DO EMBRYOS INFLUENCE MATERNAL INVESTMENT? EVALUATING MATERNAL‐FETAL COADAPTATION AND THE POTENTIAL FOR PARENT‐OFFSPRING CONFLICT IN A PLACENTAL FISH

The evolution of matrotrophy introduces the potential for genomic conflicts between mothers and embryos. These conflicts are hypothesized to accelerate the evolution of reproductive isolation and to influence the evolution of life-history traits, reproductive structures, and genomic imprinting. These hypotheses assume offspring can influence the amount of maternal investment they receive and that there is a trade-off between maternal investment into individual offspring and maternal survival or fecundity. We used field data and laboratory crosses to test whether these assumptions are met in the matrotrophic poeciliid fish Heterandria formosa . Comparisons of life histories between two natural populations demonstrated a trade-off between the level of maternal investment into individual embryos and maternal fecundity. Laboratory crosses between individuals from these populations revealed that offspring genotype exerts an influence on the level of maternal investment and affects maternal fecundity through higher rates of embryo abortion and lower numbers of full-term offspring. Our results show that the prerequisites for parent–offspring conflict to be a potent evolutionary force in poeciliid fish are present in H. formosa. However, determining whether this conflict has shaped maternal investment in nature will require disentangling any effects of conflict from those of several ecological factors that are themselves correlated with the expected intensity of conflict.     

Use of field‐portable ultrasonography reveals differences in developmental phenology and maternal egg provisioning in two sympatric viviparous snakes

A thorough understanding of the life cycles underlying the demography of wild species is limited by the difficulty of observing hidden life‐history traits, such as embryonic development. Major aspects of embryonic development, such as the rate and timing of development, and maternal–fetal interactions can be critical features of early‐life fitness and may impact population trends via effects on individual survival. While information on development in wild snakes and lizards is particularly limited, the repeated evolution of viviparity and diversity of reproductive mode in this clade make it a valuable subject of study. We used field‐portable ultrasonography to investigate embryonic development in two sympatric garter snake species, Thamnophis sirtalis and Thamnophis elegans in the Sierra Nevada mountains of California. This approach allowed us to examine previously hidden reproductive traits including the timing and annual variation in development and differences in parental investment in young. Both species are viviparous, occupy similar ecological niches, and experience the same annual environmental conditions. We found that T. sirtalis embryos were more developmentally advanced than T. elegans embryos during June of three consecutive years. We also found that eggs increased in volume more substantially across developmental stages in T. elegans than in T. sirtalis, indicating differences in maternal provisioning of embryos via placental transfer of water. These findings shed light on interspecific differences in parental investment and timing of development within the same environmental context and demonstrate the value of field ultrasonography for pursuing questions relating to the evolution of reproductive modes, and the ecology of development.     

Reproductive biology of lamnoid sharks

Synopsis The capture of recently inseminated or pregnant specimens ofCarcharias taurus, Isurus paucus, I. oxyrinchus, Alopias superciliosus andA. vulpinus has allowed new information to be obtained on the reproductive biology of these species. Oophagy and embryonic cannibalism (adelphophagy) have been documented inC. taurus, but only oophagy in other lamnoid species. The occurrence of up to nine embryos of similar size per uterus inIsurus and no indication of functional erect teeth in embryos leaves considerable doubt that embryophagy occurs in this genus. Considerable data has been collected onCarcharias taurus which allows a lamnoid reproductive model to be developed and tested, in spite of the obvious differences between the reproductive biology of this species and other lamnoids. Gonad structure, ovarian development, fertilization, early embryonic differentiation, embryonic nutrition and parturition, inC. taurus and other lamnoids differs significantly from other elasmobranchs.     

The comparative reproductive styles of two closely related African minnows (Pseadobarbus afer andP. asper) inhabiting two different sections of the Gamtoos River system

Synopsis Two species of a monophyletic lineage of flexible-rayed redfin minnows,Pseudobarbus afer andP. asper, were studied to establish if there were any significant differences in their reproductive styles. They are sister species with few morphological or meristic differences.P. afer andP. asper are open substrate benthic spawners on coarse bottoms (rocks) and non-guarders of non-adhesive eggs. Their young are photophobic as free embryos. Riverine spawning sites indicated a conservative tendency and represented a phylogenetic constraint as compared to the more variable attributes, such as egg size, which were under environmental control within the limits expressed by the genotype. The combination of life-history attributes, gonadosomatic index, fecundity, egg size, investment per clutch, number of clutches per season and reproductive lifespan was found to be different forP. afer andP. asper. P. asper is derived and atypical of otherPseudobarbus species studied to date. Differences betweenP. afer andP. asper are directly related to the two distinct environments inhabited by these species-coastal Cape Fold Belt mountain streams and the inland Karoo streams of the Gamtoos River system.P. asper may have reverted, by juvenilization, to a more altricial form to survive the turbid, intermittent Karoo stream.     

Reproductive strategies of sub-Antarctic lithodid crabs vary with habitat depth

We present the first fecundity and egg size data for three species of lithodid crab from Antarctic waters south of the Polar Front, caught in the fisheries operating around the island of South Georgia. In all species, fecundity was observed to increase with body size, but reproductive allocation was found to differ significantly between species. The highest relative fecundity (eggs^−g body weight) and smallest egg size was found in Paralomis spinosissima, which is found in shallower waters, whereas the lowest relative fecundity values and largest eggs were recorded in the deeper living species, Neolithodes diomedeae. Evidence is presented that closely related sympatric species may employ quite different reproductive strategies that suit their depth distribution whilst indicating the overriding evolutionary adaptation of reproductive traits to temperature and food availability.     

Reproductive cycle and maternal–embryonic nutritional relationship of shovelnose guitarfish Pseudobatos productus in the Gulf of California

Samples of the shovelnose guitarfish Pseudobatos productus were collected on board a vessel and at landings of artisanal commercial fisheries in the Gulf of California from May 2004 to June 2007. Samples of 650 females, 2047 embryos and 484 uterine eggs were examined. The reproductive cycle is annual, ovulation and parturition occur in July, the uterine eggs are in diapause for 9 months (July–March) before an accelerated growth of embryos of 3 months. Histological analyses of the uterine wall of pregnant females suggested that no secretions were used for embryo nourishment. The standard percentage of water content was 48·6% in fertilized eggs and 80·75% in full‐term embryos. Dry mass loss during embryonic development was 16·3% and the chemical balance of development was 0·84. This indicates that P. productus is a strictly lecithotrophic, viviparous species, that makes no maternal contribution of nutrients during embryonic development.     

Fecundity and reproductive output of the caridean shrimp Periclimenes paivai associated with scyphozoan jellyfish

Periclimenes paivai is notable for its symbiotic lifestyle with jellyfish. The objective of this study was to investigate the fecundity and reproductive output of females, and specifically to determine whether females protected in their host have a greater reproductive success than other shrimp species. All anatomical parts of the medusae were analyzed and the P. paivai individuals were separated. Among 83 females analyzed, 65 presented embryos in the first developmental stage, and 18 were in the final stage of development. The mean fecundity was 229.08 ± 120.04 in initial-stage embryos and 191 ± 114.76 in final-stage embryos. We observed a positive relationship between the embryo number and the female size; however, the embryo number was not related to the embryonic stage, which indicates that females did not lose their embryos during the incubation period. The weight of brood mass during production is closely related to the female weight according to the results of linear regression, as fecundity increased with female size. In its symbiosis, P. paivai can increase the amount of energy used to produce embryos (mean reproductive output = 10.38%) and can elevate the reproductive success.     

Condition and reproductive investment in the western mosquitofish (Gambusia affinis): little evidence for condition‐dependent sex‐biased investment

In sexually reproducing species, resources may theoretically be distributed with bias to the production of male or female offspring in response to the condition of the mother, commonly recognized as sex allocation. Using a recently characterized sex‐specific molecular marker, we tested for maternal sex allocation (i.e. maternal primary sex ratio bias and sex‐specific offspring investment) in captive laboratory‐bred western mosquitofish (Gambusia affinis) at early stages of offspring development. We found no statistical evidence to support sex allocation in G. affinis, based on maternal condition. In addition, we found little evidence for correlations between maternal condition and investment in the condition (mass) of individual offspring (of one sex or the other), although we did find that larger mothers tended to have higher fecundity.     

Female-biased sex allocation in wild populations of the eriosomatine aphid Prociphilus oriens: local mate competition or transgenerational effects of maternal investment?

Several aphid species exhibit female-biased sex allocation. Local mate competition (LMC) has been postulated to be the evolutionary factor of the female-biased sex allocation. We estimated individual sex allocation in the eriosomatine aphid Prociphilus oriens and explained the observed pattern of sex allocation based on a hypothesis other than LMC. On the basis of the relationship between maternal body size and brood size, we estimated the cost of producing a female to be 1.85 times the cost of producing a male. The population-wide allocation to males was 22–24 %. Winged mothers exhibited a large variation in the number of male and female embryos they had, including 23–30 % of winged mothers producing only female embryos. There was polymorphism in the sex-ratio expression. Thus, the constant male hypothesis assuming LMC was not supported. Winged mothers that produced an all-female brood contained larger female embryos than did mothers that produced a bisexual brood. Previous studies have indicated that a large sexual female produces a single large egg, which hatches into a first-instar larva containing a larger amount of gonads. Thus, in eriosomatine aphids, maternal investment in daughters directly affects the potential fecundity of granddaughters, whereas investment in sons does not. We propose a hypothesis that higher fitness returns from maternal investment in daughters than in sons may have primarily led to the evolution of highly female-biased sex allocation in P. oriens.     

Comparison ofMononychellus progresivus andTetranychus urticae as prey for five species of phytoseiid mites

The present study reports life-table parameters and compares the longevity, fecundity, egg-to-adult development times and the length of the reproductive periods for five phytoseiid species (Typhlodromus annectens, Amblyseius californicus, A. idaeus, Euseius concordis, andPhytoseiulus macropilis) when reared onMononychellus progresivus orTetranychus urticae. Recommendations regarding the use of these species for classical biological control ofM. tanajoa in Africa are made.     

Locomotor impairment of gravid lizards: is the burden physical or physiological?

Pregnancy is associated with reduced locomotor performance in several reptile species, but the reasons for this reduction remain unclear. Previous authors generally have assumed that the decreased maternal mobility is due to the physical burden of the clutch, but our data on a viviparous Tasmanian scincid lizard (Niveoscincus microlepidotum) suggest a different interpretation. Running speeds of gravid female skinks decrease during gestation (as litter mass increases), but this locomotor impairment is due to physiological changes associated with pregnancy, rather than simple physical burdening. Maternal running speeds are unrelated to litter masses, and do not increase in the week after parturition. Females with very large abdominal fat‐bodies (due to ad libitum feeding in the laboratory), equivalent in mass to the litter, nonetheless run rapidly. If the locomotor ‘costs’ of reproduction reflect all‐or‐none physiological changes associated with pregnancy, then the magnitude of such costs may correlate only weakly with the actual level of reproductive investment. Because life‐history models predict that the relationship between fecundity and ‘cost’ has important evolutionary consequences, our results highlight the need to clarify the causal basis for locomotor impairment in gravid reptiles.     

Size delays female senescence in a medium sized marsupial: The effects of maternal traits on annual fecundity in the northern brown bandicoot (Isoodon macrourus)

The degree to which females allocate resources between current reproduction, future fecundity and survival is a central theme in life history theory. We investigated two hypotheses proposed to explain patterns of reproductive investment, terminal investment and senescence, by examining the effects of maternal traits (age and maternal mass) on annual fecundity in female northern brown bandicoots, Isoodon macrourus (Marsupialia: Peramelidae). We found that annual fecundity in females declined in their final year of reproduction, indicating reproductive senescence. Maternal mass significantly influenced the rate of senescence and, in turn, a female's lifetime reproductive output. Mass had little effect on fecundity in 1st and 2nd year females, but a positive relationship with fecundity in 3rd year females. This meant that heavy, 3rd year females did not suffer the decline in fecundity shown in light 3rd year females. For 1st year females, mass and leg length increased between their first and second reproductive seasons, indicating a temporary shift, from the allocation of resources to reproduction, to increasing condition or structural size post their first breeding event. There were no net changes to body mass in subsequent years. We suggest that this year of post‐reproductive growth has important consequences for senescent effects on reproduction. Overall, results provided support for the effects of senescence on annual fecundity. Our findings were not consistent with the terminal investment hypothesis; reproductive output did not increase in females' final reproductive season despite a rapid decline in survival. However, this notion cannot be entirely dismissed; other measures of reproductive performance not examined here (e.g. offspring mass) may have provided an indication that females did increase their effort at the end of their lifespan. This study highlights the difficulty of measuring reproductive costs and the importance of understanding the combined effects of specific characteristics of an individual when interpreting reproductive strategies in iteroparous organisms.     

Salinity and temperature influence in rotifer life history characteristics

A review of temperature and salinity effects on rotifer population dynamics is presented together with original data of these effects for three clones of Brachionus plicatilis. There is a clear relationship between temperature and the intrinsic rate of increase, r: an increase of temperature — within the natural environmental range — produces an exponential increase of r, and the slope of the response depends on the genotype. The effect of salinity is also genetically dependent; the highest r for each clone is observed at the salinity close to that of its environmental origin. The response of r to temperature is mainly a consequence of the response of the individual rates of development and reproductive timing. The effect of temperature on fecundity (number of descendents per individual life time) is negligible when temperature values are within the normal habitat ranges. On the other hand, salinity seems to affect primarily fecundity. The interaction salinity-temperature may be important in clones or species living in fluctuating environments with positive response to the more frequent combinations found in the corresponding habitats.     

Reproductive biology of viviparous and oviparous species of the leaf beetle genus Oreina

In five species of the genus Oreina Chevrolat (Coleoptera, Chrysomelidae) we compared the size of offspring, the fecundity of the females, the timing of offspring production and female investment over the season. Two of the species, O. elongata and O. luctuosa, laid eggs, while O. cacaliae, O. gloriosa and O. variabilis gave birth to larvae. Offspring size corrected for female size was similar in the two oviparous species and in the viviparous O. cacaliae. In the two other viviparous species the larvae were two to three times bigger in relation to the female. The greater size of the offspring was not traded off for lower fecundity in these latter two species, yet the production of bigger larvae was associated with a longer laying period and thereby a spreading of reproductive investment over the season. The prediction of life history theory that higher investment in individual offspring should be traded off for lower fecundity could not be confirmed. The investigation of egg and larval development showed that in one of the oviparous species, O. luctuosa, the length of the egg stage was more variable. This corroborates the view that in this species the eggs can be retained for varying times before being laid. Greater size at birth does not necessarily lead to shortened developmental times: the larval periods of O. cacaliae, O. elongata, O. gloriosa and O. variabilis were all comparable although the larvae of the first two species were relatively smaller when laid; only the small larvae of O. luctuosa needed significantly longer for their development. For all growth parameters examined the differences between species were larger than the differences between populations. A comparison of larval growth of the oligophagous species O. cacaliae on three plant genera showed that larval growth rate is influenced by the food plant. However, the plant on which the larvae grew worst is apparently not chosen for oviposition in the field. A comparison with a phylogeny of the species based on allozymes suggests that species with similar reproductive parameters are closely related, yet that viviparity evolved independently in O. cacaliae on one hand and O. variabilis and O. gloriosa on the other.     

Geographical variation and local environment effects in the reproductive output and fecundity of the shrimp Exhippolysmata oplophoroides (Decapoda: Caridea) in southeastern Brazil

We studied the shrimp Exhippolysmata oplophoroides in southeastern Brazil (Macaé, 22º37″S; Ubatuba, 23º55″S; and Cananéia, 25º53″S) to test the hypotheses that (1) females should have the same reproductive output and fecundity at the regional scale, and (2) these reproductive parameters can vary among regions. Maximum carapace length (Macaé = 13.1 mm, Ubatuba = 12.8, Cananéia = 16), fecundity, and reproductive output differed among regions (Ancova, p < 0.05). Females in Cananéia exhibited the highest reproductive output/fecundity (18.6%/5230 embryos), followed by those in Macaé (16.0%/4365 embryos) and Ubatuba (12.6%/1206 embryos). We found that fecundity/reproductive output varies inversely with the length of the reproductive season, i.e. a considerable amount of energy is allocated during seasonal spawning periods in subtropical regions such as Cananéia. Previous studies have proved that E. oplophoroides is able to reproduce continuously in Ubatuba, with probably minor but continuous energy investment in reproduction occurring in this tropical region. In contrast, although Macaé is located at tropical latitude, it is under the influence of Cabo Frio upwelling that alters the water’s physical properties via cold water intrusion. This process may be a determining factor in the spawning seasonality of Macaé’s shrimp population, justifying the higher reproductive output recorded here than in Ubatuba.     

Colony-level single-sex alate production inPheidole ceres andPheidole pilifera (Formicidae: Myrmicinae)

Summary Patterns of colony-level reproductive investment were estimated inPheidole ceres andP. pilifera. Both species exhibited strong degrees of colony-level, single-sex alate production, but differed in the extent to which colonies produced only one sex. The proportion of reproductive investment allocated to males was negatively correlated to the total reproductive allocation in both species.     

Maturation of Squalus mitsukurii and Cirrhigaleus asper (Squalidae, Squaliformes) in the southwestern equatorial Atlantic Ocean

Specimens of Squalus mitsukurii (n = 206) and Cirrhigaleus asper (n = 93) were opportunistically collected from the catches of a research vessel using traps and benthic longlines off the coast of northeastern Brazil between March 1997 and August 2002. For both species, larger females than males were captured. Catches of S. mitsukurii were biased toward females (1 : 4.6), while no significant disequilibrium in sexes was detected for C. asper (1 : 0.86). Common regressions for total length (TL) and eviscerated weight (EW) were calculated as LnEW = 3.13LnTL − 6.217 (S. mitsukurii) and LnEW = 3.22LnTL − 7.01 (C. asper). Based on changes to the reproductive tract, females and males of each species were categorized into several stages of maturation. Sizes at sexual maturity for female (n = 169) and male (n = 37) S. mitsukurii were 77.8 and 65.0 cm TL, respectively. Gravid S. mitsukurii had between 3 and 11 embryos that ranged in size from 2.0 to 22.5 cm TL (n = 262). No significant bias in the sex ratio of embryos was detected. A clear relationship between embryonic development and maturation of the ovary demonstrated that female S. mitsukurii are ready to ovulate immediately after parturition. Female (n = 43) and male (n = 50) C. asper approached sexual maturity at 110.0 and 91.0 cm TL, respectively. Uterine fecundity in gravid C. asper ranged from 12 to 19 embryos that varied in size between 4.0 and 21.9 cm TL. Unlike S. mitsukurii, there was no concurrent development of the ovary and embryos. The results are discussed in terms of the reproductive plasticity of S. mitsukurii and the need for further life history studies on both species.     

Reproductive pattern of the freshwater prawn Pseudopalaemon bouvieri (Crustacea,Palaemonidae) from hypo-osmotic shallow lakes of Corrientes (Argentina)

Pseudopalaemon bouvieri undergoes complete abbreviated development. The reproductive cycle (proportion and size of the sexually mature population and juvenile recruitment), fecundity and egg size of this prawn were examined in three subtropical shallow lakes. The reproductive cycle was seasonal; gonadal maturation occurred during the winter, ovigerous females were abundant in the spring and breeding occurred at the end of spring. Females produced small numbers of eggs (9–55) of relatively large sizes (1.0–2.1 mm). The proportion of ovigerous females with respect to the total number of females, the fecundity and egg size differed among the lakes according to the trophic state of the environments. Pseudopalaemon bouvieri has a reproductive strategy similar to other Palaemonidae species that inhabit nutrient-poor inland waters.     

Habitat and life history differences between two species of Gambusia

Life history strategies reflect trade-offs that tend to maximize fitness, such as investment in a few large or many small offspring. We compared life histories of two temperate livebearing fishes Gambusia affinis and G. nobilis, an endangered species which is virtually unstudied. The two species persist in environments that differ widely in abiotic and biotic factors in the same local area. Gambusia affinis were typically found in habitats with high productivity and wide fluctuations in temperature, salinity and dissolved oxygen, whereas G. nobilis occurred in more stable spring-fed habitats. We collected data on life-history traits: embryo mass, brood size (number of embryos), total maternal reproductive effort, population sex ratios, and size (mass and length) distributions of adults and juveniles. There was no difference between species in reproductive effort per brood, but they differed in investment strategy. Gambusia affinis females produced large broods with small embryos, whereas G. nobilis females produced broods of fewer, larger embryos. These differences in life history strategies reflect a tradeoff between individual productivity and differential mortality rates in different environments. At our field site G. affinis persists as an annual species with relatively high growth rates and corresponding reproductive patterns, whereas G. nobilis females have a slower reproductive tempo and may live multiple years.     

Comparing wing loading,flight muscle and lipid content in ant‐attended and non‐attended Tuberculatus aphid species

Although all Tuberculatus aphids possess wings, some species associated with ants exhibit extremely low levels of dispersal compared with those not associated with ants. Furthermore, phylogenetic interspecific comparisons find significantly higher wing loading (i.e. higher ratio of body volume to wing area) in ant‐attended species. This observation indicates that ant‐attended species may allocate more of their body resources to reproductive traits (i.e. embryos) rather than flight apparatus (i.e. wings, flight muscle and lipid). The present study focuses on two sympatric aphid species and aims to investigate the hypothesized trade‐off in resource investment between fecundity and the flight apparatus; specifically, the ant‐attended Tuberculatus quercicola (Matsumura) and non‐attended Tuberculatus paiki Hille Ris Lambers. Species differences are compared in: (i) morphology, (ii) embryo production, (iii) triacylglycerol levels and (iv) wing loading and flight muscle. The results show that T. quercicola has a larger body volume, higher fecundity and higher wing loading compared with T. paiki, which has a smaller, slender‐shaped body, lower fecundity and lower wing loading. No significant difference is found between the species with respect to the percentage of triacylglycerol content in dry body weight. The flight muscle development is significantly lower in T. quercicola than in T. paiki. These results indicate that the additive effect of higher wing loading and the lower amount of flight muscle development in T. quercicola may increase the physical difficulty of flight, and hence be responsible for its lower dispersal ability. The trade‐off between fecundity and dispersal documented in wing‐dimorphic insects may therefore be applicable to T. quercicola, which has fully developed wings.