Seaweed Fly Research Articles

The effects of exposure to seaweed on willingness to mate, oviposition, and longevity in seaweed flies

Abstract 1. Large male seaweed flies (Diptera: Coelopidae) are more likely to mate than smaller males. This is due to sexual conflict over mating, by which females physically resist male attempts to copulate. In some species, large males are simply more efficient at overpowering female resistance.2. Female reluctance to mate is likely to have evolved due to the costs of mating to females. In many dipterans, males manipulate female behaviour through seminal proteins that have evolved through sperm competition. This behavioural manipulation can be costly to females, for example forcing females to oviposit in sub‐optimal conditions and increasing their mortality.3. Previous work has failed to identify any ubiquitous costs of mating to female coelopids. The work reported here was designed to investigate the effects of exposure to oviposition sites (Fucus algae) on the reproductive behaviour of four species of coelopid. Algae deposition in nature is stochastic and females mate with multiple males in and around oviposition sites. Spermatogenesis is restricted to the pupal stage and there is last‐male sperm precedence. It was predicted that males would avoid wasting sperm and would be more willing to mate, and to remain paired with females for longer, when exposed to oviposition material compared with control males. Females were predicted to incur longevity costs of mating if mating increased their rate of oviposition, especially in the presence of algae.4. The behaviour of males of all four species concurred with the predictions; however mating did not affect female receptivity, oviposition behaviour, or longevity. Exposure to algae induced oviposition and increased female mortality in all species independently of mating and egg production. The evolutionary ecology of potential costs of mating to female coelopids are discussed in the light of these findings.

Intraspecific molecular variation in the seaweed fly Coelopa frigida consistent with behavioural distinctness of British and Swedish populations.

The major aim of this study was to compare the intraspecific variation and genetic structure of the behaviourally distinct British and Swedish populations of the seaweed fly Coelopa frigida. C. frigida has been the subject of intense study into the basis of female choice. The behaviour of British females is consistent with a 'good genes' model, whereas that of the Swedish flies suggests a Fisher process, in which the difference between the former and the latter is defined by female choice increasing offspring viability in 'good genes' models. Through a study of variability in the mitochondrial cytochrome oxidase II gene from more than 600 flies, we show that there is clear differentiation at the molecular level between the two countries' populations, with an FST of > 75% and no shared haplotypes. Tajima's test reveals an excess of rare variants relative to expectation, which, if not the result of selective sweep, indicates either a population expansion or purifying selection against weakly deleterious variants. Within the two populations, substantial subpopulation differentiation is observed in the UK, where there is also evidence of isolation by distance. Swedish populations exhibit lower variability, and no evidence of isolation by distance, with the latter result possibly being related to the continuous distribution of suitable habitat. The pattern of intraspecific variation is explainable by a combination of contemporary and also historical factors. British and Swedish populations may have been descended from at least two separate founding populations during the recolonization of these areas following Pleistocene glaciations.

Mate sampling and the sexual conflict over mating in seaweed flies

The order in which females encounter, or sample, males in a population may have important consequences for mate choice, with the information gathered about males influencing both the preference function and degree of choosiness of females. Sexual selection may be affected as a result. Sampling of particular subsets of males may be a crucial component of individual variation in mate preferences within populations. However, the sequence in which males are sampled may also be important in species without traditional, active mate choice, such as when sexual selection involves sexual conflict over mating. This would occur if the likelihood of a female mating with a male of a certain phenotype changes as a result of previous encounters. We examined the effects of encountering males differing in body size, a sexually selected phenotype, in the seaweed fly Coelopa frigida. Sexual selection occurs in this species as a result of a sexual conflict over mating. We show that the outcome of the sexual conflict is independent of the order in which males are encountered by female seaweed flies, with the overall mating advantage to large males being unaffected. In addition, we explored female preference functions and evaluate the heterogeneity in female willingness to mate. We suggest that consideration of mate sampling theory is valuable when examining mate choice in species in which sexual selection is driven by sexual conflict. Copyright 2002.

Age before beauty: male flies prefer long-lived females

The issue of which indicators animals use as the basis for choosing a mate has been at the heart of evolutionary biology since its inception. In most cases, females are the choosy sex, and this is evident in the enormous array of sexually selected traits that male animals display. However, on the rare occasions where the supply of females outstrips demand, males get to choose. In such cases, males normally favour fecundity (or a correlate, such as body size). However, a recent paper by Derek Dunn and colleagues 1 Dunn D.W. et al. Male mating preference for female survivorship in the seaweed fly Gluma musgravei (Diptera: Coelopidae). Proc. R. Soc. London B Biol. Sci. 2001; 268: 1255-1258 Crossref Scopus (12) Google Scholar suggests that males of the seaweed fly Gluma musgravei (Diptera: Coelopidae) choose females not on the basis of how many eggs they have, but on their future longevity. This is the first demonstration in any species of a male preference for future survivorship in a mate.

Male mating preference for female survivorship in the seaweed fly Gluma musgravei (Diptera: Coelopidae).

The seaweed fly mating system is characterized by pre-mating struggles during which females exhibit a mate rejection response involving kicking, shaking and abdominal curling. Males must resist rejection until females become passive and allow copulation to take place. However, despite the vigorous nature of the struggle males frequently dismount passive females without attempting copulation. Here we show that rejected females suffered higher post-encounter mortality rates than those accepted by males in the seaweed fly Gluma musgravei. Furthermore, we show that males also preferentially mounted females with higher future longevity. We propose that this male mate choice for female survivorship has evolved as a result of females often having to survive for long periods after mating until suitable oviposition sites become available. Such male preferences for female survivorship may be common in species in which oviposition must sometimes be substantially delayed after mating.

The repeatability of a sexual conflict over mating

Measuring individual variation in mating behaviour is an integral part of studies of sexual selection and of considerable theoretical importance. Few studies, however, have examined individual variation in mating behaviour in a sexual conflict system and considered how individual variation influences the strength and consistency of the resulting sexual selection. We examined variation in mating behaviour of male and female pairs in the seaweed fly, Coelopa frigida. Sexual selection in seaweed flies occurs as a result of a sexual conflict over mating, with larger males generally able to overcome female rejection responses. We explored male and female mating conflicts and examined the variation in conflict outcomes within and between pairs. First, female willingness to mate was unaffected by short-term mating experience, allowing us to examine repeated interactions between a male and a female. Second, the outcomes of the sexual conflict over mating (copulation or rejection), and components of the mating interaction (number of copulations and time the male is mounted), were strongly repeatable. Third, the patterns of sexual selection on male size were consistent across mounts. Individual pairs consistently gave the same outcome to the mating conflict and yielded consistent sexual selection. Sexual conflict systems can thus be studied in the same way as those with more traditional forms of sexual selection and yield important insights into the links between variation in mating behaviour and sexual success.

Critical thermal limits, temperature tolerance and water balance of a sub-Antarctic kelp fly, Paractora dreuxi (Diptera: Helcomyzidae)

Paractora dreuxi displays distinct ontogenetic differences in thermal tolerance and water balance. Larvae are moderately freeze tolerant. Mean larval onset of chill coma was −5.1°C, and onset of heat stupor was 35.5°C. Larval supercooling point (SCP) was −3.3°C with 100% recovery, although mortality was high below −4°C. Starvation caused SCP depression in the larvae. Adults were significantly less tolerant, with critical thermal limits of −2.7 and 30.2°C, no survival below the SCP (−9.6°C), and no change in SCP with starvation. Moderate freeze tolerance in the larvae supports the contention that this strategy is common in insects from southern, oceanic islands. Fly larvae survived desiccation in dry air for 30 h, and are thus less desiccation tolerant than most other sub-Antarctic insect larvae. Water loss rates of the adults were significantly lower than those of the larvae. Lipid metabolism did not contribute significantly to water replacement in larvae, which replaced lost body water by drinking fresh water, but not sea water. Kelp fly larvae had excellent haemolymph osmoregulatory abilities. Current climate change has led to increased temperatures and decreased rainfall on Marion Island. These changes are likely to have significant effects on P. dreuxi, and pronounced physiological regulation in larvae suggests that they will be most susceptible to such change.

Female mate choice for large males in several species of seaweed fly (Diptera: Coelopidae)

The mating system of the seaweed fly Coelopa frigida involves a vigorous premating struggle during which females attempt to dislodge mounted males by kicking and shaking from side to side. Additionally females can prevent engagement of genitalia by curling their abdomens downwards. Large males gain a mating advantage. Male size is partially determined by a chromosomal inversion polymorphism which is maintained by strong heterosis. Thus female mate choice on the basis of size will affect offspring fitness. We report the occurrence of premating struggles and mate choice for large males in five additional species of seaweed fly, namely, C.nebularum, C.vanduzeei, C.pilipes, Gluma musgravei andG.nitida . Four of these species appear to lack the inversion system, suggesting that mate choice for large males can be maintained in its absence and also evolved before its establishment. Gluma females had stronger preferences thanCoelopa females and showed an additional response to mounting, namely, curling their abdomens upwards into the male. This may allow assessment of male size.

Male choice, willingness to mate and body size in seaweed flies (Diptera: Coelopidae)

The mating system of seaweed flies is characterized by scramble competition and a premating struggle during which females vigorously attempt to remove mounted males and prevent copulation. Here we investigate factors affecting the willingness of males to mate in five species ofCoelopa:C.frigida, C.nebularum, C.ursina, C.pilipesandC.vanduzeei. The data from 2000 individual observations of pairs of flies revealed no association between female size and the willingness of males to mate, suggesting that males do not exhibit mate choice for larger, more fecund females. Male willingness to mount was associated with male size inC.frigida, C.nebularumandC.ursina, although not inC.pilipesandC.vanduzeei. There is considerable intraspecific variation in male size in the former three species, including the presence of two almost discrete size classes withinC.nebularum. We suggest that males of different sizes in these species may be adopting alternative reproductive strategies. Large males may benefit from increased longevity and their ability to withstand female rejection responses, whereas small males are more active and thus likely to encounter and mount more females. In addition small males develop faster and thus gain earlier access to females.

Female mating behaviour, sexual selection and chromosome I inversion karyotype in the seaweed fly, coelopa frigida

Previous studies of the seaweed fly, Coelopa frigida, have revealed the operation of several different forces of sexual selection. The overall pattern of mate choice seen in natural populations is not consistent with the predictions of indirect sexual selection as females do not express preferences that maximize the fitness of their offspring, even though the benefits from such choice are relatively large in this species. Thus, the maintenance of female mate choice for large male size must instead either be a result of a direct benefit to the female of mating with large males, or a side-effect of the evolution of another character, in other words pleiotropy. In order to separate these two alternatives the genetical basis of female mating behaviour needs to be studied. Previous studies have revealed associations between chromosomal inversion karyotype and both general female willingness to mate and mate choice for large male size, however these associations were lost after several generations of laboratory culture. Here several isokaryotypic lines from wild collections of flies were derived. The willingness to mate and mate choice of females from each line were determined. Pairs of lines of opposite inversion karyotype that significantly differed in either or both willingness to mate and mate choice were crossed. The mating behaviour and inversion karyotype of the F2 progeny (all F1 progeny are heterokaryotypes) were determined. Clear differences in the general levels of female willingness to mate were found between the two inversion homokaryotypes in several families, whereas variation in the strength of female choice for large male size were not revealed. It is suggested that mate choice in this species occurs as a pleiotropic effect of selection acting on female willingness to mate.

Sexual selection as a side-effect of sexual conflict in the seaweed fly,Coelopa ursina(Diptera: Coelopidae)

The mating system of the seaweed fly involves a premating struggle. When mounted, females violently try to remove the male. In this study 48% of premating struggles resulted in successful rejection of the male, 46% in copulation and 6% were terminated by the male. Large males had a mating advantage. However, contrary to what would be predicted if this sexual selection occurred as a result of active female mate choice, we found a positive association between the duration of premating struggles and male size. A positive association was also found between the duration of premating struggles and male mating success, suggesting that large males may benefit through their superior ability to withstand female rejection. Large females rejected males more easily than small females, suggesting that the premating struggle has not evolved to allow mate assessment by females. We conclude that sexual selection is occurring as a side-effect of the female rejection response, which has probably evolved in order to avoid costs associated with copulation. Nevertheless, a sexual size dimorphism has evolved with males being larger and much more variable in size than females.

Asymmetric Interactions between Species of Seaweed Fly

1. This paper describes the colonization patterns of, and interactions between, three common species of British seaweed fly: the coelopids, Coelopa frigida and C. pilipes; and the sphaerocerid, Thoracochaeta zosterae. 2. All three species exhibited similar temporal patterns in abundance on wrack beds in the field: adult flies were more abundant in the first 4 days after wrack deposition and then again towards the end of the wrack bed cycle, coinciding with the emergence of the next generation. 3. Two forms of resource were presented to the flies, minced and chopped seaweed (Fucus serratus), under controlled environmental conditions. The species interacted so as to produce a dominance series, with C. frigida being the strongest species and T. zosterae the weakest. All pairwise interactions were extremely asymmetric, adding support to the growing awareness that this phenomenon is common in interactions between insects. 4. On chopped seaweed only, C. pilipes facilitated C. frigida, more than doubling the latter's emergent population size. This facilitation, in conjunction with the inhibition of C. pilipes by C. frigida, produced a contramensal (+, -) interaction. Suggestions are made as to how the facilitative effect may have been produced, but the exact mechanism is not yet understood.

September diet and reproductive state ofUta stansburiana(Phrynosomatidae) at Isla San Roque, Baja California Sur, México

In September 1994 we studied the only reptile species,Uta stansburiana elegans, at Isla San Roque off the Pacific coast of Baja California Sur. Three censuses of lizards were made over all the island. Outside the census transect, 10 adult lizards of each sex were collected. Analysis of data obtained from the reproductive tracts and stomach contents are shown. A seaweed fly of the family Coelopidae (Diptera) was the principal prey. Behavioural data suggested the existence of reproductive activity in the lizard individuals seen, which was confirmed by analysis of the reproductive tract.

Sperm numbers, their storage and usage in the flyDryomyza anilis

In the fly Dryomyza anilis females have two kinds of sperm storage organs: one bursa copulatrix and three spermathecae (two spermathecae with a common duct form the doublet, and the third is a singlet spermathecal unit). At the beginning of a mating the male deposits his sperm in the bursa copulatrix. After sperm transfer the male taps the female's abdomen with his claspers. This behaviour has been shown to increase the male's fertilization success. After mating, the female discharges large quantities of sperm before oviposition. To find out where the sperm remaining in the female are stored, I counted the number of sperm in the droplet and in the female's sperm storage organs after different types of mating. I carried out three mating experiments. In experiment 1, virgin females were mated with one male and the matings were interrupted either immediately after sperm transfer or after several tapping sequences. The results show that during male tapping more sperm moved into the singlet spermatheca. In addition, the total number of sperm correlated with sperm numbers in all sperm storage organs, and male size was positively related to the number of sperm remaining in the bursa. In experiment 2, females mated with several males. The number of sperm increased with increasing number of matings only in the doublet spermatheca. No increase in the number of sperm in the singlet spermatheca during consecutive matings suggests that sperm were replaced or did not reach this sperm storage organ. In experiment 3, virgin females were mated with a single male and half of them were allowed to lay eggs. The experiment showed that during egglaying, females primarily used sperm from their singlet spermatheca. The results from the three experiments suggest that sperm stored in the singlet spermatheca is central for male fertilization success and male tapping is related to sperm storage in the singlet spermatheca. The different female's sperm storage organs in D. anilis may have separate functions during sperm storage as well as during sperm usage.

SEXUAL SELECTION OPERATING IN A WILD POPULATION OF DROSOPHILA ROBUSTA.

Almost 60 years have elapsed since the discovery of variation in the polytene chromosomes of Drosophila (Sturtevant and Dobzhansky 1936). Inversion polymorphism studies have revealed some of the intricacies of evolutionary change, but even now, when interest in them has waned, there is little understanding of the particular alleles contained within them that alone or in relation to other genes influence any component of fitness. Perhaps the most important rule about inversion polymorphisms learned from a long history of laboratory experiments (cf. Lewontin et al. 1981) is their sensitivity to environmental features such as temperature and nutrition. Therefore, laboratory studies alone may not predict the consequences due to genotype (karyotype) by environment interactions of selection in wild populations. Only a few studies have documented selective mechanisms associated with preserving inversion polymorphisms in natural populations beyond establishing correlations with temperature, rainfall, humidity, elevation, and other environmental features. Despite the long history of interest in the ecology of Drosophila breeding and feeding sites (cf. Carson 1951, 1971; Heed 1957, 1968, 1971), experimental analyses of inversion polymorphisms involving natural breeding substrates are few because the mating sites and larval ecology of most species with well described inversion polymorphisms are poorly known, e.g., D. pseudoobscura. An early exception to this problem was the comprehensive study of inversion polymorphism in D. flavopilosa, a flower breeder from South America (Brncic 1962). Egg to adult viability differences among karyotypes were observed among preadult stages in flowers returned to the lab and exposed to contrasting temperatures (Brncic 1968). More recently, analysis of the sexratio meiotic drive system in natural populations of D. pseudoobscura suggested that most selection responsible for maintaining this polymorphism must be operating in preadult stages (Beckenbach 1996). A notable non-Drosophila example is the chromosome I polymorphism in seaweed flies, Coelopa frigida, that carry out their life cycle on decomposing seaweed on beaches around the north Atlantic and North Sea. Gene arrangement-based differences in egg to adult development time, adult body size, and mate preference have been demonstrated in seaweed-reared flies (Day et al. 1983; Engelhard et al. 1989; Gilburn et al. 1992). For species that can be collected in nature throughout their life cycle, karyotype frequencies can be estimated from life stages reared in the wild and comparisons can be made between stages of the life cycle in selection component analyses (e.g., Prout 1971; Bundgaard and Christiansen 1972). Inversion polymorphisms in cactophilic D. buzzatii have been studied this way, a species that feeds and breeds in the fermenting tissues of several species of prickly pear cactus. In general, cactophilic Drosophila have taught us much about maintenance of genetic variability, host specificity, chemical ecology, trophic adaptation, and life history evolution (Barker and Starmer 1982; Barker et al. 1990). Despite the fact that 48% (44/91) of all described and undescribed D. repleta group species possess inversion polymorphism (Wasserman 1992), in only a few species has there been concerted effort to unravel the causes for maintenance of inversion polymorphism in nature, that is, D. buzzatii and D. mojavensis. Inversion polymorphism in the latter species, along with D. pachea, a cactophilic member of the D. nannoptera group, has been recently summarized (Etges et al., in press). Ruiz et al. (1986) demonstrated endocyclic selection, directional selection in opposing directions during the life cycle, on gene arrangements of D. buzzatii. However, this pattern is population and host specific (Hasson et al. 1991) and not surprisingly is limited to a few components of fitness including egg to third instar viability and adult body size, but not mating propensity (Santos et al. 1992; Barbadilla et al. 1994). Adult size in Drosophila can be correlated with increased fitness as larger flies typically have greater reproductive potential (Robertson 1957) and dispersal ability (Mangan 1982). These studies of D. buzzatii deserve special note because they illustrate the complexity of factors that must be addressed in understanding the maintenance of inversion polymorphisms in natural populations. Thus, studies of selection on inversion polymorphisms in species with hard-to-find breeding sites have been restricted to adult flies because they can be captured in the wild. If we include the recent D. buzzatii studies mentioned above, several studies of genetic variation in male mating success (Anderson et al. 1979; Levine et al. 1980; Salceda and Anderson 1988), the recent analysis of the sex-ratio polymorphism in D. pseudoobscura (Beckenbach 1996), and mate choice in seaweed flies (Gilburn et al. 1992), most of what we know of selection operating on inversion polymorphisms under natural conditions has only recently been documented. It is interesting to note that not one example documenting an identifiable selective agent operating on inversion polymorphisms was cited by Endler (1986) in his review, Natural Selection in the Wild, despite the long history of population genetics

Sexual selection in seaweed flies: genetic variation in male size and its reliability as an indicator in natural populations

Characters that are evolving in response to indirect sexual selection operating through the production either of attractive sons (the Fisher process) or of progeny with high viability (good genes), are expected to exhibit high levels of additive genetic variation. In seaweed flies ( Coelopa frigida ) male size is subject to both direct and indirect sexual selection, whereas female size has probably evolved in response to direct selection alone. Coefficients of additive genetic variance ( CV A 9s) in adult size were shown to be larger in males than females. Virtually all the genetic variation is attributable to the αβ chromosomal inversion which is known to be associated with larval survival. Sexual selection appears to have led to differential expression of relevant loci in the two sexes, and in the focussing of this variation into a single region of the genome. Samples from 25 natural populations provided estimates of CV A 9s in male size. Although the CV A values suggest male size is, on average, a reliable indicator of offspring fitness, both spatial and temporal differences in CV A ’s were observed. We suggest that indirect sexual selection is a very inconstant force of evolution.

Sexual selection in natural populations of seaweed flies: variation in the offspring fitness of females carrying different inversion karyotypes

The effect of indirect sexual selection on offspring fitness with respect to a large chromosomal inversion system was estimated in nine widely separated populations of the seaweed fly, Coelopa frigida. The pattern of female rejection was determined for each population and estimates were made of the relative fitnesses of the inversion karyotypes. Two sets of progeny frequencies were calculated: the first on the basis of the observed pattern of mating, and the second on the hypothetical basis that all females had accepted the male available: in other words, random mating. The relative fitnesses of the offspring produced by these two mating regimes were compared. In seven of the populations the exercise of choice resulted in a modest change in progeny fitness. The change depended on the karyotype of the female: $\beta \beta $ females produced fitter offspring in all populations, $\alpha \alpha $'s usually produced less fit offspring, and there was little effect on the progeny of $\alpha \beta $'s. An association was also found between a physical factor, tidal range, and the offspring fitness of $\alpha \alpha $ females, but no association exists for $\alpha \beta $ or $\beta \beta $ females. It is suggested that the relevant genes have been subject to different evolutionary forces on the two forms of the inversion.

The genetic effects of competition in seaweed flies

In spite of abundant evidence that intra- and inter-specific competition occurs in natural communities, there is surprisingly little to suggest it is a major force promoting genetic change. This report assesses the genetic effects of competition in two species of seaweed fly,Coelopa frigidaandC. pilipes. In laboratory cultures ofC. frigidathe relative survival of heterozygotes at theAdhlocus, which was being used as a marker for the large αβ chromosomal inversion, was greater than that of homozygotes. In monocultures ofC. frigidathis competitive superiority was dependent on larval density. At low densities facilitation was seen, whereas at high larval densities there was competition. In mixed cultures of the two species, interspecific competition contributed to the differential mortality ofC. frigida, and observations of natural populations suggested that competition may have similar effects to those described in laboratory culture. A possible mechanism involving the supply of nutritive microorganisms is proposed to underly both intra- and inter-specific competition. In seaweed flies, competition and the consequent differential mortality appear to be forces maintaining rather than reducing genetic variation.

The genetic effects of competition in seaweed flies

In spite of abundant evidence that intra- and inter-specific competition occurs in natural communities, there is surprisingly little to suggest it is a major force promoting genetic change. This report assesses the genetic effects of competition in two species of seaweed fly, Coelopa frigida and C. pilipes. In laboratory cultures of C. frigida the relative survival of heterozygotes at the Adh locus, which was being used as a marker for the large αβ chromosomal inversion, was greater than that of homozygotes. In monocultures of C. frigida this competitive superiority was dependent on larval density. At low densities facilitation was seen, whereas at high larval densities there was competition. In mixed cultures of the two species, interspecific competition contributed to the differential mortality of C. frigida, and observations of natural populations suggested that competition may have similar effects to those described in laboratory culture. A possible mechanism involving the supply of nutritive microorganisms is proposed to underly both intra- and inter-specific competition. In seaweed flies, competition and the consequent differential mortality appear to be forces maintaining rather than reducing genetic variation.

The evolution of female choice when the preference and the preferred trait are linked to the same inversion system

This study reports results of computer simulations of the evolution of female mating preferences when both the preference and the preferred character are associated with the same chromosomal inversion system. When there is strong heterosis associated with the inversion system and no direct selection acting on mating preferences, a pattern of disassortative mating with respect to the inversion is predicted to evolve. Females mating disassortatively produce highly fit heterokaryotypic offspring. However, when heterosis is weak, Fisherian sexual selection can maintain strong assortative preferences, but the inversion polymorphism is lost. Assortative preferences are only likely to be maintained in conjunction with a polymorphic inversion system if direct sexual selection is operating. The results of this study are discussed with respect to the seaweed fly, Coelopa frigida, in which the preference and preferred trait are associated with the αβ inversion system.