The molecular basis of melanism and mimicry in a swallowtail butterfly

Melanism in Lepidoptera, either industrial or in mimicry, is one of the most commonly cited examples of natural selection [1] [2]. Despite extensive studies of the frequency and maintenance of melanic genes in insect populations [1] [2], there has been little work on the underlying molecular mechanisms. Nowhere is butterfly melanism more striking than in the Eastern Tiger Swallowtail (Papilio glaucus) of North America [3] [4] [5]. In this species, females can be either yellow (wild type) or black (melanic). The melanic form is a Batesian mimic of the distasteful Pipevine Swallowtail (Battus philenor), which is also black in overall color. Melanism in P. glaucus is controlled by a single Y-linked (female) black gene [6]. Melanic females, therefore, always have melanic daughters. Black melanin replaces the background yellow in melanic females. Here, we show that the key enzyme involved is N-beta-alanyl-dopamine-synthase (BAS), which shunts dopamine from the melanin pathway into the production of the yellow color pigment papiliochrome and also provides products for cuticle sclerotization. In melanic females, this enzyme is suppressed, leading to abnormal melanization of a formerly yellow area, and wing scale maturation is also delayed in the same area. This raises the possibility that either reduced BAS activity itself is preventing scale sclerotization (maturation) or, in contrast, that the delay in scale maturation precludes expression of BAS at the correct stage. Together, these data show how changes in expression of a single gene product could result in multiple wing color phenotypes. The implications for the genetic control of mimicry in other Lepidoptera are discussed.     

Divergence in the ovipositional behavior of the Papilio glaucus group

This study contrasts the ovipositional profiles of four members of the Papilio glaucus group, P. glaucus , P. multicaudatus , P. canadensis , and P. rutulus. We used seven choice oviposition bioassays containing leaves from hosts in seven plant families utilized by members of the P. glaucus group. Specifically, we contrast the overall ovipositional profiles of these species and their acceptance of a host in a novel plant family ( Populus tremuloides : Salicaceae) and a host in a putatively ancestral host plant family ( Liriodendron tulipifera : Magnoliaceae). Significant differences were observed between the ovipositional profiles of P. glaucus and P. multicaudatus relative to each other and to P. canadensis and P. rutulus. In contrast, no significant differences were observed between the ovipositional profiles of P. canadensis and P. rutulus , which were also the only species that accepted P. tremuloides. Unlike the acceptance of P. tremuloides , the acceptance of L. tulipifera was present throughout the group despite the inability of the larvae of most species in the group to utilize this host. These results support the prediction of the "hierarchical threshold model" that ancestral host plants are likely to be retained in the ovipositional hierarchy while novel hosts should only be accepted by derived populations.     

The role of survival for the evolution of female philopatry in a solitary forager, the grey mouse lemur (Microcebus murinus)

It is widely accepted that natal philopatry is a prerequisite for the evolution of sociality. The life-history hypothesis maintains that longevity of adults results in extended territory tenure and thus limits breeding vacancies for offspring, which makes natal philopatry more likely. Here, we tested the importance of longevity for natal philopatry in females of a basal primate, the grey mouse lemur (Microcebus murinus). This species is regarded as being solitary due to its foraging habits but while males disperse, female offspring in this species forgo dispersal and form long-term sleeping groups with their mothers. We tested whether high adult survival could be a cause for natal philopatry of female offspring. In addition, we assessed costs and benefits associated with space sharing between mothers and daughters and whether mothers actively increase survival of daughters by beqeauthal of territories, information transfer about resources or thermoregulation. Contrary to our predictions, adult females had low-survival rates. Space sharing appeared to improve survival of both, mothers and daughters. This could be a result of information transfer about sleeping sites and thermoregulatory benefits. Our results cast doubt on the idea that longevity predisposes species for social traits and provide support for benefits of philopatry.     

Lack of Sex-Biased Maternal Investment in spite of a Skewed Birth Sex Ratio in White-Headed Langurs (Trachypithecus leucocephalus)

Numerous hypotheses have been developed to explain sex allocation. In male-dispersing, female cooperatively breeding species, the local resource competition model predicts male-biased birth sex ratio, the local resource enhancement model predicts female-biased birth sex ratio, and the population adjustment model predicts that biased birth sex ratio should not be favored if the two sexes are equally costly to rear. The male quality model predicts that, in polygynous species, females in better physical condition will either produce more sons than daughters or invest more heavily in sons than in daughters. White-headed langurs are a female philopatry and female cooperatively breeding species. During a 11-yr study, a total of 133 births were recorded, among which birth sex ratio (M:F = 73:49) was significantly male-biased. This is consistent with the prediction of the local resource competition model. On the other hand, if mothers balanced their investment between the two sexes, according to Fisher's population adjustment model, males should be the less-costly-to-rear sex. However, we found no sex difference for infant mortality (12.3% in males and 12.2% in females), and sons induced slightly longer interbirth interval (son: 26.4 ± 1.1 mo, daughter: 24.1 ± 0.6 mo) and lactational period (son: 20.9 ± 1.0 mo, daughters: 19.6 ± 0.5 mo) for their mothers. Thus, the population adjustment model was not supported by this study. The local resource enhancement model was not supported because birth sex ratio did not bias to females who provided more reproductive assistance. On the individual level, probit regression showed no relation between birth sex ratio and group size. Because the group size was considered to be negatively related to female physical condition, our study did not support the male-quality model. We suggested several possibilities to explain these results.     

GENETICS OF MIMICRY IN THE TIGER SWALLOWTAIL BUTTERFLIES,PAPILIO GLAUCUS AND P. CANADENSIS (LEPIDOPTERA: PAPILIONIDAE)

The tiger swallowtail butterfly, Papilio glaucus, exhibits a female-limited polymorphism for Batesian mimicry; the Canadian tiger swallowtail, Papilio canadensis, lacks the mimetic (dark) form entirely. The species hybridize to a limited extent where their ranges overlap. Field collections and censuses indicate that mimetic females occur throughout the range of P. glaucus but at lowest frequencies in populations at the latitudinal edges of its geographic range such as the southernmost part of Florida and along the entire northern edge of its distribution from Massachusetts to Minnesota. Frequencies of mimetic females have remained relatively stable over time. Inheritance of the mimetic form is controlled primarily by two interacting sex-linked loci. The typical matrilineal pattern of inheritance in P. glaucus can be explained by polymorphism at a Y-linked locus, b. Analysis of P. glaucus × P. canadensis crosses has also revealed an X-linked locus, s, which controls the expression of the mimetic phenotype. The P. canadensis allele, s^can, suppresses the mimetic phenotype in hybrid and backcross females. Results from more than 12 yr of rearing tiger swallowtails, including interspecies hybrids, indicate that the absence of mimetic P. canadensis females is due to both a high frequency of the “suppressing” allele s^can and low frequency of the black-pigment-determining b + allele. The frequency of s^can (or other suppressing alleles of s) in P. glaucus populations outside the hybrid zone is low. Some males heterozygous at the s locus and some suppressed mimetic females occur within the hybrid zone. A simple genetic model predicts the frequency of daughters that differ in phenotype from their mothers.     

Local adaptation and matching habitat choice in female barn owls with respect to melanic coloration

Local adaptation is a major mechanism underlying the maintenance of phenotypic variation in spatially heterogeneous environments. In the barn owl (Tyto alba), dark and pale reddish-pheomelanic individuals are adapted to conditions prevailing in northern and southern Europe, respectively. Using a long-term dataset from Central Europe, we report results consistent with the hypothesis that the different pheomelanic phenotypes are adapted to specific local conditions in females, but not in males. Compared to whitish females, reddish females bred in sites surrounded by more arable fields and less forests. Colour-dependent habitat choice was apparently beneficial. First, whitish females produced more fledglings when breeding in wooded areas, whereas reddish females when breeding in sites with more arable fields. Second, cross-fostering experiments showed that female nestlings grew wings more rapidly when both their foster and biological mothers were of similar colour. The latter result suggests that mothers should particularly produce daughters in environments that best match their own coloration. Accordingly, whiter females produced fewer daughters in territories with more arable fields. In conclusion, females displaying alternative melanic phenotypes bred in habitats providing them with the highest fitness benefits. Although small in magnitude, matching habitat selection and local adaptation may help maintain variation in pheomelanin coloration in the barn owl.     

Hot summer temperatures may stop movement of Papilio canadensis butterflies and genetic introgression south of the hybrid zone in the North American Great Lakes Region

The reasons that the northern tiger swallowtail butterfly Papilio canadensis does not move south of the Great Lakes hybrid zone, where it meets P. glaucus , may be largely due to natural temperature-induced stress on diapausing pupae. Temperatures of 36°C for only four days killed all P. canadensis (from northern Michigan) and most of the Papilio troilus , a species that lives south of the hybrid zone (sympatrically with P. glaucus ). In contrast, interspecific hybrids ( P. glaucus mother× P. canadensis father) had significant adult eclosion or pupal survival at both 30° and 36°C. All surviving hybrid pupae were only females (the heterogametic sex, which are known to express the prolonged diapause due to Haldane effects).
The southern species, P. troilus , had almost all (81%) normal (non-deformed) adults eclose at 30°C, whereas only 20% of the P. canadensis females and ca 30% of the P. canadensis males eclosed to produce non-deformed adults. Unlike the case with P. troilus and P. canadensis , no hybrid females eclosed at 30°C (only males did). Unlike P. troilus and P. canadensis pupae, hybrid (female) pupae remain viable, some of which have already successfully emerged after the chamber experiments.
A follow-up study using P. glaucus , P. canadensis (from Vermont), and their hybrids with more normal lower thermal regimes included (27°, 30°, 33°, and 36°C) again showed higher hybrid survival as uneclosed (living) pupae at 36°C. In addition, P. glaucus and P. canadensis showed high mortality and wing deformity of eclosing adults at 36°C, suggesting that geographic source of the P. canadensis may reflect differential tolerances of the extreme 36°C temperature.     

Successful sons or superior daughters: sex-ratio variation in springbok

Mothers would often benefit from producing more offspring of one sex than the other. Although some species show an astonishing ability to skew their sex ratio adaptively, the trends found in many studies on vertebrates have proved inconsistent. Furthermore, evidence for a mechanism by which such a bias is achieved is equivocal at best. Here, we examine sex-ratio variation over 30 years, both at an individual and a population level, in the highly polygynous, size-dimorphic springbok (Antidorcas marsupialis). Many previous studies of similar species have shown that mothers in superior condition preferentially produce sons, whereas those in poorer condition produce more daughters. We found the opposite to be true in springbok, perhaps because daughters provide mothers in superior condition with a more rapid and secure fitness return. This theory was supported by the findings that earlier-conceived offspring tended to be female and that an increased proportion of daughters were produced with increasing rainfall (which was likely to reduce nutritional stress). We also show that selective reabsorption of embryos is unlikely to be the main mechanism by which deviations from an equal sex ratio are achieved. Hence, either differential implantation occurs or females are able to influence the sex of the sperm fertilizing an egg.     

Effects of age, dominance, and seasonal changes on proximity relationships in female Japanese macaques (Macaca fuscata) in a free-ranging group at Katsuyama

The present study compares the behavior of old female Japanese macaques (Macaca fuscata) with that of their full adult daughters in a free-ranging group, with respect to dominance and seasonal changes. Old mothers (21 to 25 years old) spent more time resting and alone than did their middle-aged adult daughters (10 to 17 yr old). However, the number of skin-related animals in proximity to the subject females, did not differ between mothers and their adult daughters. Mothers maintained proximity to more non-kin-related immature animals in the mating season than did their adult daughters, perhaps to avoid sexual aggression from males and to reduce the loss of body temperature in the cold. Dominance rank clearly influenced the social interactions of old mothers: high-ranking mothers interacted with more non-related adult females and immature animals than did low-ranking mothers, indicating that old age does not decrease the attractiveness of high-ranking animals.     

Female-limited polymorphism in the copulatory organ of a traumatically inseminating insect

Sexual conflict can produce several evolutionary outcomes, one of which is female-limited trait polymorphism. We examine the African bat bug Afrocimex constrictus (Cimicidae), a species where both sexes are subjected to traumatic intromission from males. We show that males possess female genital structures that in related species ameliorate the costs of traumatic insemination. Moreover, the male form of these structures differs morphologically from the standard female form. Examination of females in our isolated study population revealed a discrete polymorphism in female genitalia. Some females had the typical cimicid form, while others had genitalia that more closely resembled the distinctive male form. Males, as well as females with the distinctive male form, experienced fewer traumatic copulations than the typical female morph. We propose that some females mimic the bizarre male condition in order to reduce the frequency of costly traumatic inseminations. To our knowledge this is the first example of a distinct female-limited genital polymorphism: its nature, as well as its association with traumatic sexual interactions, strongly suggests that sexual conflict underpins this unique phenomenon.     

Age,reproductive value,and dominance-related behaviour in vervet monkey females: cross-generational influences on social relationships and reproduction

Behavioural interactions among captive socially-living adult female vervet monkeys were analysed to determine whether (1) the motivation to maintain and increase, dominance rank declines with age as individual reproductive value declines, or (2) the cross-generational inheritance of dominance rank causes adult females to continue to involve themselves in dominance-related behaviours for the benefit of their daughters, even though their own reproductive value, is declining. The results indicate that adult females do not reduce their involvement in aggressive and dominance-related behaviours as they age. There was strong support for the hypothesis that older adult females maintain affiliative and supportive ties with their adult daughters, and that the daughters benefit from this relationship both in terms of social relationships and reproductive success. Young adult females without mothers were the recipients of more aggression, were less likely to be defeded when they were attacked and were less likely to challenge the rank of others compared to females with mothers living in the group. Young adult females with mothers produced significantly more surviving offspring and had a lower level of infant mortality than comparable adult females without mothers.     

Colour patterns of Syrphidae. III. Sexual dimorphism in Eristalis arbustorum

Abstract. 1. The hoverfly Eristalis arbustorum L. (Diptera, Syrphidae) is a sexually dimorphic Batesian mimic of bees and wasps.
2. This dual mimicry entails good mimicry of several small, dark bees (mainly mining bees) by female E.arbustorum , and less specific mimicry of wasps and other yellow and black Hymenoptera by males.
3. There is also variability of colour pattern within both sexes of E.arbustorum .
4. Seasonal fluctuations in the pattern frequencies of males occur because the temperature during pupal development influences the coloration of the adult.
5. Temporal changes in the pattern frequencies of females are attributable to developmental darkening of the abdomen.
6. These effects can be explained by the fact that the phenotypic requirements for thermoregulation and protection against predation will be different for males and females, and will also vary with time.
7. Behavioural differences between males and females are a component of the sexual dimorphism in this species.     

Further hormonal suppression of eldest daughter cotton-top tamarins following birth of infants

Reproductive suppression of females is found throughout the Callitrichids. However, in many species some evidence of ovarian activity is observed in subordinate females. Subordinate cotton-top tamarin females in our colony have never been observed to ovulate in the presence of a reproductive female. However, ovarian follicular development does occur, and measurable levels of urinary estrogen and luteinizing hormone are frequently found in subordinate females. We studied 11 female tamarins living in family groups with a reproductive female. Each of the 8 eldest daughters had measurable urinary estrogen and LH levels and showed a reduction of hormonal levels when new infants were born. The 3 younger daughters showed barely detectable hormonal levels that did not change. Following the birth of infants the eldest daughters scent marked less frequently, increased time in contact with and grooming group members other than the mother, but they were more often targets of aggression than immediately prior to infant births. The eldest daughters were somewhat less involved in care of new infants than expected, although they spent much time in proximity to those carrying the infants. These results suggest that the further reduction of hormonal levels in subordinate females after the birth of infants may function to prevent these females from competing with mothers during the post-partum estrus rather than recruiting the eldest daughters as helpers for infant care. © 1993 Wiley-Liss, Inc.     

A morphologically distinct Phlebotomus argentipes population from active cutaneous leishmaniasis foci in central Sri Lanka

Although the reported aetiological agent of cutaneous leishmaniasis (CL) in Sri Lanka is Leishmania donovani, the sandfly vector remains unknown. Ninety-five sandflies, 60 females and 35 males, collected in six localities in the district of Matale, central Sri Lanka, close to current active transmission foci of CL were examined for taxonomically relevant characteristics. Eleven diagnostic morphological characters for female sandflies were compared with measurements described for Indian and Sri Lankan sandflies, including the now recognised Phlebotomus argentipes sensu lato species complex. The mean morphometric measurements of collected female sandflies differed significantly from published values for P. argentipes morphospecies B, now re-identified as Phlebotomus annandalei from Delft Island and northern Sri Lanka, from recently re-identified P. argentipes s.s. sibling species and from Phlebotomus glaucus. Furthermore, analysis of underlying variation in the morphometric data through principal component analysis also illustrated differences between the population described herein and previously recognised members of the P. argentipes species complex. Collectively, these results suggest that a morphologically distinct population, perhaps most closely related to P. glaucus of the P. argentipess. I. species complex, exists in areas of active CL transmission. Thus, research is required to determine the ability of this population of flies to transmit cutaneous leishmaniasis.     

In poor families, mothers' milk is richer for daughters than sons: A test of Trivers-Willard hypothesis in agropastoral settlements in Northern Kenya

The Trivers–Willard hypothesis predicts the unequal parental investment between daughters and sons, depending on maternal condition and offspring reproductive potential. Specifically, in polygynous populations where males have higher reproductive variance than females, it predicts that mothers in good condition will invest more in sons, whereas mothers in poor condition will invest more in daughters. Previous studies testing this hypothesis focused on behavioral investment, whereas few examined biological investment. This study investigates the Trivers–Willard hypothesis on both behavioral and biological parental investment by examining breastfeeding frequencies and breast milk fat concentrations. Data from exclusively breastfeeding mothers in Northern Kenya were used to test hypotheses: Economically sufficient mothers will breastfeed sons more frequently than daughters, whereas poor mothers will breastfeed daughters more frequently than sons, and economically sufficient mothers will produce breast milk with higher fat concentration for sons than daughters, whereas poor mothers will produce breast milk with higher fat concentration for daughters than sons. Linear regression models were applied, using breastfeeding frequency or log‐transformed milk fat as the dependent variable, and offspring's sex (son = 1/daughter = 0), socioeconomic status (higher = 1/lower = 0), and the sex‐wealth interaction as the predictors, controlling for covariates. Our results only supported the milk fat hypothesis: infant's sex and socioeconomic status interacted (P = 0.014, n = 72) in their relation with milk fat concentration. The model estimated that economically sufficient mothers produced richer milk for sons than daughters (2.8 vs. 0.6 gm/dl) while poor mothers produced richer milk for daughters than sons (2.6 vs. 2.3 gm/dl). Further research on milk constituents in relation to offspring's sex is warranted. Am J Phys Anthropol , 2012. © 2012 Wiley Periodicals, Inc.     

Brood insurance via protogyny: a source of female-biased sex allocation

Sex allocation patterns and colony productivity are examined in Exoneura nigrescens, a social allodapine bee. As for previous studies on Australian allodapine bees, numerical sex ratios were strongly female biased in the smallest broods, but neared equality in larger broods. Local fitness enhancement has been suggested previously to explain female-biased allocation in allodapine bees. Here, we propose an alternative model, the 'insurance model', which predicts protogyny and, as a consequence, female-biased sex allocation in small broods with decreasing bias in larger broods. Because allodapine broods are reared progressively in an open burrow, broods require that adult females be present throughout their development in order to survive to maturity. If mothers invest in daughters (alloparents) first, these daughters can rear younger, dependent brood in cases in which orphaning occurs. If such daughters behave as surrogate mothers, then investment in them by mothers should not be regarded as investment in female sex allocation per se, giving rise to apparently female-biased broods. The model predicts a pattern of sex ratios as a function of total brood size that very closely match empirical data from E. nigrescens.     

Male offspring production by asexual Potamopyrgus antipodarum, a New Zealand snail

As only females contribute directly to population growth, sexual females investing equally in sons and daughters experience a two-fold cost relative to asexuals producing only daughters. Typically, researchers have focused on benefits of sex that can counter this 'cost of males' and thus explain its predominance. Here, we instead ask whether asexuals might also pay a cost of males by quantifying the rate of son production in 45 experimental populations ('lineages') founded by obligately asexual female Potamopyrgus antipodarum. This New Zealand snail is a powerful model for studying sex because phenotypically similar sexual and asexual forms often coexist, allowing direct comparisons between sexuals and asexuals. After 2 years of culture, 23 of the 45 lineages had produced males, demonstrating that asexual P. antipodarum can make sons. We used maximum-likelihood analysis of a model of male production in which only some lineages can produce males to estimate that ~50% of lineages have the ability to produce males and that ~5% of the offspring of male-producing lineages are male. Lineages producing males in the first year of the experiment were more likely to make males in the second, suggesting that some asexual lineages might pay a cost of males relative to other asexual lineages. Finally, we used a simple deterministic model of population dynamics to evaluate how male production affects the rate of invasion of an asexual lineage into a sexual population, and found that the estimated rate of male production by asexual P. antipodarum is too low to influence invasion dynamics.     

Onset of plural cooperative breeding in common marmoset families following replacement of the breeding male

Common marmosets, Callithrix jacchus, are usually characterized as singular cooperative breeders, with only a single, dominant female reproducing in each group. Anecdotal reports, however, have described two females breeding concurrently when an unrelated male joins their group. We tested the hypothesis that incorporation of an unrelated adult male into a family systematically leads to the onset of reproductive activity in a daughter and investigated the underlying mechanisms. We collected hormonal and behavioural data from mothers and their eldest daughters before and after the father was removed from the family and either replaced by an unrelated male (N=11) or immediately returned to the family (N=7). Variation between daughters in the occurrence of ovulatory cyclicity was not associated with the presence of an unrelated male but was closely linked to daughters' relationships with their mothers: only anovulatory daughters behaved submissively towards their mothers. Daughters never engaged in sexual behaviour with their fathers, but most did so with unrelated males. Similarly, daughters never conceived in intact natal families but did so in eight of 11 families containing an unrelated male. In six of these families, the mother and daughter bred concurrently. Thus, incorporation of an unrelated adult male into a marmoset family may frequently lead to the onset of plural breeding by activating sexual behaviour in a daughter; however, daughters ovulate only if they are not behaviourally subordinate to their mothers. Therefore, both inbreeding avoidance and rank-related reproductive suppression may constrain reproduction in marmoset daughters and contribute to maintenance of singular breeding.     

Simultaneous failure of two sex-allocation invariants: implications for sex-ratio variation within and between populations

Local mate competition (LMC) occurs when male relatives compete for mating opportunities, and this may favour the evolution of female-biased sex allocation. LMC theory is among the most well developed and empirically supported topics in behavioural ecology, clarifies links between kin selection, group selection and game theory, and provides among the best quantitative evidence for Darwinian adaptation in the natural world. Two striking invariants arise from this body of work: the number of sons produced by each female is independent of both female fecundity and also the rate of female dispersal. Both of these invariants have stimulated a great deal of theoretical and empirical research. Here, we show that both of these invariants break down when variation in female fecundity and limited female dispersal are considered in conjunction. Specifically, limited dispersal of females following mating leads to local resource competition (LRC) between female relatives for breeding opportunities, and the daughters of high-fecundity mothers experience such LRC more strongly than do those of low-fecundity mothers. Accordingly, high-fecundity mothers are favoured to invest relatively more in sons, while low-fecundity mothers are favoured to invest relatively more in daughters, and the overall sex ratio of the population sex ratio becomes more female biased as a result.     

Female reproductive competition within families in rural Gambia

Many studies show that the extended human family can be helpful in raising offspring, with maternal grandmothers, in particular, improving offspring survival. However, less attention has been given to competition between female kin and co-residents. It has been argued that reproductive conflict between generations explains the evolution of menopause in cooperatively breeding species where females disperse, and that older females are related to the offspring of younger females through their sons, whereas younger, incoming females are unrelated to older females. This means the pattern of help will be asymmetric, so older females lose in reproductive conflict and become 'sterile helpers'. Here, we seek evidence for female reproductive competition using longitudinal demographic data from a rural Gambian population, and examine when women are helping or harming each other's reproductive success. We find that older women benefit and younger women suffer costs of reproductive competition with women in their compound. But the opposite is found for mothers and daughters; if mother and daughter's reproductive spans overlap, the older woman reduces her reproduction if the younger woman (daughter) reproduces, whereas daughters' fertility is unaffected by their mothers' reproduction. Married daughters are not generally co-resident with their mothers, so we find not only competition effects with co-resident females, but also with daughters who have dispersed. Dispersal varies across human societies, but our results suggest reproductive conflict could be influencing reproductive scheduling whatever the dispersal pattern. A cultural norm of late male marriage reduces paternal grandmother/daughter-in-law reproductive overlap almost to zero in this population. We argue that cultural norms surrounding residence and marriage are themselves cultural adaptations to reduce reproductive conflict between generations in human families.