Linkage disequilibrium and natural selection for mimicry in the Batesian mimic Hypolimnas misippus (L.) (Lepidoptera: Nymphalidae) in the Afrotropics

On two occasions, on opposite sides of the African continent (Cape Coast, Ghana, and Dar es Salaam, Tanzania), high adult population densities in the polymorphic butterfly Hypolimnas misippus (a presumed mimic of Danaus chrysippus) were followed by linkage disequilibrium in combinations of fore‐ and hindwing colour patterns. On both occasions, disequilibrium was caused by significant changes in morph frequencies favouring rarer and more mimetic forms. Recaptures were too few for analysis at Dar, although the changes there took place within a single generation and must have been the result of differential survival. Recapture rate data and survival rate estimates at Cape Coast support the hypothesis that selective predation was responsible, as does the observation of synchronous linkage disequilibrium at Dar in the model D. chrysippus, indicating parasitic mimicry. There was clear selection for the perfection of mimicry for forewings at Dar and for hindwings at Cape Coast. Disequilibrium is also reported for two other sites, Legon (Ghana) and Boksburg (South Africa) and, in all four sites, it was associated with an increase in the most mimetic forms. New chemical evidence is presented to support the contention that D. chrysippus is a defended model. Although all the evidence leads to the conclusion that H. misippus is a Batesian mimic of D. chrysippus, many questions remain, particularly with regard to the identity of predators, the episodic nature of selective predation events, and their apparent lack of lasting and significant impact on overall gene frequencies. We conclude that H. misippus presents both challenges and opportunities for studies on mimicry, and we suggest that linkage disequilibrium can be a useful generic indicator for Gestalt predation on polymorphic prey. © 2010 The Linnean Society of London, Biological Journal of the Linnean Society, 2010, 100 , 180–194.     

All-female broods and mimetic polymorphism in Acraea encedon (L.) (Lepidoptera: Acraeidae) in Tanzania

In some populations of the African butterfly, Acraea encedon, there are two kinds of females, one producing offspring in a normal 1:1 sex ratio, the other producing females only; in other populations the sex ratio is apparently normal. All-female broods had hitherto been mainly associated with populations in which field sampling revealed an excess of females. The all-female brood trait is described from a population at Dar es Salaam which field sampling suggested was normal, and this indicates that the trait may be much more widespread and common than had previously been supposed. This discovery also extends the known distribution of the trait across Africa from Sierra Leone to eastern Tanzania. The butterfly is also a polymorphic Müllerian mimic of Danaus chrysippus, which is a highly unusual phenomenon as Müllerian mimicry is almost invariably monomorphic. The relative frequencies of two corresponding colour forms of the two species of butterflies at Dar es Salaam adds support to the hypothesis that they are indeed Mullerian mimics. The results of breeding experiments suggest that the polymorphic forms in Acraea encedon are allelic with dominance.     

Heterosis, epistasis and linkage disequilibrium in a wild population of the polymorphic butterfly Danaus chrysippus (L.)

The colour polymorphism of the Danaus chrysippus population at Dar es Salaam, East Africa, is controlled at three major loci, each with two alleles. Two of the loci, one governing ground colour and the other forewing pattern, are closely linked. The third locus, determining hindwing pattern, assorts independently. Thirty-eight broods raised from wild mated pairs, Fl and F2 generations gave 857 offspring of 23 genotypes (out of 27 possible). The forewing length, taken as an index of size, was investigated in relation to the genotype. Heterosis is evident at all three loci. The two linked loci show epistatic interaction of an unexpected kind: double heterozygotes are smaller than heterozygotes at only one locus but larger than double homozygotes. The heterotic effect at the third, unlinked locus is the most pronounced and is additive to that at the other two. Heterosis is more marked in males than females. The possibility that body size has importance in connexion with sexual selection, food resources and mimetic relationships is discussed. Analysis of gene and chromosome frequencies in the wild parents of 61 broods suggests that double heterozygotes for the two linked loci may have heterozygous advantage. Seventy-eight per cent of chromosomes are repulsion phase: thus, there is pronounced linkage disequilibrium which must be maintained by selection as crossing over is almost 296. In particular, the chromosome carrying both dominant alleles in coupling is rare. Consideration of the centres of distribution and present ranges of the alleles at all three loci suggests that three geographical races, aegyptius, dorippus and alcippus, were isolated by forest barriers, during wet periods in the Pleistocene, in south-west, north-east and north-west Africa respectively. They have probably expanded their ranges in the post-glacial period to overlap and interbreed in central and east Africa. Either heterozygous advantage or seasonal (directional) selection or a combination of both is responsible for the persistence of the polymorphism.     

Apostasy and selection for crypsis in the marine snail Littoraria filosa: an explanation for a balanced colour polymorphism

The marine snail, Littoraria filosa, is polymorphic for shell colour, with yellow, brown, and pink morphs that correspond in both appearance and frequency to the predominant background colours of its habitat. Previous research on this polymorphism has found indirect evidence of apostatic selection and selection for crypsis by unknown agents, probably crabs, and direct evidence of selection for crypsis by the parasitoid fly Sarcophaga megafilosia. In the present study, we report on field experiments to investigate whether S. megafilosia and shell‐crushing predators exert apostatic selection on L. filosa. For S. megafilosia, seven experimental treatments containing yellow and brown snails in the proportions of 0.1, 0.2, 0.4, 0.5, 0.6, 0.8, and 0.9 of each colour were established on mangrove trees and used to separately quantify the proportions of each colour attacked on grey/brown trunks and yellow/green leaves. The results obtained confirmed an earlier finding of selection for crypsis, but only showed slight, but significant, anti‐apostatic selection by S. megafilosia. For shell‐crushing predators, seven experimental treatments containing yellow and brown snails in the proportions of 0.08, 0.17, 0.33, 0.50, 0.66, 0.83, and 0.92 were established on two types of trees that differed in their background proportions of brown and green: (1) trees which had been pruned of approximately 90% of their foliage and (2) unpruned trees. The results obtained showed both selection for crypsis and apostatic selection. Furthermore, a selectively neutral frequency for yellow L. filosa was found for each background, and was less on pruned trees than unpruned ones (and vice versa for brown L. filosa), which can therefore account for the maintenance of a colour polymorphism where the proportions of each morph tend to resemble and correspond in frequency to the colours of the background. © 2008 The Linnean Society of London, Biological Journal of the Linnean Society, 2008, 95 , 62–71.     

Females show greater changes in wing colour with latitude than males in the green‐veined white butterfly,Pieris napi (Lepidoptera: Pieridae)

In butterflies, wing colour may simultaneously be under sexual selection in the context of mating selection and natural selection in the context of thermoregulation. In the present study, we collected mated females of the green‐veined white butterfly (Pieris napi) from locations spanning 960 km of latitude across Fennoscandia, and investigated sex‐specific latitudinal wing colour variation in their offspring raised under identical conditions. We measured wing colour characteristics, including reflectance at wavelengths 300–700 nm and the degree of wing melanization. At all latitudes, females reflected more light in the short wavelengths (< 400 nm) and less in the long wavelengths (> 450 nm), and they were more melanized than males. However, female wing colour varied more with latitude than that of males. Among females, long wavelength reflectance decreased, whereas short wavelength reflectance and melanization increased, towards the north. By contrast, among males, latitudinal variation was found only in the ventral hindwing melanization. These results are consistent with the idea that the balance between natural and sexual selection acting on wing colour changes with latitude differently in males than females. The dark wing colour of females in the north may be a thermoregulatory adaptation, although males may be constrained from evolving the dark dorsal wing colour favoured by natural selection because of constant sexual selection across latitudes. © 2012 The Linnean Society of London, Biological Journal of the Linnean Society, 2012, ?? , ??–??.     

The Utricularia-Cyanophyta association and its nitrogen-fixing capacity

Utricularia inflexa Forsk. growing in a shallow lake near Dar es Salaam, Tanzania was found to be abundantly associated with blue-green algae and other microorganisms, though blue-green algae were not found in the lake water. The epiphytes occurred both on the outer surfaces of the macrophyte and inside its traps. Seven genera of the Cyanophyta were observed, amongst which Anabaena was the most abundantly and consistently associated.Both epiphytes on the outer surfaces of the macrophyte and those inside mature traps fixed nitrogen in situ. Mature parts of the macrophyte fixed nitrogen at higher rates than immature parts, indicating the former was associated with a greater abundance of nitrogen fixers. The Utricularia-Cyanophyta association showed a nitrogen fixation (acetylene reduction) rate of 2012 nmol C₂H₄ g^–1 dry weight h^–1 or, in terms of lake area, of 4 500 nmol C₂H₄ m^–2 h^–1. The relative contributions of blue-green algae and bacteria were not determined.It is proposed that the association may involve a degree of physiological interdependence and that the association has potential as a biofertilizer for rice.Based on an M.Sc. thesis by G. M. Wagner submitted to the Department of Botany, University of Dar es Salaam, 1983.Based on an M.Sc. thesis by G. M. Wagner submitted to the Department of Botany, University of Dar es Salaam, 1983.     

The niche variation hypothesis and the evolution of colour polymorphism in birds: a comparative study of owls, nightjars and raptors

We studied the evolution of colour polymorphism in diurnal raptors, owls and nightjars, the avian taxa in which this trait is most widespread, in relation to species ecological niche width and diet. Two main mechanisms have been put forward to explain the maintenance of polymorphism, namely apostatic selection and disruptive selection. The niche variation hypothesis states that species with broader ecological niches should be more variable compared with those with narrow niches because of the action of disruptive selection; the apostatic selection hypothesis conversely suggests that intraspecific colour variation should be promoted in predators by prey forming an avoidance image for the more common colour morph. Our aim was to determine if colour polymorphism occurrence was associated with broad ecological niches as predicted by the niche variation hypothesis, or with predation on intelligent and sharp‐sighted prey as predicted by the avoidance image hypothesis. Pairwise comparisons were made between pairs of closely related species differing in variables expected to influence the occurrence of polymorphism. We found that polymorphic species of all three groups showed wider and more continuous distribution ranges, frequented many different habitats, both open and closed, and lived in seasonally alternating dry/wet climates. Polymorphic species were more migratory compared with monomorphic ones, and they showed an activity pattern covering both day and night. Conversely, colour polymorphism was not higher in species preying on birds and mammals. All these findings support the hypothesis that colour polymorphism evolved in bird species with wider niche breadth and not in species preying on intelligent prey. Therefore, we propose that disruptive selection may be the main mechanism maintaining colour polymorphism in these bird groups by favouring different morphs in different environmental conditions. © 2004 The Linnean Society of London, Biological Journal of the Linnean Society, 2004, 82 , 237–248.     

Hologenomic speciation: synergy between a male‐killing bacterium and sex‐linkage creates a ‘magic trait’ in a butterfly hybrid zone

Danaus chrysippus (L.) in Africa comprises four substantially isolated semispecies that are migratory and hybridize on a seasonal basis throughout the eastern and central part of the continent. In the hybrid zone (but not elsewhere), the butterfly is commonly host to a male killing endosymbiotic bacterium, Spiroplasma sp., which principally infects one semispecies, Danaus chrysippus chrysippus in Kenya. A W‐autosome mutation, inherited strictly matrilinearly, links B and C colour gene loci, which have thus gained sex‐linkage in chrysippus. We have monitored variation in sex ratio and genotype at the A and C colour gene loci for two extended periods of 18 months (2004–5) and 12 months (2009–10) in adults reared from wild eggs laid on trap plants in Kasarani, near Nairobi, Kenya. Additionally, in 2009–10, all surviving adult butterflies were screened for Spiroplasma infection. The hybridizing Kasarani population is highly atypical in three respects, and has apparently been so for some 30 years: first, the sex ratio is permanently female‐biased (as expected), although subject to seasonal fluctuation, being lowest (male/female) when D. c. chrysippus (cc) peaks and highest when Danaus chrysippus dorippus (CC) predominates; second, the population is invariably dominated by Cc heterozygotes of both sexes but especially females; and third, cc males are always scarce because they are systematically eliminated by male killing, whereas the CC genotype is male‐biased. It is this imbalance of sex versus genotype that determines the massive departure from Hardy–Weinberg equilibrium in the population, in part because cc females have little choice but to pair with C‐ males. We suggest that: first, Cc hybrids of both sexes fail to disperse in the company of either parental semispecies; second, Spiroplasma positive females carrying the W‐autosome mutation have a selective advantage over females that lack the translocation; third, the endoparasite and the translocation create a ‘magic trait’ linkage group that underlies hologenomic reproductive isolation between two emerging species, D. c. chrysippus and D. c. dorippus; and, fourth, that the predominance of males in dorippus suggests that individuals must be protected by a male‐killing suppressor gene. By contrast to the C locus, Aa heterozygotes are in substantial and permanent deficit, suggesting either assortative mating between AA (chrysippus and dorippus) and aa (Danaus chrysippus alcippus), or heterozygote unfitness, or both. © 2013 The Linnean Society of London, Biological Journal of the Linnean Society, 2014, 111 , 92–109.     

The diet of the edible cockle Anadara antiquata L. (Bivalvia,Arcidae) in Dar es Salaam,Tanzania, during the northeast monsoons

The diet of the cockle Anadara antiquata L. was studied along Dar es Salaam coast during the N-E Monsoon season. No zooplankton were found in the 80 cockle guts examined. 27 phytoplankton genera were identified, an indication of wide phytophagy. Members of classes Bacillariophyceae, Chlorophyceae, Pyrophyceae and Prasnophyceae were very prevalent in the diet. Scenedesmus, Chlamydomonas, Palmeria, Exuviella, and Coscinodiscus showed the highest recurrence frequencies per gut.     

Natural selection for rare and mimetic colour pattern combinations in wild populations of the diadem butterfly, Hypolimnas misippus L

Mark recapture and morph frequency data, gathered during a population irruption of Hypolimnas misippus in southern Ghana, provide evidence for apostatic and mimetic selection. During a period of low adult survival, both the recapture rate and the frequency of the commonest morph ( misippus ) were significantly reduced. Selection against this form increased phenotypic diversity and generated significant disequilibrium in the combinations of unlinked fore- and hindwing phenotypes. There was also evidence for selection against those forms (weak alcippoides ) which most closely resemble misippus . Other morphs, including both good mimics of Danaus chrysippus and rare non-mimics, showed no reductions in recapture rate during the period of low survival, but only the good mimics increased significantly in frequency. The results provide a predictive ecological model for density-dependent selection by predators which is consistent with field data from previous studies of H. misippus in Ghana and Tanzania. Their evolutionary implications are discussed, and it is suggested that anomalies in the mimicry of this species may be partly due to lack of predation when it is scarce.     

Cerebrospinal fluid and serum biomarkers of cerebral malaria mortality in Ghanaian children

Background

Successful malaria vector control depends on understanding behavioural interactions between mosquitoes and humans, which are highly setting-specific and may have characteristic features in urban environments. Here mosquito biting patterns in Dar es Salaam, Tanzania are examined and the protection against exposure to malaria transmission that is afforded to residents by using an insecticide-treated net (ITN) is estimated.

Methods

Mosquito biting activity over the course of the night was estimated by human landing catch in 216 houses and 1,064 residents were interviewed to determine usage of protection measures and the proportion of each hour of the night spent sleeping indoors, awake indoors, and outdoors.

Results

Hourly variations in biting activity by members of the Anopheles gambiae complex were consistent with classical reports but the proportion of these vectors caught outdoors in Dar es Salaam was almost double that of rural Tanzania. Overall, ITNs confer less protection against exophagic vectors in Dar es Salaam than in rural southern Tanzania (59% versus 70%). More alarmingly, a biting activity maximum that precedes 10 pm and much lower levels of ITN protection against exposure (38%) were observed for Anopheles arabiensis, a vector of modest importance locally, but which predominates transmission in large parts of Africa.

Conclusion

In a situation of changing mosquito and human behaviour, ITNs may confer lower, but still useful, levels of personal protection which can be complemented by communal transmission suppression at high coverage. Mosquito-proofing houses appeared to be the intervention of choice amongst residents and further options for preventing outdoor transmission include larviciding and environmental management.     

The causes of colour and colour change in caterpillars of the poplar and eyed hawkmoths (Laothoe populi and Smerinthus ocellata)

Caterpillars of the poplar and eyed hawkmoths (Laothoe populi and Smerinthus ocellata respectively) were reared under different conditions in order to determine why final instar caterpillars vary in colour. Poplar hawkmoth caterpillars normally rest on the undersides of leaves. Dull green and redspotted caterpillars are genetically determined polymorphisms. Caterpillars that are not dull green, however, can become white when fed on Populus alba or yellow-green when fed on Salix fragilis. Experiments showed that it is the reflective qualities of the leaves that determines which colour the caterpillar develops: if the young larva sees white then it becomes white, but if it sees green, grey or black then it becomes yellow-green. Young eyed hawkmoth larvae always developed into grey-green final instar caterpillars under our rather poorly-illuminated rearing conditions, but when reared on wild plants in white muslin sleeves they became whitish-green. In this species also it appears that colour of the final instar is determined by the reflectance of the substrate perceived by the young caterpillar.     

The heritable basis and cost of colour plasticity in coastrange sculpins

Both genetic and plastic traits contribute to adaptation in novel environments. Phenotypic plasticity can facilitate adaptation by allowing for existence in a wider range of conditions and a faster response to environmental change than gene‐based selection. Coastrange sculpins (Cottus aleuticus) colonize new and variable streams arising in the wake of receding glaciers in south‐east Alaska, and substrate‐matching plasticity may enhance colonization success by reducing detection by visual predators. As part of a long‐term study of the fitness consequences of colour plasticity and its capacity to respond to both positive and negative selection, we investigated whether it is heritable and costly. We raised full‐sib broods of sculpins in the laboratory: one half of each brood was raised in white containers, the other half in black. After 4 months, we digitally analysed their colour and found significant but weak heritability in both baseline colour and colour plasticity. To investigate the cost of colour plasticity, we compared the growth and mortality rates of juvenile sculpins reared under constant substrate colours to those reared on substrates that changed colour frequently, and compared growth rates among sculpin that differed in their colour change ability. We found evidence of small costs of plasticity, consistent with other studies of natural populations. Evidence of heritable genetic variation for plasticity and small costs to its maintenance and expression contributes to explanations of how plasticity is variable and persistent among wild populations and underscores its ability to respond both positively and negatively to selection in variable habitats.     

Impact of Community-Based Larviciding on the Prevalence of Malaria Infection in Dar es Salaam,Tanzania

Background

The use of larval source management is not prioritized by contemporary malaria control programs in sub-Saharan Africa despite historical success. Larviciding, in particular, could be effective in urban areas where transmission is focal and accessibility to Anopheles breeding habitats is generally easier than in rural settings. The objective of this study is to assess the effectiveness of a community-based microbial larviciding intervention to reduce the prevalence of malaria infection in Dar es Salaam, United Republic of Tanzania.

Methods and Findings

Larviciding was implemented in 3 out of 15 targeted wards of Dar es Salaam in 2006 after two years of baseline data collection. This intervention was subsequently scaled up to 9 wards a year later, and to all 15 targeted wards in 2008. Continuous randomized cluster sampling of malaria prevalence and socio-demographic characteristics was carried out during 6 survey rounds (2004–2008), which included both cross-sectional and longitudinal data (N = 64,537). Bayesian random effects logistic regression models were used to quantify the effect of the intervention on malaria prevalence at the individual level. Effect size estimates suggest a significant protective effect of the larviciding intervention. After adjustment for confounders, the odds of individuals living in areas treated with larviciding being infected with malaria were 21% lower (Odds Ratio = 0.79; 95% Credible Intervals: 0.66–0.93) than those who lived in areas not treated. The larviciding intervention was most effective during dry seasons and had synergistic effects with other protective measures such as use of insecticide-treated bed nets and house proofing (i.e., complete ceiling or window screens).

Conclusion

A large-scale community-based larviciding intervention significantly reduced the prevalence of malaria infection in urban Dar es Salaam.     

Global biogeography of warning coloration in the butterfly Danaus chrysippus

Warning coloration provides a textbook example of natural selection, but the frequent observation of polymorphism in aposematic species presents an evolutionary puzzle. We investigated biogeography and polymorphism of warning patterns in the widespread butterfly Danaus chrysippus using records from citizen science (n = 5467), museums (n = 8864) and fieldwork (n = 2586). We find that polymorphism in three traits controlled by known mendelian loci is extensive. Broad allele frequency clines, hundreds of kilometres wide, suggest a balance between long-range dispersal and predation of unfamiliar morphs. Mismatched clines for the white hindwing and forewing tip in East Africa are consistent with a previous finding that the black wingtip allele has spread recently in the region through hitchhiking with a heritable endosymbiont. Light/dark background coloration shows more extensive polymorphism. The darker genotype is more common in cooler regions, possibly reflecting a trade-off between thermoregulation and predator warning. Overall, our findings show how studying local adaptation at the global scale provides a more complete picture of the evolutionary forces involved.     

Outlook for survivors of childhood in sub-Saharan Africa: adult mortality in Tanzania. Adult Morbidity and Mortality Project.

OBJECTIVE--To measure age and sex specific mortality in adults (15-59 years) in one urban and two rural areas of Tanzania. DESIGN--Reporting of all deaths occurring between 1 June 1992 and 31 May 1995. SETTING--Eight branches in Dar es Salaam (Tanzania''s largest city), 59 villages in Morogoro rural district (a poor rural area), and 47 villages in Hai district (a more prosperous rural area). SUBJECTS--40,304 adults in Dar es Salaam, 69,964 in Hai, 50,465 in Morogoro rural. MAIN OUTCOME MEASURES--Mortality and probability of death between 15 and 59 years of age (45Q15). RESULTS--During the three year observation period a total of 4929 deaths were recorded in adults aged 15-59 years in all areas. Crude mortalities ranged from 6.1/1000/year for women in Hai to 15.9/1000/year for men in Morogoro rural. Age specific mortalities were up to 43 times higher than rates in England and Wales. Rates were higher in men at all ages in the two rural areas except in the age group 25 to 29 years in Hai and 20 to 34 years in Morogoro rural. In Dar es Salaam rates in men were higher only in the 40 to 59 year age group. The probability of death before age 60 of a 15 year old man (45Q15) was 47% in Dar es Salaam, 37% in Hai, and 58% in Morogoro; for women these figures were 45%, 26%, and 48%, respectively. (The average 45Q15s for men and women in established market economies are 15% and 7%, respectively.) CONCLUSION--Survivors of childhood in Tanzania continue to show high rates of mortality throughout adult life. As the health of adults is essential for the wellbeing of young and old there is an urgent need to develop policies that deal with the causes of adult mortality.     

Transmission of Schistosoma bovis in Mkulwe (Mbozi District, Mbeya region, southern highlands of Tanzania)

Various populations of laboratory bred bulinid snails were exposed to miracidia of Schistosoma bovis from Mbozi. The parasite is naturally transmitted by Bulinus globosus in the area. Laboratory infection revealed a good relationship with B. forskalii and B. globosus from Mbozi and a population of B. forskalii from Dar es Salaam (infection rates 100%, 63.6% and 41.7% respectively). Populations of B. globosus and B. nasutus from Dar es Salaam were refractory. It appears that both snail species (B. globosus and B. forskalii) present in Mbozi district transmit S. bovis.     

Phenotype-dependent mate choice and the influence of mixed-morph lineage on the reproductive success of a polymorphic and aposematic moth

Polymorphic warning signals in aposematic organisms are puzzling because efficient predator learning should select for the most efficient warning colouration. Yet, there are many examples of polymorphic and aposematic organisms in nature. Here, we investigated whether perceived trade-offs between natural and sexual selection, combined with different degrees of morph lineage admixture, can maintain polymorphic yellow and white hindwing colouration in aposematic wood tiger moth males (Arctia plantaginis). Prior research in the system suggests that yellow males have better warning colouration against predators, whereas white male morphs have higher mating success. We performed a mating experiment where females were offered four males: two white and two yellow. One male from each colour came from (purely) monomorphic lines (i.e. including the same paternal colour for multiple generations), whereas one male from each colour were from mixed-morph (or hybrid) lineages. We then assessed whether phenotype (colour), lineage, or an interaction between the two, best affected mating success. Our results showed that although white hindwing coloured males tended to have overall better reproductive success, this was mainly due to the significantly higher mating and hatching success of mixed-morph compared to pure-line individuals. Notably, this suggests the advantage of mixed-morph lineage is limited to white individuals, while on the contrary yellow mixed lineage moths have a disadvantage, i.e. the lowest mating success. The latter also suggests a cost to reproductive success in producing the more efficient against predators yellow warning colouration, even when those individuals recently descend from a white hindwing coloured lineage. Heterozygote, or hybrid advantage, even when confined to only one morph, has been shown to promote polymorphism in some systems, therefore, our results point at the need to further examine genetic architecture and the role of mixed-morph lineages in understanding the maintenance of polymorphisms in nature.     

Polymorphic Müllerian mimicry and interactions with thermal melanism in ladybirds and a soldier beetle: a hypothesis

It is argued that groups of similarly coloured species of coccinellids are Müllerian mimicry rings. This is based on a synthesis of the literature about the nature of their biology and aposematic colour patterns, their highly developed chemical defence and the responses of bird predators to them. The system of multiple mimicry ‘rings’ is illustrated for the Dutch coccinellid fauna. Some polymorphic species, including Adalia, exhibit red forms and black melanic forms which are apparently components of different putative mimicry rings. A similar reasoning is put forward with regard to the orange and the black forms of the soldier beetle Cuntharis livida. Hypotheses involving spatial variation in comimics, as have been developed to account for some other cases of polymorphic Miillerian mimicry, predict that sympatric polymorphic species exhibiting similar sets of phenotypes will show parallels in their geographical variation. This is tested for A. bipunctata and A. decempunctata in The Netherlands. On this local scale there is no parallel variation; A. bipunctata exhibits marked geographical differentiation whereas A. decempunctata shows a general uniformity in morph frequency. Observations on their population biology show that only in A. bipunctata is there a major spring period of adult reproduction on shrubs exposed to direct sunshine. Previous work has demonstrated an influence of thermal melanism in this period of the life cycle. It is suggested that local responses in species such as A. bipunctata may reflect a partial ‘escape’ from stabilizing aposematic selection. The basis of a steep cline found in C. livida, which opposes one in A. bipunctata, is unknown and unlikely to be related to mimicry. There is some evidence that the polymorphism is influenced by non-random mating. When species and communities of coccinellids are considered on a wide geographical scale many observations about their colour patterns and spatial variation, especially those of Dobzhansky, support an interaction between selection favouring mimetic resemblance and forms of climatic selection, especially thermal melanism. The polymorphism in Adalia is discussed in relation to a system of multiple mimicry rings and to Thompson's recent theoretical treatment of the maintenance of some polymorphisms for warning coloration by a balance between aposematic and apostatic selection. This becomes more tenable in coccinellids because of evidence that bird predators show a variable response to them. Frequency-independent selection arising from thermal melanism can provide the basis of spatial variation in equilibrium points. An alternative to such a hypothesis is one in which differences in unpalatability between species of coccinellids are emphasized (after experiments of Pasteels and colleagues). Some less unpalatable species such as Adalia may have responded to periods of prolonged disruptive selection acting in a frequency-dependent way to promote polymorphic mimicry associated with different modal colour patterns and intermediate in nature between classical Batesian and Müllerian mimicry. The likely occurrence of a supergene controlling polymorphism in some coccinellids is consistent with such an explanation.