Dynamics of an ant-ant obligate mutualism: colony growth, density dependence and frequency dependence

In insect societies, worker vs. queen development (reproductive caste) is typically governed by environmental factors, but many Pogonomyrmex seed-harvester ants exhibit strict genetic caste determination, resulting in an obligate mutualism between two reproductively isolated lineages. Same-lineage matings produce fertile queens while alternate-lineage matings produce sterile workers. Because new virgin queens mate randomly with multiple males of each lineage type, and both worker and queen phenotypes are required for colony growth and future reproduction, fitness is influenced by the relative frequency of each lineage involved in the mutualistic breeding system. While models based solely on frequency-dependent selection predict the convergence of lineage frequencies towards equal (0.5/0.5), we surveyed the lineage ratios of 49 systems across the range of the mutualism and found that the global lineage frequency differed significantly from equal. Multiple regression analysis of our system survey data revealed that the density and relative frequency of one lineage decreases at lower elevations, while the frequency of the alternate lineage increases with total colony density. While the production of the first worker cohort is largely frequency dependent, relying on the random acquisition of worker-biased sperm stores, subsequent colony growth is independent of lineage frequency. We provide a simulation model showing that a net ecological advantage held by one lineage can lead to the maintenance of stable but asymmetric lineage frequencies. Collectively, these findings suggest that a combination of frequency-dependent and frequency-independent mechanisms can generate many different localized and independently evolving system equilibria.     

SEX RATIO SELECTION AND THE EVOLUTION OF ENVIRONMENTAL SEX DETERMINATION IN LABORATORY POPULATIONS OF MENIDIA MENIDIA

What happens when a population with environmental sex determination (ESD) experiences a change to an extreme environment that causes a highly unbalanced sex ratio? Theory predicts that frequency-dependent selection would increase the proportion of the minority sex and decrease the level of ESD in subsequent generations. We empirically modeled this process by maintaining five laboratory populations of a fish with temperature-dependent sex determination (the Atlantic silverside, Menidia menidia) in extreme constant temperature environments that caused highly skewed sex ratios to occur initially. Increases in the minority sex consistently occurred from one generation to the next across all five populations, first establishing and then maintaining a balanced sex ratio until termination of the experiment at 8 to 10 generations. The extent to which the level of ESD changed as balanced sex ratios evolved, however, was not consistent. Two populations that experienced high temperatures each generation displayed a loss of ESD, and in one of these ESD was virtually eliminated. This suggests that temperature-insensitive, sex-determining genes were being selected. In populations maintained in low temperature environments, however, the level of ESD did not decline. Instead, the response of sex ratio to temperature was adjusted upward or downward, perhaps by selection of sex-determining genes sensitive to higher (or lower) temperatures. The two different outcomes at low versus high temperatures occurred independent of the geographic origin of the founding population. Our results demonstrate that ESD is capable of evolving in response to selection.     

THE MAINTENANCE OF SPERM VARIABILITY: CONTEXT‐DEPENDENT SELECTION ON SPERM MORPHOLOGY IN A BROADCAST SPAWNING INVERTEBRATE

Why are sperm so variable despite having a singular, critical function and an intimate relationship with fitness? A key to understanding the evolution of sperm morphology is identifying which traits enable sperm to be successful fertilizers. Several sperm traits (e.g., tail length, overall size) are implicated in sperm performance, but the benefits of these traits are likely to be highly context dependent. Here, we examined phenotypic selection on sperm morphology of a broadcast spawning tube worm (Galeolaria gemineoa). We conducted laboratory experiments to measure the relationship between average sperm morphology and relative fertilization success across a range of sperm environments that were designed to approximate the range of sperm concentrations and ages encountered by eggs in nature. We found that the strength and form of multivariate selection varied substantially across our environmental gradients. Sperm with long tails and small heads were favored in high‐concentration environments, whereas sperm with long heads were favored at low concentrations and old ages. We suggest variation in the local fertilization environment and resulting differences in selection can preserve variability in sperm morphology both within and among males.     

A FIELD TEST FOR HOST-PLANT DEPENDENT SELECTION ON LARVAE OF THE APPLE MAGGOT FLY,RHAGOLETIS POMONELLA

Host-plant dependent fitness trade-offs refer to traits that enhance the performance of an insect on one plant species to its detriment on others. Such trade-offs are central to models of sympatric speciation via host shifts, but have proven difficult to empirically demonstrate. Here, we test for host-plant dependent selection on larvae of apple (Malus pumila L.)- and hawthorn (Crataegus mollis L. spp.)-infesting races of Rhagoletis pomonella (Walsh). Samples of larvae were reared in the field and under protective conditions in a garage. Our rationale was that the garage should slow rates of fruit rot relative to the field, relaxing selection pressures associated with declining fruit quality. Four findings emerged from the study. (1) Larvae suffered higher mortality in fruits in the field than the garage. (2) The increase in mortality was greater for larvae in haws. (3) Larvae possessing the alleles Me 100, Acon-2 95, and Mpi 37, three allozymes displaying host-related differentiation in R. pomonella that map to linkage group II in the fly, left fruits earlier than other genotypes. (4) Allele frequencies for Me 100, Acon-2 95, and Mpi 37 were significantly higher in both apple and haw larvae surviving the field versus the garage treatment. Our results suggested that field conditions favored larvae that rapidly developed and left rotting fruits. Since these individuals tended to possess the alleles Me 100, Acon-2 95, and Mpi 37, frequencies of these allozymes were higher in the field. Selection on larvae was directional for Me 100, Acon-2 95, and Mpi 37 (or linked genes) in both host races. We previously showed that these same alleles can be disfavored in the pupal stage, especially in the apple race, where they correlate with premature diapause termination. Fitness trade-offs in Rhagoletis may therefore be due as much to differences in the relative strengths of directional selection pressures acting on different life stages as to disruptive selection affecting any one particular stage. The necessity to consider details of the entire life-cycle highlights one of the many challenges posed to documenting fitness trade-offs for phytophagous insects.     

RESPONSES OF FLORAL TRAITS TO SELECTION ON PRIMARY SEXUAL INVESTMENT IN SPERGULARIA MARINA: THE BATTLE BETWEEN THE SEXES

Two widespread assumptions underlie theoretical models of the evolution of sex allocation in hermaphroditic species: (1) resource allocations to male and female function are heritable; and (2) there is an intrinsic, genetically based negative correlation between male and female reproductive function. These assumptions have not been adequately tested in wild species, although a few studies have detected either genetic variation in pollen and ovule production per flower or evidence of trade-offs between male and female investment at the whole plant level. It may also be argued, however, that in highly autogamous, perfect-flowered plant taxa that exhibit genetic variation in gamete production, strong stabilizing selection for an efficient pollen:ovule ratio should result in a positive correlation among genotypes with respect to mean ovule and mean pollen production per flower. Here we report the results of a three-generation artificial selection experiment conducted on a greenhouse population of the autogamous annual plant Spergularia marina. Starting with a base population of 1200 individuals, we conducted intense mass selection for two generations, creating four selected lines (high and low ovule production per flower; high and low anther production per flower) and a control line. By examining the direct and correlated responses of several floral traits to selection on gamete production per flower, we evaluated the expectations that primary sexual investment would exhibit heritable variation and that resource-sharing, variation in resource-garnering ability, or developmental constraints mold the genetic correlations expressed among floral organs. The observed direct and correlated responses to selection on male and female gamete production revealed significant heritabilities of both ovule and anther production per flower and a significant negative genetic correlation between them. When plants were selected for increased ovules per flower over two generations, ovule production increased and anther production declined relative to the control line. Among plants selected for decreased anthers per flower, we observed a decline in anther production and an increase in ovule production relative to the control line. In contrast, the lines selected for low ovules per flower and for high anthers per flower exhibited no evidence for significant genetic correlations between male and female primary investment. Correlated responses to selection also indicate a genetically based negative correlation between the production of normal versus developmentally abnormal anthers (staminoid organs); a positive correlation between the production of ovules versus staminoid organs; and a positive correlation between the production of anthers and petals. The negative relationship between male versus female primary investment supports classical sex allocation theory, although the asymmetrical correlated responses to selection indicate that this relationship is not always expressed.     

A SEX DIFFERENCE IN THE PROPENSITY TO ENTER DIRECT/DIAPAUSE DEVELOPMENT: A RESULT OF SELECTION FOR PROTANDRY

In monandrous mating systems with discrete nonoverlapping generations males should maximize the expected number of matings by starting to emerge before females. This is known as protandry. Moreover, Evolutionarily Stable Strategies (ESS) models show that the male emergence curve should be abruptly truncated before female emergence has ceased. In temperate areas where many insects have partial second generations, we accordingly predict that males should enter diapause development at an earlier date than should females, as a result of late-emerging males being penalized in terms of fewer mating opportunities. The decision to diapause or to develop directly is usually mediated by response to environmental stimuli of which day length is the most important. Hence we predict that the mechanism by which males enter diapause at an earlier date than females will be that of the male reaction norm for diapause development being shifted towards longer day lengths when compared to that of females. As a result of the greater tendency of males to enter diapause development, partial second generations that develop directly should be female biased. As a corollary, first generations should be male biased because some males of the first generation are from the previous year. The prediction that males should enter diapause development earlier in the season, i.e., at longer day lengths, as compared to females was corroborated by rearing Pieris napi under a variety of critical day length regimes producing mixed broods of directly developing and diapausing individuals, and by outdoor rearings of cohorts of larvae of P. napi and P. rapae initiated throughout the season. The prediction that partial second generations should be female biased was corroborated by laboratory rearings at constant temperature of P. napi (Pieridae), Polygonia c-album (Nymphalidae), and Pararge aegeria (Satyridae) under critical day length conditions, producing female-biased sex ratio under direct, and male-biased sex ratio under diapause development.     

THE RESPONSE TO SELECTION FOR FAST LARVAL DEVELOPMENT IN DROSOPHILA MELANOGASTER AND ITS EFFECT ON ADULT WEIGHT: AN EXAMPLE OF A FITNESS TRADE-OFF

A selection experiment using Drosophila melanogaster revealed a strong trade-off between adult weight and larval development time (LDT), supporting the view that antagonistic pleiotropy for these two fitness traits determines mean adult size. Two experimental lines of flies were selected for a shorter LDT (measured from egg laying to pupation). After 15 generations LDT was reduced by an average of 7.9%. The response appeared to be controlled primarily by autosomal loci. A correlated response to the selection was a reduction in adult dry weight: individuals from the selected populations were on average 15.1% lighter than the controls. The lighter females of the selected lines showed a 35% drop in fecundity, but no change in longevity. Thus, there is no direct relationship between LDT and adult longevity. The genetic correlation between weight and LDT, as measured from their joint response to selection, was 0.86. Although there was weak evidence for dominance in LDT, there was none for weight, making it unlikely that selection acting on this antagonistic pleiotropy could lead to a stable polymorphism. In all lines, sex differences in weight violated expectations based on intrasex genetic correlations: Females, being larger than males, ought to require a longer LDT, whereas there was a slight trend in the opposite direction. Because the sexual dimorphism in size was not significantly altered by selection, it appears that the controlling loci are either invariant or have very limited pleiotropic effect on developmental time. It is suggested that they probably control some intrinsic, energy-intensive developmental process in males.