedand sex-roles reversed, as is the case in this species. Sincetemperature differently influenced the potential reproductiverates of males and females, with the sexual difference largerat lower temperatures, more intense female-female competitionis predicted at low temperatures.     

Reproductive ecology of the jacky dragon (Amphibolurus muricatus): an agamid lizard with temperature‐dependent sex determination

Abstract The jacky dragon, Amphibolurus muricatus (White, ex Shaw 1790) is a medium sized agamid lizard from the southeast of Australia. Laboratory incubation trials show that this species possesses temperature‐dependent sex determination. Both high and low incubation temperatures produced all female offspring, while varying proportions of males hatched at intermediate temperatures. Females may lay several clutches containing from three to nine eggs during the spring and summer. We report the first field nest temperature recordings for a squamate reptile with temperature‐dependent sex determination. Hatchling sex is determined by nest temperatures that are due to the combination of daily and seasonal weather conditions, together with maternal nest site selection. Over the prolonged egg‐laying season, mean nest temperatures steadily increase. This suggests that hatchling sex is best predicted by the date of egg laying, and that sex ratios from field nests will vary over the course of the breeding season. Lizards hatching from eggs laid in the spring (October) experience a longer growing season and should reach a larger body size by the beginning of their first reproductive season, compared to lizards from eggs laid in late summer (February). Adult male A. muricatus attain a greater maximum body size and have relatively larger heads than females, possibly as a consequence of sexual selection due to male‐male competition for territories and mates. If reproductive success in males increases with larger body size, then early hatching males may obtain a greater fitness benefit as adults, compared to males that hatch in late summer. We hypothesize that early season nests should produce male‐biased sex ratios, and that this provides an adaptive explanation for temperature‐dependent sex determination in A. muricatus.     

Hatching order and sex ratio in Southern Grey Shrike Lanius meridionalis in relation to clutch size

Despite major advances in sex ratio theory, how offspring sex should vary with hatching order remains unclear. We examine nestling sex ratio in the Southern Grey Shrike Lanius meridionalis according to hatching order and clutch size. Southern Grey Shrike nestlings present a different sex ratio with body‐mass rank order depending on clutch size. When the clutch size was five eggs (with a very low risk of brood reduction; 13%) the less costly sex (male) was found at the end of the body mass hierarchy. However, when clutch size was six eggs (with a high risk of brood reduction; 42%) the larger sex (female) was found at intermediate positions in the hatching order, possibly to decrease competitive asymmetries.     

Low temperature has opposite effects on sex determination in a marine fish at the larval/postlarval and juvenile stages

Temperature‐dependent sex determination (TSD) can be observed in multiple reptile and fish species. It is adaptive when varying environmental conditions advantage either males or females. A good knowledge of the thermosensitive period is key to understand how environmental changes may lead to changes in population sex ratio. Here, by manipulating temperature during development, we confirm that cold temperature (16°C) increases the proportion of fish that develop as females in European sea bass (Dicentrarchus labrax) until 56 days posthatching, but show that it has an opposite effect at later stages, with the proportion of males reaching ~90% after 230 days at 16°C. This is the first observation of opposite effects of temperature at different time periods on the sex ratio of a vertebrate. Our results highlight the potential complexity of environmental effects on sex determination.     

Constrained sex allocation in a parasitoid due to variation in male quality

The theory of constrained sex allocation posits that when a fraction of females in a haplodiploid population go unmated and thus produce only male offspring, mated females will evolve to lay a female-biased sex ratio. I examined evidence for constrained sex ratio evolution in the parasitic hymenopteran Uscana semifumipennis. Mated females in the laboratory produced more female-biased sex ratios than the sex ratio of adults hatching from field-collected eggs, consistent with constrained sex allocation theory. However, the male with whom a female mated affected her offspring sex ratio, even when sperm was successfully transferred, suggesting that constrained sex ratios can occur even in populations where all females succeed in mating. A positive relationship between sex ratio and fecundity indicates that females may become sperm-limited. Variation among males occurred even at low fecundity, however, suggesting that other factors may also be involved. Further, a quantitative genetic experiment found significant additive genetic variance in the population for the sex ratio of offspring produced by females. This has only rarely been demonstrated in a natural population of parasitoids, but is a necessary condition for sex ratio evolution. Finally, matings with larger males produced more female-biased offspring sex-ratios, suggesting positive selection on male size. Because the great majority of parasitic hymenoptera are monandrous, the finding of natural variation among males in their capacity to fertilize offspring, even after mating successfully, suggests that females may often be constrained in the sex allocation by inadequate number or quality of sperm transferred.     

Food affects the potential reproductive rates of sand goby females but not of males

The interspawning interval of female sand gobies, Pomatoschistusminutus, a batch-spawning fish with paternal care, was significantlyshorter when the fish were fed daily than when they were fedevery fourth day. The incubation time of males was not affectedby feeding, nor was the interbrood interval Males have an equalor higher potential reproductive rate than females. As femalesreproduce more slowly when food is scarce than when it is abundant,and males do not, the difference between the sexes in potentialreproductive rate increases when there is food shortage. Becauseof this difference, both male bias in operational sex ratioand intensity in male-male competition for mates are predictedto increase as food availability decreases. Furthermore, a tradeoffbetween current and future reproduction is demonstrated to operateonly when resources are limited, because the correlation betweenegg number of the first and second clutch was positive amonghigh-food females but negative among low-food females. The numberof eggs per female clutch did, however, not differ between treatmentsin first or second dutch. I conclude that operational sex ratioand sexual selection are expected to vary within and betweensand goby populations in accordance with prey availability     

The evolution of sexual size dimorphism in the house finch. V. Maternal effects

The phenotype of a mother and the environment that she provides might differentially affect the phenotypes of her sons and daughters, leading to change in sexual size dimorphism. Whereas these maternal effects should evolve to accommodate the adaptations of both the maternal and offspring generations, the mechanisms by which this is accomplished are rarely known. In birds, females adjust the onset of incubation (coincident with the first egg or after all eggs are laid) in response to the environment during breeding, and thus, indirectly, determine the duration of offspring growth. In the two house finch (Carpodacus mexicanus) populations that breed at the extremes of the species' distribution (Montana and Alabama), females experience highly distinct climatic conditions during nesting. We show that in close association with these conditions, females adjusted jointly the onset of incubation and the sequence in which they produced male and female eggs and consequently modified the growth of sons and daughters. The onset of incubation in newly breeding females closely tracked ambient temperature in a pattern consistent with the maintenance of egg viability. Because of the very different climates in Montana and Alabama, females in these populations showed the opposite patterns of seasonal change in incubation onset and the opposite sex bias in egg-laying order. In females with breeding experience, incubation onset and sex bias in laying order were closely linked regardless of the climatic variation. In nests in which incubation began with the onset of egg laying, the first-laid eggs were mostly females in Montana, but mostly males in Alabama. Because in both populations, male, but not female, embryos grew faster when exposed to longer incubation, the sex-bias produced highly divergent sizes of male and female juveniles between the populations. Overall, the compensatory interaction between the onset of incubation and the sex-biased laying order achieved a compromise between maternal and offspring adaptations and contributed to rapid morphological divergence in sexual dimorphism between populations of the house finch breeding at the climatic extremes of the species range.     

Population variation and ecological correlates of tychoparthenogenesis in the mayfly, Stenonema femoratum

Species in which both sex and parthenogenesis co‐occur are extremely valuable for investigating ecological conditions favouring sex. Tychoparthenogenesis is a breeding system characterized by hatching of a small proportion of unfertilized eggs (typically < 10%) from females of sexually reproducing species. With tychoparthenogenesis, both sexual and parthenogenetic reproduction co‐occur within the same population. To identify ecological conditions that may favour this breeding system, I quantified population variation in females’ capacity for tychoparthenogenesis and investigated biotic and abiotic correlates of tychoparthenogenesis. I estimated tychoparthenognetic capacity (proportion of unfertilized eggs hatching) for females from 12 Missouri populations of the mayfly, Stenonema femoratum (Ephemeroptera: Heptageniidae), across three different habitat types – temporary streams, permanent streams and lakes. Tychoparthenogenetic capacity, measured as the population mean hatch success of unfertilized eggs, ranged from 3.8 to 10.7%. Tychoparthenogenetic capacity varied among habitats in 1996, but not in 1997. In 1996, temporary streams showed hatch success of unfertilized eggs twice that of permanent streams and lakes. Tychoparthenogenetic capacity also varied among sampling dates within years. Temporary streams also showed extremely low nymph densities compared to the other two habitats. However, habitats did not differ in adult density. Furthermore, in all populations nymphs showed significantly female‐biased sex ratios. In contrast, adult sex ratios were equal or slightly male biased. Tychoparthenogenetic capacity was negatively correlated with nymph density in 1996, but not in 1997, suggesting possible reproductive assurance in some years. Adult densities also suggested that there may be certain times of year when tychoparthenogenesis may provide benefits of reproductive assurance. Although habitats differed significantly in their abiotic characteristics, tychoparthenogenetic capacity was correlated significantly with water temperature only. © 2002 The Linnean Society of London, Biological Journal of the Linnean Society, 2002, 75 , 101–123.     

Effect of prey density on sex ratio of two predacious mites, Phytoseiulus persimilis and Amblyseius womersleyi (Acari: Phytoseiidae)

The sex ratios of two phytoseiid mites, Phytoseiulus persimilis and Amblyseius womersleyi, were observed under various prey conditions. Upon consumption of abundant prey, both phytoseiids produced progeny in a female-biased sex ratio (approximately 0.8 females). When few prey were consumed, the sex ratio was lowered to 0.5 (the unbiased sex ratio). Under the conditions in which the unbiased sex ratio was observed, male and female progeny appeared in an alternating sequence. To determine the change in the sex ratio and the sequence of progeny, the size of eggs deposited by females under various prey conditions was first compared. Survivorship and developmental rate of progeny (immatures) hatched under ample and poor prey conditions were also examined. The eggs deposited under poor prey conditions were smaller than those deposited under ample prey conditions. This is an indication that the phytoseiid females did not invest extra energy into the eggs to secure survival of their progeny under poor prey conditions. The male and female progeny from the small eggs developed slowly, probably due to the small egg size. However, hatchability of the small eggs and survival of the immatures were the same as those of the normal eggs when the immatures were reared under ample prey conditions. The immature survivorship was little affected by the prey consumption rate of their mothers when the immatures were reared under poor prey conditions. We concluded that the sex ratio of phytoseiid mites is not determined by the characteristics of the progeny, but by the nutritious condition of the females.Exp Appl Acarol 22: 709723 © 1998 Kluwer Academic Publishers     

Antigua revisited: the impact of climate change on sand and nest temperatures at a hawksbill turtle (Eretmochelys imbricata) nesting beach

Whether a turtle embryo develops into a male or a female depends, as with many other reptiles, on the temperature during incubation of the eggs. With sea turtles, warm temperatures produce 100% females. Therefore, global warming has the potential to drastically alter their sex ratios. Air temperatures on Antigua have increased by 0.7°C over the last 35 years. Measurements in both the sand and the clutches laid by hawksbill turtles (Eretmochelys imbricata) at Pasture Bay, Antigua, show that for important parts of the nesting season temperatures are already above the level producing 50% of each sex (pivotal level). Comparisons are made to sand temperature measurements taken on this beach in 1989 and 1990. It is estimated that fewer males were produced in 2003 than in the previous years. Recommendations are made for close monitoring of the fertility of eggs and for research on any turtles nesting at cooler times of year.     

Long-lasting fitness consequences of prenatal sex ratio in a viviparous lizard

Maternal effects and early environmental conditions are important in shaping offspring developmental trajectories. For example, in laboratory mammals, the sex ratio during gestation has been shown to influence fitness-related traits via hormonal interaction between fetuses. Such effects have the potential to shape, or constrain, many important aspects of the organism's life, but their generality and importance in natural populations remain unknown. Using long-term data in a viviparous lizard, Lacerta vivipara, we investigated the relationship between prenatal sex ratio and offspring growth, survival, and reproductive traits as adults. Our results show that females from male-biased clutches grow faster, mature earlier, but have lower fecundity than females from female-biased clutches. Furthermore, male reproduction was also affected by the sex ratio during embryonic development, with males from male-biased clutches being more likely to successfully reproduce at age one than males from female-biased clutches. Thus, the sex ratio experienced during gestation can have profound and long-lasting effects on fitness in natural populations of viviparous animals, with important implications for life-history evolution and sex allocation.     

Temperature affects operational sex ratio and intensity of male-male competition: an experimental study of sand gobies, Pomatoschistus minutus

The operational sex ratio is intimately related to the intensityof sexual selection, but factors governing variation in theoperational sex ratio and their effects on mating competitionare still poorly understood. In this study, temperature wasfound to affect both the operational sex ratio and the intensityof male-male competitive interactions in the sand goby [Pomatoschistusminutus (Pallas)]. In an experiment with two different temperaturetreatments, the operational sex ratio became male biased inthe warm treatment (15°C) and males in that treatment interactedmore frequendy than in the cold treatment (8.5°C). Theseresults were as predicted since the potential reproductive rateof males increases faster with temperature than does the potentialreproductive rate of females. Thus, an environmental factor,water temperature, affects not only the reproductive rates ofthe sexes, but also the operational sex ratio and mating competition,and thereby the intensity of sexual selection. Operational sexratio was not found to be correlated with male behavior. Thismay suggest a direct effect of temperature or potential reproductiverates on mate competition. The mechanism behind the evolutionof such a direct relationship would, however, probably be theimpact of potential reproductive rates on operational sex ratio,which in turn direcdy affects sexual selection.     

Latitudinal differences in temperature effects on the embryonic development and hatchling phenotypes of the Asian yellow pond turtle,Mauremys mutica

The effect of incubation temperature on embryonic development and offspring traits has been widely reported for many species. However, knowledge remains limited about how such effects vary across populations. Here, we investigated whether incubation temperature (26, 28, and 30 °C) differentially affects the embryonic development of Asian yellow pond turtle (Mauremys mutica) eggs originating from low‐latitude (Guangzhou, 23°06′N) and high‐latitude (Haining, 30°19′N) populations in China. At 26 °C, the duration of incubation was shorter in the high‐latitude population than in the low‐latitude population. However, this pattern was reversed at 30 °C. As the incubation temperature increased, hatching success increased in the low‐latitude population but slightly decreased in the high‐latitude population. Hatchlings incubated at 30 °C were larger and righted themselves more rapidly than those incubated at 26 °C in the low‐latitude population. In contrast, hatchling traits were not influenced by incubation temperature in the high‐latitude population. Overall, 30 °C was a suitable developmental temperature for embryos from the low‐latitude population, whereas 26 and 28 °C were suitable for those from the high‐latitude population. This interpopulation difference in suitable developmental temperatures is consistent with the difference in the thermal environment of the two localities. Therefore, similarly to posthatching individuals, reptile embryos from different populations might have evolved diverse physiological strategies to benefit from the thermal environment in which they develop. © 2014 The Linnean Society of London, Biological Journal of the Linnean Society, 2014, 114 , 35–43.     

The transition from sitting on eggs to sitting on young in ring doves, Streptopelia risoria: squab-egg preferences during the normal cycle.

Ring doves of both sexes sit on young squabs after hatching in much the same manner as they sit on eggs before hatching, but this study demonstrates that the preferred stimulus varies with the state of the animal. A simultaneous, squab-egg choice test was given on days 1, 4, 10, and 13 of incubation and on the day following hatching in normal reproductive cycles of experienced and naïve male and female ring doves. Naïve doves were more likely than experienced doves to choose eggs throughout the cycle (P<0·005) and, overall, eggs were more likely to be chosen during early incubation and squabs posthatching (P<0·005).     

Adaptive seasonal trend in brood sex ratio: test in two sister species with contrasting breeding systems

Evolutionary theory predicts adaptive adjustment in offspring sex ratio by females. Seasonal change in sex ratio is one possibility, tested here in two sister species, the Common sandpiper and the Spotted sandpiper Actitis hypoleucos and A. macularia. In the monogamous Common sandpiper, males are the most competitive sex. In each of 3 years, there was a change from mainly sons in early clutches to mainly daughters in late clutches. This seasonal adjustment of clutch sex ratio took place within the female before the eggs were laid, not by differential egg or chick survival. The sex of all eggs laid in the clutches used here was determined molecularly from chick blood taken at the time of hatching. The Spotted sandpiper in contrast is polyandrous, with partly reversed sex roles. There was no seasonal trend from sons to daughters in this species. When tested together, the two species differed significantly as predicted by the hypothesis of adaptive sex ratio adjustment by females.     

Brood sex ratio in the Kentish plover

How and why do the mating opportunities of males and femalesdiffer in natural population of animals? Previously we showedthat females have higher mating opportunities than males inthe Kentish plover Charadrius alexandrinus. Both parents incubatethe eggs, and males provide more brood care than females; thusit is not obvious why the females find new mates sooner thanthe males. In this study we investigated whether the sex-biasedmating opportunities stem from biased offspring sex ratios.We determined the sex of newly hatched, precocial chicks usingCHD gene markers. Among fully sexed broods, 0.461 ± 0.024(SE) of chicks (454 chicks in 158 broods) were male, and thissex ratio was not significantly different from unity. The proportionof males at hatching decreased significantly over the breedingseason, which occurred consistently in all 3 years of the study.Large chicks were more likely to be males than females. Neitherparental age nor body size of male and female parents was relatedto brood sex ratio. We also sexed a number of chicks that werecaught after they left their nest (range of estimated ages 0–17days) and found that the proportion of males increased withbrood age. This relationship remained highly significant whencontrolling statistically for hatching date. As brood size decreaseddue to mortality after the chicks left their nest, these resultssuggest that the mortality of daughters was higher than thatof the sons shortly after hatching. Taken together, our resultsshow that the female-biased mating opportunities in the Kentishplover are not due to biased brood sex ratio at hatching but,at least in part, are due to female-biased chick mortality soonafter hatching.     

Complex sex allocation in the laughing kookaburra

In groups of the cooperatively breeding laughing kookaburra(Dacelo novaeguineae), offspring sex varied with the type ofsocial group and with hatch rank. Groups with female helpers,especially if all helpers were female, had male-biased clutchand fledging sex ratios. Groups without female helpers (unassistedpairs or male-only helpers) had female-biased clutch and fledgingsex ratios. Breeding females responded facultatively to increasesin the number of female helpers in their group by producingmore male eggs. These biases may occur if breeding femalestry to limit the number of daughters recruited into their groupbecause unlike male helpers, female helpers depress the breedingsuccess of their parents. Across all nests, two-thirds of first-hatchedyoung were male, two-thirds of second-hatched young were female, and the sex ratio of third-hatched young was even. Hatch ranksex ratios also varied dramatically between different typesof social groups, from 16.7% for second-hatched nestlings ofunassisted pairs to 100% for first-hatched nestlings of groupswith only female helpers. A corollary of the relationship betweenhatch rank and sex was that hatching sex sequences were distributed nonrandomly: all groups avoided hatching a daughter first followedby a son (FM). Sibling competition is aggressive and sometimesfatal. Since females grow to be 15% larger than males the hatchingsequence of sexes could affect nestling growth and mortality.However, an exhaustive analysis found little evidence thatgrowth or survival of males was compromised if hatched aftera sister. The small number of FM sequences may only have occurredin nests that were able to ameliorate any negative consequences.Alternatively, when clutch size is small and fledging successunpredictable because of brood reduction, the preferred broodsex ratio may be contingent on the number of fledged young,making it advantageous to order the sexes in the brood.