Life history adaptation along a latitudinal cline in the water strider Aquarius remigis (Heteroptera: Gerridae)

We addressed the general hypothesis that life history differences among eastern populations of the North American water strider, Aquarius remigis (Heteroptera: Gerridae), along a north-south gradient are manifestations of genetic differentiation due to natural selection. We raised offspring of two field-caught populations from each of three latitudes in a common laboratory environment at 20° C and two photoperiods. Nearly all Quebec (PQ) individuals (ca. 46° N) entered diapause to reproduce the following spring (univoltine life cycle), while intermediate proportions of New York (NY; ca. 43° N) and New Jersey (NJ; ca. 41° N) individuals reproduced directly, producing a second generation (bivoltine life cycle). PQ females were smaller, developed faster, and laid smaller eggs than NY and NJ individuals; NY and NJ populations differed little in these variables. NY females had longer life spans than either PQ or NJ females, but lower oviposition rates. Total reproductive output did not differ across latitudes. Photoperiod affected body length, development time, and reproductive pathway, resulting in a latitude by environmental interaction. PQ individuals reproduced directly under 15L : 9D (summer) conditions only, while the NY and NJ populations exhibited more direct reproduction under 13L : 11D (spring or fall) conditions. Some life history characters of the NY and NJ populations displayed the higher variability indicative of phenological transition zones. These results indicate local adaptation of populations to long-term climatic patterns. Water striders appear to adapt to longer seasons by extending development, growing larger, and breeding directly. Larger body size and extended or rapid development are associated with bivoltinism and increase in egg size, but not necessarily with higher fecundity or oviposition rate. The phenological transition zone appears to be unrelated to a transition zone a little further south established by allozyme data and morphology, as all populations studied here could be electrophoretically identified as northern "type".     

Assembly of the fluorescent acrosomal matrix and its fate in fertilization in the water strider,Aquarius remigis

Animal sperm show remarkable diversity in both morphology and molecular composition. Here we provide the first report of intense intrinsic fluorescence in an animal sperm. The sperm from a semi‐aquatic insect, the water strider, Aquarius remigis, contains an intrinsically fluorescent molecule with properties consistent with those of flavin adenine dinucleotide (FAD), which appears first in the acrosomal vesicle of round spermatids and persists in the acrosome throughout spermiogenesis. Fluorescence recovery after photobleaching reveals that the fluorescent molecule exhibits unrestricted mobility in the acrosomal vesicle of round spermatids but is completely immobile in the acrosome of mature sperm. Fluorescence polarization microscopy shows a net alignment of the fluorescent molecules in the acrosome of the mature sperm but not in the acrosomal vesicle of round spermatids. These results suggest that acrosomal molecules are rearranged in the elongating acrosome and FAD is incorporated into the acrosomal matrix during its formation. Further, we followed the fate of the acrosomal matrix in fertilization utilizing the intrinsic fluorescence. The fluorescent acrosomal matrix was observed inside the fertilized egg and remained structurally intact even after gastrulation started. This observation suggests that FAD is not released from the acrosomal matrix during the fertilization process or early development and supports an idea that FAD is involved in the formation of the acrosomal matrix. The intrinsic fluorescence of the A. remigis acrosome will be a useful marker for following spermatogenesis and fertilization. J. Cell. Physiol. 226: 999–1006, 2011. © 2010 Wiley‐Liss, Inc.     

Allometry for sexual size dimorphism: testing two hypotheses for Rensch's rule in the water strider Aquarius remigis

Within any given clade, male size and female size typically covary, but male size often varies more than female size. This generates a pattern of allometry for sexual size dimorphism (SSD) known as Rensch's rule. I use allometry for SSD among populations of the water strider Aquarius remigis (Hemiptera, Gerridae) to test the hypothesis that Rensch's rule evolves in response to sexual selection on male secondary sexual traits and an alternative hypothesis that it is caused by greater phenotypic plasticity of body size in males. Comparisons of three populations reared under two temperature regimes are combined with an analysis of allometry for genital and somatic components of body size among 25 field populations. Contrary to the sexual-selection hypothesis, genital length, the target of sexual selection, shows the lowest allometric slope of all the assayed traits. Instead, the results support a novel interpretation of the differential-plasticity hypothesis: that the traits most closely associated with reproductive fitness (abdomen length in females and genital length in males) are "adaptively canalized." While this hypothesis is unlikely to explain Rensch's rule among species or higher clades, it may explain widespread patterns of intraspecific variation in SSD recently documented for many insect species.     

Mate disruption in the water strider Aquaris remigis Say, 1832 (Hemiptera: Gerridae)

This report describes the behaviour of a previously uncharacterised mating tactic amongst male water striders (Aquarius remigis Say, 1832), involving the physical break up of existing mating pairs. Using data from four separate laboratory observations on the water strider mating system, we show that this behaviour represents roughly 12.6% of all mating attempts by males. Furthermore, we demonstrate that males are successful in breaking up the existing mating pair in 15.6% of the cases, resulting in secure matings with the disrupted female 6.2% of time. We suspect that mate disruption may serve as an alternative means for acquiring mates by males with low mating success using conventional behaviours. Further research should be performed to determine the prevalence of this behaviour in various natural populations and the specific contexts in which this behaviour occurs.     

Fitness consequences of alternative life histories in water striders,Aquarius remigis (Heteroptera: Gerridae)

Using field and laboratory observations and experiments over 3 years, I investigated whether reproductive trade-offs shape individual life histories in two natural populations of the water strider, Aquarius remigis, in which univoltine and bivoltine life cycles coexist. Both later eclosion dates and food shortages, even after adult eclosion, induced diapause in females, thus deferring reproduction to the following spring. Adult body size was positively affected by food availability during juvenile development. Higher food levels also increased the reproductive output of females, but not their longevity or oviposition period. When compared to spring breeders (univoltine life cycle), direct (summer) breeders (bivoltine life cycle) experienced reduced lifetime egg numbers and longevity, as well as reduced survivorship of their second-summer-generation offspring; these reproductive costs offset, at least in part, the advantage in non-decreasing populations of having two generations per year. Fecundity was correlated with body size, and among summer-generation females direct breeders were larger than non-breeders. The time remaining before the onset of winter and/or the time since adult eclosion augmented cumulative energy uptake, and consequently the lipid reserves and winter survival probability of non-breeding (diapausing) summer adults approaching hibernation. Overwintered spring reproductives died at faster rates than non-reproductive summer individuals despite greater food availability in spring, indicating a mortality cost of reproduction. Body length correlated with absolute and not with proportional lipid content but showed no consistent relationship with survivorship in the field. These results are in agreement with current theory on the evolution of insect voltinism patterns, and further indicate high degrees of life history flexibility (phenotypic plasticity) in the study populations in response to variable environmental factors (notably photoperiod and food availability). This may be related to their location in a geographic transition zone from uni- to bivoltine life cycles.     

Genital morphology and taxonomy of the water strider Aquarius remigis (Say) (Insecta, Hemiptera-Heteroptera: Gerridae)

The shape of the dorsal vesical plate was used to determine the extent of morphological differentiation among populations of the water strider Aquarius remigis (Say) (Hemiptera-Heteroptera: Gerridae), and between species assigned to the A. remigis species group. Populations were sampled throughout North America and Mesoamerica, and included paratypes of A. remigoides Gallant & Fairbairn, and material collected from the type localities of A. amplus (Drake & Harris) and A. nyctalis (Drake & Hottes). If taxonomy is to be inferred from the shape of the dorsal vesical plate, as suggested by previous authors, several taxonomic issues need to be reconsidered. First, there was one species distributed widely across North America and deep into Mexico that is very likely to represent A. remigis , meaning that populations from the western USA previously assigned to ' A. nyctalis ' should be synonymized with this species. Second, A. remigoides as currently defined also includes some populations of A. remigis , and is probably much less widely distributed in the south-eastern USA than previously thought. A hybridization zone in Pennsylvania between A. remigis and A. remigoides , as inferred from measurements of body size and allozyme electrophoresis, is not congruent with data from the male genitalia, which indicated a transition zone between the two forms in Virginia much further to the south. Finally, A. amplus was widespread in Mexico, reaching into Guatemala to the south and into Arizona to the north.  © 2007 The Linnean Society of London, Biological Journal of the Linnean Society , 2007, 90 , 381–398.     

The histology and histochemistry of oogenesis in the water strider, Gerris remigis Say

In each ovariole of Gerris remigis, nurse cells arise by mitotic divisions at the anterior end of the germarium. These cells enlarge as they move posteriorly. This size increase is possibly caused by fusion of cells, but probably by endopolyploidy as well. The nurse cells then establish connections with a central trophic core, which receives the products of subsequent nurse cell degradation. Two possible pathways of nuclear degradation are suggested: one involves the condensation of chromatin within the nucleus; the other, the release of DNA as fine granules into the cytoplasm. Cytoplasmic areas containing such DNA are also rich in proteinaceous granules, but have a meager content of RNA. The remainder of the cytoplasm of the mature nurse cells contains a high concentration of RNA, as do the nucleoli. Posteriorly the trophic core connects via nutritive cords with each developing oocyte in the prefollicular region and in the anterior vitellarium. RNA is apparently contributed to the ooplasm via the trophic stream. Patches of cytoplasmic DNA are present in the young oocytes; the origin and fate of this DNA is uncertain. During early oocyte maturation chromosomal stainability decreases, and the nucleolus enlarges. In previtellogenic stages, numerous proteinaceous bodies appear in association with the nucleolus-chromosome complex. These bodies, like the nucleolus, have only a low RNA content. They may pass to the cytoplasm, but cannot be traced with certainty. During the latter part of this period a complex population of small proteinaceous and lipid preyolk bodies accumulates peripherally in the oocyte. Definitive protein and lipid yolk are probably derived by the enlargement and inward migration of these bodies. The oocytes are each surrounded by a layer of follicle cells proliferated in the prefollicular region. These become binucleate and enlarge as the enclosed oocytes grow and elongate. RNA also increases in the nucleoli and cytoplasm of the follicle cells as they move posteriorly in the vitellarium. There is no evidence of transfer of nucleic acids or protein from the follicle cells to the oocyte. The nurse cells are therefore implicated as the major source of nucleic acids for the maturing oocyte.     

Costs and benefits for water strider (Aquarius paludum) females of carrying guarding, reproductive males

We describe the mating system of Aquarius paludum insularis based on field observations and test hypotheses about the effects of body size, hunger level and post-copulatory guarding on reproductive performance. The mating sequence of this species was typical for temperate water striders, except that most oviposition was carried out by tandem pairs, most of which were submerged. Mate guarding continued until the end of oviposition, lasting up to 18.2h, which was much longer than that recorded for other species of water striders. Pair partners changed after oviposition. Extended contact guarding reduced female mobility. In the case of females that carried long-winged males, there was a significant reduction in speed and stride between tandem as opposed to single females. However, when short-winged males were carried, there was not a significant difference. Short-term foraging efficiency did not differ significantly between tandem and single females, and thus did not reflect the difference in mobility. Hunger level did not significantly affect female mating receptivity. Although the number of harassment bouts by unpaired males did not differ between single and tandem females, single females suffered significantly more harassment. Females were able to lay fertilized eggs for about 15 days after a single copulation, but they accepted long guarding and multiple mating during this period as well. The cost of resisting male mating attempts appears to be greater than the cost of carrying males.     

Alternative life histories in the water strider Gerris lacustris: time constraint on wing morph and voltinism

The wing dimorphic water strider Gerris lacustris L. (Heteroptera: Gerridae) switches to a bivoltine life cycle under favorable climatic conditions. The switch in voltinism is accompanied by a reduction of wing development in the directly reproducing midsummer generation, while the diapausing generation has a high fraction of long‐winged individuals. We investigated whether the thermal energy (degree‐days) available in natural habitats constrains the combination of developmental pathway and wing morph. Offspring of G. lacustris were reared under quasi‐natural conditions at two temperature regimes to determine the thermal constant k required to complete adult development in either wing morph. The thermal constant for egg‐to‐adult development of the short‐winged morph was about 20% lower than of the long‐winged morph. Based on the results from the outdoor laboratory experiment, we calculated the total degree‐days necessary to complete the possible combinations of wing morph pattern and voltinism. Comparison of these estimates with the thermal energy actually available during the reproductive season of 2004 for various natural habitats (sun‐exposed field ponds and shaded forest ponds) suggests that voltinism as well as wing morph pattern is strongly limited by the number of degree‐days available in these habitats. On forest ponds, only univoltine life cycles were possible, whereas on field ponds temperature allowed bivoltine life cycles. However, only the eggs laid at the very beginning of the season had the potential to accumulate enough degree‐days to complete a bivoltine life cycle with both generations long‐winged. We conclude that thermal energy is the main environmental constraint limiting voltinism of populations in the two habitat types. Furthermore, the available thermal energy also seems to influence the determination of the seasonal wing pattern in G. lacustris.     

Costs of loading associated with mate-carrying in the waterstrider, Aquarius remigis

When one sex carries the other during some phase of courtshipor mating, the associated loading may entail a significant costto the carrier. This paper presents a series of laboratory experimentsdesigned to identify the costs of mate-carrying in Aquariusremigis. Female A. remigis mate repeatedly and carry each matefor several hours. Dead males and lead weights were used tosimulate normal mating and loading associated with mate-carrying,respectively. Females carrying weights equivalent to the weightof an average male showed no detectable reductions in survival,lipid reserves, or foraging success, and maintained themselveson the water surface for more than 10 days without access toresting sites. Weights equivalent to two males were supportedfor 6.1 ± 4.9 days. Thus, female A. remigis appear tobe very well adapted to carrying their mates and are unlikelyto be near their load limits when carrying a single mate. However,females carrying males or equivalent weights suffered a significantreduction in maximum mobility (stride length and speed), andan increased risk of predation by frogs (Rana clamitans). Femalescarrying weights were more susceptible to predation than unburdenedfemales but were less susceptible than females carrying males,suggesting that loading contributes significantly to, but doesnot fully explain, the increased predation risk. This risk probablyresults from both reduced mobility due to loading and greatervisibility (size). Possible influences of the costs of loadingon mating behavior and sexual size dimorphism are discussed.     

Avoidance of egg parasitism through submerged oviposition by tandem pairs in the water strider, Aquarius paludum insularis (Heteroptera: Gerridae)

Abstract.  1. Females of the water strider Aquarius paludum insularis (Motschulsky) (Heteroptera: Gerridae) carry males on their backs and oviposit under water after copulation. This study focuses on the benefit  A. paludum insularis receives by ovipositing in tandem.
2. Males guarded females in tandem through to the end of oviposition in 85% of copulations. Females in tandem dived deeper than single females, and the density of A. paludum insularis eggs increased with water depth. The proportion of eggs parasitized by a scelionid wasp, Tiphodytes gerriphagus Marchal (Hymenoptera: Scelionidae) decreased with increasing water depth.
3. These results suggest that during oviposition guarding by males is beneficial for females, because it enables pairs to dive and lay eggs deeper and in oviposition sites where the risk of egg parasitism is lower.     

Glinal variation in morphology among eastern populations of the waterstrider, Aquarius remigis Say (Hemiptera: Gerridae)

We examined morphological variation among populations of the stream-dwelling waterstrider, Aquarius remigis. A previous analysis of allozyme variation along a transect from southern Quebec to southern North Carolina revealed two distinct 'types' of A. remigis, north and south of a transition zone in southern New York and northern Pennsylvania. To assess the concordance of morphological and allozyme differentiation, adults were sampled from 15 populations along the original transect, as well as 11 additional populations in New York, Connecticut and New Jersey. Eight measurements of leg and body size were taken of preserved individuals. Univariate and multivariate analyses (multiple regression, PCA, discriminant analysis) reveal significant differentiation between northern and southern populations with a transition zone between latitudes 39^oand 42^onorth. Strong clines within each region and a clear transition between regions support previous suggestions that there are two distinct 'types' of this species in eastern North America. The transition zone, in morphology coincides with that revealed by the allozyme variation, but extends further south. The covariance of allozyme frequency and morphometric traits suggests that differentiation has occurred through vicariance and secondary contact, and that in this system, cladistic and adaptive differentiation are coupled.     

The sexual arms race and phenotypic correlates of mating success in the waterstrider,Aquarius remigis (Hemiptera: Gerridae)

Intersexual conflicts over mating decisions may have an important impact on the evolution of mating behaviours and strategies and may develop into an arms race between the sexes. In waterstrider species, where intersexual conflict is known to occur, the evolution of male traits that allow them to overcome female reluctance to mate is expected. Reproductively active waterstriders,Aquarius remigis, were videotaped in the laboratory to examine the influence of total body length and front femoral width of males, male: female body size ratio, and female reproductive condition (number of mature eggs) on three variables associated with mating success: duration of the premating struggle, duration of mating, and number of successful matings. None of these behaviors was significantly correlated with the size ratio of the mating pair. However, total body length was negatively correlated with premating struggle duration, male front femoral width was positively correlated with number of successful matings, and number of mature eggs in females was positively correlated with duration of both the premating struggle and the mating itself. The relative influence of male sexual armaments and female choice on the outcome of mating interactions is discussed.     

Changes in life‐history traits of the water strider Aquarius paludum in accordance with global warming

Seasonal records of nymphs of the water strider Aquarius paludum Fabricius (Heteroptera: Gerridae) at a waterway in Kochi prefecture, Japan (33°00′N to 33°30′N), in 2007, show that populations of new generation adults occur four or more times during the year, in mid and late May; late July to early August; September; and October to November. In laboratory experiments, more than 50% of adults are reproductive, irrespective of photoperiod, and this ratio increases to 80% even under a short‐day LD 11.5 : 13.5 h photocycle, which corresponds to the winter season at Kochi (33°N). There is a diminishing photoperiodic response in relation to the induction of diapause compared with measurements made in previous years (1995–1997), suggesting that reproduction may be possible over a much longer period in the near future (and even in winter) if local climate warming is sustained. A high proportion of males sampled in 2008 have small testes and a high proportion of females do not have mature oöcytes even in summer. This contrasts with earlier data showing that the testis volume index for the same period is greater in 1995–1997, and that 75% of females have mature oöcytes. These changes suggest that the Kochi‐Nankoku population of A. paludum is beginning to show partial aestivation. Overwintering adults of both sexes are found to have no mature flight muscles in October/November 2008. This is in marked contrast with earlier data from 1995 and 2004. Adults that are reared in the laboratory also show a lower flight propensity in response to shorter day lengths. The absence of mature flight muscles in the autumn and lower flight propensity under shorter days may indicate a cessation of dispersal between the summer habitats and overwintering sites on land far from the waterways. Taken together, these data suggest that populations of A. paludum in the Kochi‐Nankoku region are continuing to show adaptive changes, apparently in relation to global warming.     

Comparing salinity tolerance in embryonic and larval development of two species of water strider,Aquarius paludum and Gerris latiabdominis (Hemiptera: Gerridae)

Water strider Aquarius paludum (Fabricius) is a cosmopolitan species colonizes mainly freshwater but occasionally brackish habitats throughout the Palearctic and Oriental regions. Water strider Gerris latiabdominis (Miyamoto) is a common species in Japan lives in temporary habitats as freshwater paddy fields. These two species often occur syntopically. We investigated differences in the developmental response to brackish water during embryonic and larval stages between the two species. Eggs were exposed to 0–1.8% NaCl solutions within 24 h of oviposition. Larvae of G. latiabdominis were exposed to salinities of 0, 0.5%, and 0.9% from the first instar until adult emergence. Limits of NaCl concentration for hatching were 1.3% and 1.0% for A. paludum and G. latiabdominis, respectively. The hatching rate of G. latiabdominis was lower than that of A. paludum at salinities ≥0.9%. The period of embryonic development of G. latiabdominis was more prolonged than that of A. paludum at a given salinity. Although the salinity tolerance of G. latiabdominis was lower than that of A. paludum, our results suggest G. latiabdominis has the physiological capacity to expand into brackish waters. High and low salinity tolerances of A. paludum and G. latiabdominis, respectively, reflect the relatively wide range of habitat salinities utilized by A. paludum and the relatively restricted habitats preferred by G. latiabdominis. The high salinity tolerance of A. paludum could be an important factor contributing to their cosmopolitan distribution because high tolerance to salinity means the possibility of them to be dispersed via ocean or sea to other continents and islands.     

Sex‐specific selection and sexual size dimorphism in the waterstrider Aquarius remigis

We estimated selection on adult body size for two generations in two populations of Aquarius remigis, as part of a long‐term study of the adaptive significance of sexual size dimorphism (SSD). Net adult fitness was estimated from the following components: prereproductive survival, daily reproductive success (mating frequency or fecundity), and reproductive lifespan. Standardized selection gradients were estimated for total length and for thorax, abdomen, genital and mesofemur lengths. Although selection was generally weak and showed significant temporal and spatial heterogeneity, patterns were consistent with SSD. Prereproductive survival was strongly influenced by date of eclosion, but size (thorax and genital lengths in females; total and abdomen lengths in males) played a significant secondary role. Sexual selection favoured smaller males with longer external genitalia in one population. Net adult fitness was not significantly related to body size in females, but was negatively related to size (thorax and total length) in males.     

Body size and fecundity in the waterstrider Aquarius remigis: a test of Darwin's fecundity advantage hypothesis

The general female bias in body size of animals is usually attributed to fecundity selection. While many studies have demonstrated a positive relationship between body size and fecundity, the most common interpretation of fecundity selection is that larger females have larger abdomens and can hold more eggs, yet the relationship between abdomen size and fecundity has rarely been examined. For the waterstrider, Aquarius remigis, we find a significant relationship between body size and fecundity and demonstrate that the target of fecundity selection is abdomen size. Thus, larger females have higher fecundities because they have larger abdomens and not because of their total size per se. The rate at which fecundity increases with increasing abdomen size exceeds that which would be expected due to a simple volume constraint and suggests that other factors, such as increased ability to obtain resources, may contribute to the increase in fecundity with body size. Selection intensities estimated from our data indicate that fecundity selection could be a significant selective force on both total and abdomen lengths. Previous studies have found that abdomen size increased faster than body size and thus, larger females had relatively larger abdomens. The relationship of abdomen length and thorax length in A. remigis is hypoallometric and indicates that larger females have relatively smaller abdomens. We hypothesize that this may reflect conservation of abdomen size in females developing under poor conditions. Finally, while egg size is not directly related to body size, we find a trade-off between egg size and number when female abdomen length is held constant, suggesting that selection on egg size may influence abdomen length only indirectly through its effects on fecundity.     

Vibratory signals enhance mate-guarding in a water strider (Hemiptera: Gerridae)

Mating males of the water strider Gerris remigisproduce vibratory signals when-single males grasp mating pairs. When played through live females with dead males on their backs, these signals repelled mating attempts by single males. A previous study showed that male mate-guarding enhances female foraging effectiveness in this species. Thus male mate-guarding signals also enhance female foraging effectiveness.