Parental care in a tropical nymphalid butterfly Hypolimnas anomala

doi:10.1016/S0003-3472(88)80213-6

Animal Behaviour

Volume 36, Issue 5, September–October 1988, Pages 1425-1431

https://doi.org/10.1016/S0003-3472(88)80213-6 Get rights and content

Abstract

A tropical butterfly Hypolimnas anomala (Lepidoptera: Nymphalidae) straddles its eggs and guards them. Over 50% of the butterflies remained with their eggs until the eggs hatched. When butterflies were removed from their eggs, there was a significant increase in the number of eggs killed by predators compared to the number of eggs lost when the butterflies were left guarding them. Guarding was effective in reducing egg predation by several species of ants which were too small to remove the eggs whole, but was not effective against the ant Solenopsis geminata, which was large enough to carry off whole eggs. The smaller ants were the most common predators at the sites studied. Guarding also did not deter parasitoids from attacking the eggs. Some of the butterflies remained associated with the newly hatched larvae for 1 or more days, until the larvae left the leaf. When the butterfly remained with the larvae, survival of the larvae increased during the 1-day period following hatching. Thus, parental care improved the survival of the eggs and very young larvae from 36% to 61%.

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Tropical fire ant, red imported fire ant, and yellow crazy ant have in common; vigorously invading new areas, attacking native species, and destroying ecological balances. TFA, RIFA and YCA builds up colonies in soil, in open fields, and even in artificial buildings (Van Pelt, 1956; Vogt et al., 2003; Hoffmann, 2015), and attacks indigenous vertebrates and invertebrates (Nafus and Schreiner, 1988, Way et al., 1998; Morrison et al., 2004; Wetterer, 2005; Norasmah et al., 2006; Wauters et al., 2014). TFA and RIFA cause economic losses by damaging human-made facilities (e.g., irrigation tubes, and electronic cables), and agricultural products (Chang and Ota, 1976; Perfecto, 1994).
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Evolution of Hypolimnas butterflies (Nymphalidae): Out-of-Africa origin and Wolbachia-mediated introgression
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Females of the exceptionally widespread, pantropical species H. misippus mimic Danaus chrysippus through out the Old World - a species that is itself unusually widespread (Vane-Wright et al., 1977; Braby et al., 2015). Hypolimnas butterflies have been the subject of research on reproductive diapause (Kemp, 2001a; Pieloor and Seymour, 2001), seasonal polyphenism (Kemp, 2000; Kemp and Jones, 2001), territorial behaviour (Stride, 1956; Kemp, 2001b; Kemp and Rutowski, 2001), and parental care (Nafus and Schreiner, 1988; Schreiner and Nafus, 1991). Recent studies on Hypolimnas have focused on the microscopic ornamentation of wing scale arrangements (Saito, 2002; Kemp and Macedonia, 2006; Siddique et al., 2016).
Hypolimnas butterflies (Nymphalidae), commonly known as eggflies, are a popular model system for studying a wide range of ecological questions including mimicry, polymorphism, wing pattern evolution, and Wolbachia-host interactions. The lack of a time-calibrated phylogeny for this group has precluded understanding its evolutionary history. We reconstruct a species-level phylogeny using a nine gene dataset and estimate species divergence times. Based on the resulting tree, we investigate the taxon’s historical biogeography, examine the evolution of host plant preferences, and test the hypothesis that the endosymbiotic bacterium Wolbachia mediates gene transfer between species. Our analyses indicate that the species are grouped within three strongly supported, deeply divergent clades. However, relationships among these three clades are uncertain. In addition, many Hypolimnas species are not monophyletic or monophyletic with weak support, suggesting widespread incomplete lineage sorting and/or introgression. Biogeographic analysis strongly indicates that the genus diverged from its ancestor in Africa and subsequently dispersed to Asia; the strength of this result is not affected by topological uncertainties. While the larvae of African species feed almost exclusively on Urticaceae, larvae of species found further east often feed on several additional families. Interestingly, we found an identical mitochondrial haplotype in two Hypolimnas species, H. bolina and H. alimena, and a strong association between this mitotype and the Wolbachia strain wBol1a. Future investigations should explore the plausibility of Wolbachia-mediated introgression between species.
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Two hypotheses could explain the evolution of paternal care: caring males are more attractive to females and mate more often (sexual selection); males care when the benefits in terms of offspring survival exceed the costs (natural selection). To test these hypotheses we used Phyllomorpha laciniata: females can choose whether to lay eggs on plants or on conspecifics, and the extent to which males carry eggs varies between populations. Our results do not support the sexual selection hypothesis: females did not choose to mate with egg-carrying males in either natural populations or experimental contexts. We compared two populations that differ in the extent of male egg carrying and we show that in the population where male egg carrying was more prevalent, parasitism pressure was higher. Field experiments revealed that, in the population with high parasitism rate, egg mortality as a result of parasitoid attack was up to 10 times higher on plants than on conspecifics. Egg carrying is thus an effective strategy that protects eggs against parasitoids. We conclude that the main benefit derived by males from egg carrying is an increase in offspring survival, and that males are sensitive to interpopulation differences in egg mortality risks. Male care in this system has evolved despite intermediate levels of paternity certainty because the impact on offspring survival is high, and the costs in terms of loss of mating opportunities low. Thus, our findings support the natural selection hypothesis, although additional work on more populations is needed to verify this.
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Females of the shield bug Parastrachia japonensis Scott progressively provision nymph-containing nests with drupes of the host tree, Schoepfia jasminodora (Olicaceae: Rosidae: Santales). The majority of nests are 5–15 m from the host tree, a distance thought to have been a major impetus for the occurrence of provisioning in this species. However, the function of provisioning is not well understood. We carried out two field experiments to determine whether provisioning is nutritionally important and whether it affords protection against predation. Development of nymphs was significantly delayed and their survival was low in the absence of provisioning, even when nests were within the area of ground on to which the drupes fell, apparently because of the poor quality of the majority of the drupes. Selective provisioning of good-quality drupes by female P. japonensis, a semelparous species, was thus necessary for young nymphs to obtain enough food for their development. Furthermore, even without a female in attendance, having drupes in the nest significantly reduced early mortality in the presence of a predator.
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Ecological and physiological analyses of invertebrate parental care need to be integrated. This chapter reviews the physiological and behavioral mechanisms that control the onset, intensity, and termination of parental care; and the use of invertebrates to address parental care theory. This approach is taken to demonstrate that mechanistic studies of invertebrate parental behavior will provide insight as well as experimental tools for ecologists, to fill gaps in the coverage of invertebrates, and to reveal the potential for the use of invertebrate models in tests of parental care theory. Broad phylogenetic comparisons have the potential to address how physiology constrains the expression of parental care. Parental care in numerous independent phylogenetic lines of insects is regulated by the same neural and endocrine structures. Individuals from selected genetic lines can be employed to examine the physiological differences between individuals with varying tendencies to express parental behavior; genetic lines also will be useful in field experiments investigating the ecological trade-offs of adopting alternative patterns of investment. The effects of development on the expression of care have been neglected as well. The ease with which the developmental environment of many immature invertebrates can be manipulated suggests that the lack of understanding is caused by neglect and not by experimental barriers.
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Animal Behaviour

Abstract

References (17)

Presocial insects

Maternal care in Gargaphia solani (Hemiptera: Tingidae)

Anim. Behav.

The ecology and behavior of a subsocial pentatomid bug and two scelionid wasps: strategys and counterstrategy in a host and its parasitoids

Smithson. Contrib. Zool.

Factors influencing aggregation between nymphs of the lime aphid, Eucallipterus tiliae (L.)

Ecol. Entomol.

Spur- und Alarmstoffe bei der gefleckten Brutwanze Elasmucha grisea

Insectes Soc.

Sozialverhalten zweier Elasmucha-Arten (Heteroptera: Insekta)

Z. Tierpsychol.

Ökologische Bedeutung des Sozialverhaltens zweier Elasmucha-Arten (Heteroptera: Insekta)

Oecologia

Cited by (35)

Development of a predictive model for soil temperature and its application to species distribution modeling of ant species in South Korea

Evolution of Hypolimnas butterflies (Nymphalidae): Out-of-Africa origin and Wolbachia-mediated introgression

Male egg carrying in Phyllomorpha laciniata is favoured by natural not sexual selection

Provisioned Parastrachia japonensis (Hemiptera: Cydnidae) nymphs gain access to food and protection from predators

Parental Care in Invertebrates

Protective function of maternal care against egg predators in the shield bug Sastragala esakii (Hemiptera: Acanthosomatidae)