Female Life History Research Articles

Variations in female swordtip squid Uroteuthis edulis life history traits between southern Japan and northern Taiwan (Northwestern Pacific)

Swordtip squid Uroteuthis edulis is a commercially important species in coastal waters throughout the Northwestern Pacific, including those of Japan and Taiwan. Despite the importance of U. edulis to fisheries, previous studies on the life history traits (growth rate, size at maturity, and fecundity) of its populations in the Northwestern Pacific have been localized and region specific. Thus, we report life history traits of female swordtip squid from the waters off southern Japan and northern Taiwan, to identify seasonal variations within each population, as well as geographical variations between them. Variations in life history traits, including growth rate, mantle length (ML) at maturity, and female reproductive traits (gonadosomatic index, fecundity and egg size), are described and recognized to vary seasonally in both populations. Winter spawners in Japan have the highest growth rate, followed by spring spawners and summer spawners. Spring spawners in Taiwan mature at a younger age than autumn spawners. Geographical variations between populations are reported: fecundity level and egg size of spring spawners in Japan differ from those of spring and autumn spawners in Taiwan, but those of summer spawners in Japan are similar to those of spring and autumn spawners in Taiwan. Data on seasonal and geographical variations in life history traits of U. edulis are useful for effective squid fisheries management.

Weak relationships of parasite infection with sexual and life‐history traits in wild‐caught Texas field crickets (Gryllus texensis)

Sex differences in immune investment and infection rate are predicted due to the divergent life histories of males and females, where females invest more toward immunity due to the fitness consequences of a reduced lifespan and males allocate less toward immunity due to increased resource investment in traits critical to sexual selection. Consequently, males are expected to fight infection less adeptly, resulting in higher parasite loads relative to females across all taxa. Wild animals rarely face a single parasite within their given environment, yet nearly all studies on sex‐biased infection rates have focused on a single host–parasite relationship. Here, we investigate how simultaneous natural infections of ecto‐ and endosymbionts (i.e. both parasitic and phoretic taxa) correlate with sex biases in host immune response and reproductive investment in a field‐caught cricket, Gryllus texensis. Our comprehensive analysis found no significant sex differences in two measures of immune response (melanization and nodulation), and found no strong evidence of a sex bias in the prevalence or intensity of parasitism by the three most common parasites infecting wild G. texensis field crickets (Eutrombidiidae, gregarines, and nematodes). Two traits related to female fitness, egg number and egg size, showed no relation to parasitic infection; however, males having wider heads and poorer body condition were significantly more infected by eutrombidiid mites, gregarines, and nematodes. Despite frequent predictions of male‐biased parasitism in the literature, our results concur with many other studies indicating that the divergent life histories of males and females alone are not sufficient to explain natural infection rates in wild insects.

Mating in the absence of fertilization promotes a growth-reproduction versus lifespan trade-off in female mice

Trade-offs between growth, reproduction, and lifespan constrain animal life histories, leading to evolutionary diversification of life history cycles in different environments. In female mammals, gestation and lactation are expected to impose the major costs of reproduction, driving reproductive trade-offs, although mating also requires interactions with males that could themselves influence life history. Here we show that a male's presence by itself leads to lifelong alterations in life history in female mice. Housing C57BL/6J female mice with sterilized males early in life led to an increase in body weight, an effect that persisted across life even when females were later allowed to produce pups. We found that those females previously housed with sterile males also showed enhanced late-life offspring production when allowed to reproduce, indicating that earlier mating can influence subsequent fecundity. This effect was the opposite to that seen in females previously housed with intact males, which showed the expected trade-off between early-life and late-life reproduction. However, housing with a sterile male early in life came at a cost to lifespan, which was observed in the absence of females ever undergoing fertilization. Endocrinologically, mating also permanently reduced the concentration of circulating prolactin, a pituitary hormone influencing maternal care. Changes in hormone axes that influence reproduction could therefore help alter life history allocation in response to opposite-sex stimuli. Our results demonstrate that mating itself can increase growth and subsequent fecundity in mammals, and that responses to sexual stimuli could account for some lifespan trade-offs normally attributed to pregnancy and lactation.

Plasticity in male mating behavior modulates female life history in fruit flies

In many species, intense male-male competition for the opportunity to sire offspring has led to the evolution of selfish reproductive traits that are harmful to the females they mate with. In the fruit fly, Drosophila melanogaster, males modulate their reproductive behavior based on the perceived intensity of competition in their premating environment. Specifically, males housed with other males subsequently transfer a larger ejaculate during a longer mating compared to males housed alone. Although the potential fitness benefits to males from such plasticity are clear, its effects on females are mostly unknown. Hence, we tested the long-term consequences to females from mating with males with distinct social experiences. First, we verified that competitive experience influences male mating behavior and found that males housed with rivals subsequently have shorter mating latencies and longer mating durations. Then, we exposed females every other day for 20 days to males that were either housed alone or with rivals, and subsequently measured their fitness. We found that females mated to males housed with rivals produce more offspring early in life but fewer offspring later in life and have shorter lifespans but similar intrinsic population growth rates. These results indicate that plasticity in male mating behavior can influence female life histories by altering females' relative allocation to early versus late investment in reproduction and survival.

Multiple traits and multifarious environments: integrated divergence of morphology and life history

Understanding complex responses of multiple character suites (e.g. behaviour, life history, morphology) across multifarious environments is a challenging task. Here we use a multivariate approach (partial least squares structural equation modelling) to disentangle environmental drivers (i.e. predation, resource availability and population demographics) of population divergence in life history and morphology. We further employ a two‐block partial least squares analysis in a novel approach to uncovering integrated and independent aspects of divergence in correlated character suites. Examining Bahamas mosquitofish Gambusia hubbsi inhabiting blue holes, we found phenotypic divergence mainly resulted from differences in predation regimes, but demography and resources also proved important in particular aspects of divergence. We uncovered significant covariation among life histories and morphologies, and revealed that phenotypic divergence between predation regimes involved both integrated and independent responses. For instance, female life histories strongly diverged independently of morphology, while some morphological shifts (abdominal distension) resulted from changes in fecundity; males showed strong morphological divergence independent of life history, but much of their life‐history shifts reflected joint morphological changes (lean weight and body shape). Our study illustrates the utility of gathering disparate data types from multiple populations/species to better understand the causes and nature of phenotypic divergence in the wild.

Nutritional composition of the diet of the western gorilla (Gorilla gorilla): Interspecific variation in diet quality.

To meet nutritional needs, primates adjust their diets in response to local habitat differences, though whether these dietary modifications translate to changes in dietary nutrient intake is unknown. A previous study of two populations of the mountain gorilla (MG: Gorilla beringei) found no evidence for intraspecific variation in the nutrient composition of their diets, despite ecological and dietary differences between sites. One potential explanation is that nutritional variability in primate diets requires greater ecological divergence than what was captured between MG sites, underpinning environmental differences in the nutrient quality of plant foods. To test whether Gorilla exhibits interspecific variation in dietary composition and nutrient intake, we studied the composition and macronutrients of the western gorilla (WG: Gorilla gorilla) staple diets and compared them with published data from the two MG populations. We recorded feeding time and food intake of four adult female WGs from one habituated group over a period of 11 months (December 2004-October 2005) at the Mondika Research Center, Republic of Congo, allowing for assessment of seasonal patterns of nutrient intake. Staple diets of WGs and MGs diverged in their dietary and macronutrient composition. Compared to MGs, the staple diet of WGs (by intake) contained higher proportions of fruit (43%) and leaf (12%) and a lower proportion of herb (39%), resulting in a higher intake of total nonstructural carbohydrate and fiber and a lower intake of crude protein. Staple gorilla fruits and herbs differed in nutrient quality between sites. Gorillas exhibit nutritional flexibility that reflects ecological variation in the nutrient quality of plant foods. Since dietary quality typically affects rates of growth and reproduction in primates, our results suggest that interspecific differences in nutrient intake and food quality may shape differences in gorilla nutrient balancing and female life history strategies.

Sperm number assessed by flow cytometry in species of Daphnia (Crustacea, Cladocera)

AbstractDaphnia magna and Daphnia pulex are two important model species in ecotoxicology. In daphniids, studies of the effects of contaminants have mostly focused on female life history traits, yet it would also be important to examine male reproductive traits, particularly in relation to endocrine disruptors. In this study, we developed a protocol that uses flow cytometry to measure sperm number in individual males of different species of Daphnia. We tested our protocol on 114 males from several clones of three common species of Daphnia. Sperm count varied widely among individuals and reached high numbers (up to 1.45 × 105). Positive relationships between male length and sperm number were observed in D. pulex and Daphnia pulicaria, but not in D. magna. Important inter‐clonal differences in sperm production were observed in all species, with some clones producing very little sperm. Duplicated sperm samples showed on average only 6% difference in sperm counts. Sperm counts were stable at least over a 2‐hr period and up to 5 hr for most samples. This sperm isolation protocol and flow cytometric enumeration approach will be of major interest to ecotoxicologists.

Plasticity, state-dependency, and individual consistency in Canada goose nest defense behavior

Animals are thought to adjust the intensity of their parental defense to fitness benefits associated with their current reproduction. They should be more defensive when they breed early in the season, when they produce more young, or as their young get older. Beyond these plastic changes, associations among traits could be explained by consistent among-individual differences. Separating the mechanisms at the origin of behavioral phenotypic variation is essential to understand the determinants and evolution of parental care. During four breeding seasons, we investigated whether variation in Canada goose (Branta canadensis) nest defense resulted from individual short-term plastic adjustments to reproductive stage within breeding seasons, plastic adjustments to brood value across breeding seasons, or from long-term among-individual differences. We thus estimated the among- and within-individual relationships between nest defense, clutch size, and laying date. Female and male nest defense behaviors were highly repeatable in time (R = 0.72 and 0.67 on the short term). At the among-individual level, we found no significant association between female nest defense and life history traits, but the more defensive males were mated with the more fecund females. Female and male nest defense was not adjusted to annual variation in laying date nor in clutch size. However, females adjusted their nest defense within each breeding season and became more defensive when approaching egg hatching. Thus, Canada goose nest defense behavior is partly explained by plastic adjustments, but also by consistent among-individual differences which indicate the evolutionary potential of nest defense behavior. An association between traits at the phenotypic level can be partitioned into association at the among- and within-individual levels. This allows to better understand covariation of traits resulting from both among-individual differences and phenotypic plasticity. We observed 141 Canada goose pairs to identify what affected the intensity of their nest defense behavior. We found that geese were very consistent in their nest defense behavior and that female fecundity was related to male personality. Females also became more defensive as their young got older. Analyzing different sources of variation in parental behaviors enables a better understanding of their evolution. Our study also demonstrates the importance of studying nest defense in both sexes even in species where only females incubate eggs, as both sexes can invest in nest defense.

Growth and reproductive characteristics of rarely observed resident female Dolly Varden (Salvelinus malma malma) in North America

Among North American populations of northern form Dolly Varden (Salvelinus malma malma) exhibiting partial migration, the resident female life history is rarely encountered. Between 2012 and 2016, three sexually mature females confirmed as residents using otolith strontium analysis were captured from three rivers in the western Canadian Arctic (< 1% of residents sampled). Size-at-capture and size-at-age, estimated using otolith back-calculation, were compared to resident males and anadromous females. Fecundity, egg diameter, and gonadosomatic index (GSI) were compared to anadromous female current-year spawners. Resident females (fork length range 220–360 mm) tended to be among the largest-sized residents (two were > 90th percentile). Early size-at-age of resident females either exceeded or were among the largest sizes compared to resident males and pre-smolt anadromous females. Residents had similar fecundity predicted for length and egg size (range 3.5–4.2 mm) compared to anadromous, although GSI (range 13.2–17.4%) was inconsistent among populations. Interestingly, one resident female attained a greater size-at-capture and fecundity than the smallest anadromous current-year spawner. Our results suggest that conditional mating tactics of Dolly Varden can be expressed by both sexes in multiple populations, and increases understanding of Dolly Varden life history diversity and bet-hedging strategies in partially migratory populations.

Relationships of the Sphaeromatidae genera (Peracarida: Isopoda) inferred from 18S rDNA and 16S rDNA genes

The Sphaeromatidae has 100 genera and close to 700 species with a worldwide distribution. Most are abundant primarily in shallow (&lt; 200 m) marine communities, but extend to 1.400 m, and are occasionally present in permanent freshwater habitats. They playan important role as prey for epibenthic fishes and are commensals and scavengers. Sphaeromatids’ impressive exploitation of diverse habitats, in combination with diversity in female life history strategies and elaborate male combat structures, has resulted in extraordinary levels of homoplasy. We sequenced specimens from 39 genera for nuclear 18S rDNA and mitochondrial 16S rDNA genes, comprehensively reviewed the effects of alignments on tree topology, and performed Garli and MrBayes analyses. These data consistently retrieved clades (genus groups), Sphaeroma, Exosphaeroma, Cymodoce, Ischyromene, Cerceis, and Dynamenella and the monogeneric clade of Gnorimosphaeroma. We define the major clades using morphological characters, attribute sampled taxa to consistently and strongly supported ones and suggest placement of unsampled genera based on their morphological characteristics. Within each clade, we also highlight unresolved and poorly sampled genera. We point out taxonomic problems in hopes of encouraging further phylogenetic exploration. Although we identify clades containing consistent generic groups and are confident that some groups will prove stable and reliable, we feel our sampling is insufficient to propose nomenclatural changes at this time.

Hunting regulation favors slow life histories in a large carnivore

As an important extrinsic source of mortality, harvest should select for fast reproduction and accelerated life histories. However, if vulnerability to harvest depends upon female reproductive status, patterns of selectivity could diverge and favor alternative reproductive behaviors. Here, using more than 20 years of detailed data on survival and reproduction in a hunted large carnivore population, we show that protecting females with dependent young, a widespread hunting regulation, provides a survival benefit to females providing longer maternal care. This survival gain compensates for the females’ reduced reproductive output, especially at high hunting pressure, where the fitness benefit of prolonged periods of maternal care outweighs that of shorter maternal care. Our study shows that hunting regulation can indirectly promote slower life histories by modulating the fitness benefit of maternal care tactics. We provide empirical evidence that harvest regulation can induce artificial selection on female life history traits and affect demographic processes.

Physiological consequences of biologic state and habitat dynamics on the critically endangered Yangtze finless porpoises (Neophocaena asiaeorientalis ssp. asiaeorientalis) dwelling in the wild and semi-natural environment.

The objectives of this study were to investigate the effects of habitat and biological state on the physiology of critically endangered wild and semi-natural Yangtze Finless Porpoises (YFPs; Neophocaena asiaeorientalis ssp. asiaeorientalis) by measuring and comparing serum biochemical parameters. A total of 168 YFPs were sampled, 68 living in the semi-natural (Tian-E-Zhou Oxbow) and 98 living in the wild (Poyang Lake, PL) environment. The YFPs in the Tian-E-Zhou Oxbow were sampled from 2002 to 2015 and in the PL from 2009 to 2017. Each population was divided into Juvenile Male, Juvenile Female, Adult Male, Pregnant and Lactating Female life history categories. Overall, with location, 19/33 of the analytes and with season 18/33 of the analytes were significantly different. Similarly, within each location, 15/33 of the analytes changed with time in PL while only 8/33 changed with time in Tian-E-Zhou Oxbow, respectively. Finally, 15/33 of the analytes demonstrated significant differences between the different age and sex groups of animals. In our study, a significant variation, as well as an increasing and decreasing pattern of several parameters in both populations, suggest a worsening ecological environment of both habitats. This study will help in health assessment, improving conservation and management practices, a crucial requisite for biodiversity conservation.

Reproductive Energetics of Female Mantled Howlers (Alouatta palliata)

The energetic costs of reproduction have an important influence on the life histories of female primates. At present, however, the interplay of female reproductive state, food availability, and strategies aimed at maintaining energy balance has been described for only a few species, limiting our ability to understand intra- and interspecific variation in female life histories. We assessed how female mantled howlers (Alouatta palliata) are affected by reproductive seasonality, and whether they alter their behavior to cope with the energetic demands of reproduction. From August 2013 to July 2015 we measured the reproductive state, behavior (1100 h of focal animal observations), and energetic condition (312 urine samples collected for C-peptide analysis) of 7 adult females, and assessed food availability (weekly phenological sampling of 397 food trees). Female behavior did not vary with reproductive state or reproductive seasonality. There were, however, differences in how females responded to variation in food availability according to reproductive state. Cycling and gestating females spent more time feeding than lactating females, and cycling females less time resting than females in other reproductive states, when food was more available. C-peptide concentrations were unaffected by either individual or overall variation in reproductive state, except for cycling females, whose concentrations increased during periods of high food availability. The energetic condition of female mantled howlers is broadly maintained over different stages of reproduction, but is sensitive to variation in food availability.

Hyleina kaphetea, a new genus and species of clearwing moths from tropical Africa (Lepidoptera: Sesiidae: Sesiini)

A new species and genus of Sesiini, Hyleina kaphetea new gen. &amp; new sp., from tropical Africa is described. The type series comprises twelve male specimens from the Democratic Republic of Congo, Malawi, Tanzania and Zambia. Female specimens and life history are unknown.

Differential effects of developmental thermal plasticity across three generations of guppies (Poecilia reticulata): canalization and anticipatory matching

Developmental plasticity can match offspring phenotypes to environmental conditions experienced by parents. Such epigenetic modifications are advantageous when parental conditions anticipate offspring environments. Here we show firstly, that developmental plasticity manifests differently in males and females. Secondly, that under stable conditions, phenotypic responses (metabolism and locomotion) accumulate across several generations. Metabolic scope in males was greater at warmer test temperatures (26–36 °C) in offspring bred at warm temperatures (29–30 °C) compared to those bred at cooler temperatures (22–23 °C), lending support to the predictive adaptive hypothesis. However, this transgenerational matching was not established until the second (F2) generation. For other responses, e.g. swimming performance in females, phenotypes of offspring bred in different thermal environments were different in the first (F1) generation, but became more similar across three generations, implying canalization. Thirdly, when environments changed across generations, the grandparental environment affected offspring phenotypes. In females, the mode of the swimming thermal performance curve shifted to coincide with the grandparental rather than the parental or offspring developmental environments, and this lag in response may represent a cost of plasticity. These findings show that the effects of developmental plasticity differ between traits, and may be modulated by the different life histories of males and females.

Predation effects on matrotrophy, superfetation and other life history traits in Phalloceros harpagos

AbstractThis study investigates the effect of a predation gradient on the female life history traits of the poeciliid live‐bearing fish Phalloceros harpagos from a tropical stream in Brazil. Females’ length at maturity, somatic dry mass, reproductive allotment and fecundity varied significantly among predation sites. Phalloceros harpagos from the high‐predation site showed smaller size at maturity and somatic dry mass, greater reproductive allotment and higher fecundity than the nonpredation site. In all sites, we observed superfetation: pregnant females with two broods at different developmental stages. The presence of superfetation was not observed before in other congeneric species, and it may represent an additional independent evolutionary origin of superfetation in the fish family Poeciliidae. Matrotrophy, the postfertilisation maternal provisioning of nutrients to developing embryos throughout gestation, was observed in all three sites, with values of the matrotrophy index above two. The population under high predation pressure showed the highest degree of matrotrophy (embryos quadruplicate their dry mass during development) and the greatest percentage of females with superfetation (44.4%). Some life history traits responded more strongly to predators’ presence and others to predator density. These results suggest that different predation regimes shape female life history traits, increasing fecundity in high‐predation sites. The results also suggest a link between the cost of reproduction and the evolution of matrotrophy and superfetation, potentially to reduce the risk of predation without reducing fecundity.

Age-related sex differences in body condition and telomere dynamics of red-sided garter snakes.

Life-history strategies vary dramatically between the sexes, which may drive divergence in sex-specific senescence and mortality rates. Telomeres are tandem nucleotide repeats that protect the ends of chromosomes from erosion during cell division. Telomeres have been implicated in senescence and mortality because they tend to shorten with stress, growth and age. We investigated age-specific telomere length in female and male red-sided garter snakes, Thamnophis sirtalis parietalis We hypothesized that age-specific telomere length would differ between males and females given their divergent reproductive strategies. Male garter snakes emerge from hibernation with high levels of corticosterone, which facilitates energy mobilization to fuel mate-searching, courtship and mating behaviours during a two to four week aphagous breeding period at the den site. Conversely, females remain at the dens for only about 4 days and seem to invest more energy in growth and cellular maintenance, as they usually reproduce biennially. As male investment in reproduction involves a yearly bout of physiologically stressful activities, while females prioritize self-maintenance, we predicted male snakes would experience more age-specific telomere loss than females. We investigated this prediction using skeletochronology to determine the ages of individuals and qPCR to determine telomere length in a cross-sectional study. For both sexes, telomere length was positively related to body condition. Telomere length decreased with age in male garter snakes, but remained stable in female snakes. There was no correlation between telomere length and growth in either sex, suggesting that our results are a consequence of divergent selection on life histories of males and females. Different selection on the sexes may be the physiological consequence of the sexual dimorphism and mating system dynamics displayed by this species.

Life history evolution, reproduction, and the origins of sex-dependent aging and longevity.

Males and females in many species differ in how they age and how long they live. These differences have motivated much research, concerning both their evolution and the underlying mechanisms that cause them. We review how differences in male and female life histories have evolved to shape patterns of aging and some of the mechanisms and pathways involved. We pay particular attention to three areas where considerable potential for synergy between mechanistic and evolutionary research exists: (1) the role of estrogens, androgens, the growth hormone/insulin-like growth factor 1 pathway, and the mechanistic target of rapamycin signaling pathway in sex-dependent growth and reproduction; (2) sexual conflict over mating rate and fertility, and how mate presence or mating can become an avenue for males and females to directly affect each other's life span; and (3) the link between dietary restriction and aging, and the emerging understanding that only the restriction of certain nutrients is involved and that this is linked to reproduction. We suggest that ideas about life histories, sex-dependent selection, and sexual conflict can inform and be informed by the ever more refined and complex understanding of the mechanisms that cause aging.

Where and what to feed? Differential effects on fecundity and longevity in the invasive Drosophila suzukii

Successful establishment of invasive species requires that the species meet environmental conditions favouring their longevity and fecundity. When juveniles and adults consume different resources, gravid females may have to choose whether to feed or to reproduce. We used a successful invasive species to test whether female life history traits are affected by the potential nutrients found in reproductive sites. The pest species, Drosophila suzukii, lays eggs in fruits that could provide nutrients since fruit exudates are generated during oviposition. We demonstrated that D. suzukii adults cannot survive when they have only access to reproductive sites (i.e. undamaged fruits). But they can find the nutrients necessary for longevity on these reproductive sites if there are larger holes in the exocarp. Egg maturation is low when D. suzukii feeds on nutrients from fruits, even when damaged, suggesting that females cannot acquire sufficient nutrients for egg maturation where they lay their eggs. Finally, a field experiment supported our laboratory results: wild females have a low degree of egg maturation, even when captured near reproductive sites. Our study hence shows constraints on egg production, and therefore on fruit infestation, determined by the nutritional ecology of pest females.

Testing for links between face color and age, dominance status, parity, weight, and intestinal nematode infection in a sample of female Japanese macaques.

Studies of the role of secondary sexual ornaments in mate choice tend to focus on colorful traits in males, but females of many animal species express colorful ornamentation too. Among non-human primates, investigations into the role of female secondary sexual traits as indicators of life history characteristics, reproductive success, and health status have mostly focused on sexual swellings, whereas only few studies have been conducted on the role of facial color. Recent studies on rhesus macaques and mandrills suggested that female ornamentation might provide information about female life history characteristics, but not on disease resistance factors and parasite infection, which have been shown to affect male ornamentation in some non-primate species. In Japanese macaques (Macaca fuscata), females have brightly colored faces that are indicative of their reproductive status. Here, we aimed to determine whether female facial color might also convey information about age, dominance rank, parity, weight, and intestinal nematode infection in free-ranging individuals. We analyzed whether female facial parameters (luminance and redness) were linked to these individual characteristics, using digital photography and data on intestinal parasite infection collected systematically during 1 month for each of seven free-ranging females. We found no evidence to suggest that female facial color is an indicator of any of these measures in Japanese macaques. Considering our small data set, it is still preliminary to draft any clear conclusions. Future studies combining digital, hormonal, parasitological and behavioral data are needed to assess the possible role of female face color on male preferences and mating choice in Japanese macaques.