Krushnamegh Kunte

doublesex is a mimicry supergene

One of the most striking examples of sexual dimorphism is sex-limited mimicry in butterflies, a phenomenon in which one sex—usually the female—mimics a toxic model species, whereas the other sex displays a different wing pattern. Sex-limited mimicry is phylogenetically widespread in the swallowtail butterfly genus Papilio, in which it is often associated with female mimetic polymorphism. In multiple polymorphic species, the entire wing pattern phenotype is controlled by a single Mendelian ‘supergene’. Although theoretical work has explored the evolutionary dynamics of supergene mimicry, there are almost no empirical data that address the critical issue of what a mimicry supergene actually is at a functional level. Using an integrative approach combining genetic and association mapping, transcriptome and genome sequencing, and gene expression analyses, we show that a single gene, doublesex, controls supergene mimicry in Papilio polytes. This is in contrast to the long-held view that supergenes are likely to be controlled by a tightly linked cluster of loci. Analysis of gene expression and DNA sequence variation indicates that isoform expression differences contribute to the functional differences between dsx mimicry alleles, and protein sequence evolution may also have a role. Our results combine elements from different hypotheses for the identity of supergenes, showing that a single gene can switch the entire wing pattern among mimicry phenotypes but may require multiple, tightly linked mutations to do so.

The Diversity and Evolution of Batesian Mimicry in Papilio Swallowtail Butterflies

Papilio swallowtail butterflies exhibit a remarkable diversity of Batesian mimicry, manifested in several sex-limited and polymorphic types. There is little understanding of how this diversity is distributed within Papilio, and how different mimicry types have evolved in relation to each other. To answer these questions, I present a graphical model that connects various mimicry types by hypothetical character state changes within a phylogenetic framework. A maximum likelihood analysis of evolution of mimicry types on the Papilio phylogeny showed that sexually monomorphic mimicry and female-limited mimicry have evolved repeatedly but predominantly independently in different clades. However, transitions between these mimicry types are rarely observed. The frequency distribution of character state changes was skewed in favor of the evolution of mimicry, whereas many theoretically plausible character state changes, especially evolutionary loss of mimicry, were not evident. I discuss these findings in relation to studying the tempo of evolutionary change, loss of traits, and directionality and connectivity among character states. The pathway approach and phylogenetic patterns of mimicry demonstrated in Papilio are useful to test novel hypotheses regarding the diversity and evolutionary directionality of Batesian mimicry in other systems.

Female-limited mimetic polymorphism: a review of theories and a critique of sexual selection as balancing selection

Mimicry theory played a prominent role in the development of natural selection theory, and sparked a long-lasting interest in the observation that Batesian mimicry in some butterflies is female limited and polymorphic. Mimetic females of polymorphic species clearly have a selective advantage due to reduced predation pressure, but the selective forces that maintain nonmimetic female forms remain unclear. Attention has lately been focused on three explanations based on sexual selection: (1) male mate preference, (2) pseudo-sexual selection and (3) sexual harassment avoidance. These are thought to favour nonmimetic female forms and allow them to persist in the population via balancing selection. Here I review the assumptions and evidence for each of these hypotheses and assess their relative merit. I find that: (a) key predictions of the hypotheses have not been tested, (b) the hypotheses interpret surrogate measures of fitness trade-offs implicit in balancing selection (e.g. mating frequency) differently, and (c) sexual selection may not maintain nonmimetic females at high mimic frequencies if male mate preference is frequency dependent. As a result, none of the hypotheses is unequivocally supported by available data. I show that a fourth, non-sexual selectionist hypothesis, namely that physiological trade-offs maintain mimetic female polymorphism, is based on unclear assumptions and probably explains minor variation in female polymorphism. Finally, I show that the basic framework of frequency-dependent mimetic advantage, independent of sexual selection, can adequately explain female-limited mimetic polymorphism in a broad range of species. Testing this framework should be a priority in resolving this problem.

Mimetic butterflies support Wallace's model of sexual dimorphism

Theoretical and empirical observations generally support Darwins view that sexual dimorphism evolves due to sexual selection on, and deviation in, exaggerated male traits. Wallace presented a radical alternative, which is largely untested, that sexual dimorphism results from naturally selected deviation in protective female coloration. This leads to the prediction that deviation in female rather than male phenotype causes sexual dimorphism. Here I test Wallaces model of sexual dimorphism by tracing the evolutionary history of Batesian mimicry—an example of naturally selected protective coloration—on a molecular phylogeny of Papilio butterflies. I show that sexual dimorphism in Papilio is significantly correlated with both female-limited Batesian mimicry, where females are mimetic and males are non-mimetic, and with the deviation of female wing colour patterns from the ancestral patterns conserved in males. Thus, Wallaces model largely explains sexual dimorphism in Papilio. This finding, along with indirect support from recent studies on birds and lizards, suggests that Wallaces model may be more widely useful in explaining sexual dimorphism. These results also highlight the contribution of naturally selected female traits in driving phenotypic divergence between species, instead of merely facilitating the divergence in male sexual traits as described by Darwins model.

Genome-Wide Characterization of Adaptation and Speciation in Tiger Swallowtail Butterflies Using De Novo Transcriptome Assemblies

Hybrid speciation appears to be rare in animals, yet characterization of possible examples offers to shed light on the genomic consequences of this unique phenomenon, as well as more general processes such as the role of adaptation in speciation. Here, we first generate transcriptome assemblies for a putative hybrid butterfly species, Papilio appalachiensis, its parental species, P. glaucus and P. canadensis, and an outgroup, P. polytes. Then, we use these data to infer genome-wide patterns of introgression and genomic mosaicism using both phylogenetic and population genetic approaches. Our results reveal that there is little genetic divergence among all three of the focal species, but the subset of gene trees that strongly support a specific tree topology suggest widespread sharing of genetic variation between P. appalachiensis and both parental species, likely as a result of hybrid speciation. We also find evidence for substantial shared genetic variation between P. glaucus and P. canadensis, which may be due to gene flow or ancestral variation. Consistent with previous work, we show that P. applachiensis is more similar to P. canadensis at Z-linked genes and more similar to P. glaucus at mitochondrial genes. We also identify a variety of targets of adaptive evolution, which appear to be enriched for traits that are likely to be important in the evolution of this butterfly system, such as pigmentation, hormone sensitivity, developmental processes, and cuticle formation. Overall, our results provide a genome-wide portrait of divergence and introgression associated with adaptation and speciation in an iconic butterfly radiation.

Integrating biodiversity and conservation with modern agricultural landscapes

Abstract To achieve food security and meet the demands of the ever-growing human populations, farming systems have assumed unsustainable practices to produce more from a finite land area. This has been cause for concern mainly due to the often-irreversible damage done to the otherwise productive agricultural landscapes. Agro-ecology is proclaimed to be deteriorating due to eroding integrity of connected ecological mosaics and vulnerability to climate change. This has contributed to declining species diversity, loss of buffer vegetation, fragmentation of habitats, and loss of natural pollinators or predators, which eventually leads to decline in ecosystem services. Currently, a hierarchy of conservation initiatives is being considered to restore ecological integrity of agricultural landscapes. However, the challenge of identifying a suitable conservation strategy is a daunting task in view of socio-ecological factors that may constrain the choice of available strategies. One way to mitigate this situation and integrate biodiversity with agricultural landscapes is to implement offset mechanisms, which are compensatory and balancing approaches to restore the ecological health and function of an ecosystem. This needs to be tailored to the history of location specific agricultural practices, and the social, ecological and environmental conditions. The offset mechanisms can complement other initiatives through which farmers are insured against landscape-level risks such as droughts, fire and floods. For countries in the developing world with significant biodiversity and extensive agriculture, we should promote a comprehensive model of sustainable agricultural landscapes and ecosystem services, replicable at landscape to regional scales. Arguably, the model can be a potential option to sustain the integrity of biodiversity mosaic in agricultural landscapes.

Prey from the eyes of predators: Color discriminability of aposematic and mimetic butterflies from an avian visual perspective.

Predation exerts strong selection on mimetic butterfly wing color patterns, which also serve other functions such as sexual selection. Therefore, specific selection pressures may affect the sexes and signal components differentially. We tested three predictions about the evolution of mimetic resemblance by comparing wing coloration of aposematic butterflies and their Batesian mimics: (a) females gain greater mimetic advantage than males and therefore are better mimics, (b) due to intersexual genetic correlations, sexually monomorphic mimics are better mimics than female‐limited mimics, and (c) mimetic resemblance is better on the dorsal wing surface that is visible to predators in flight. Using a physiological model of avian color vision, we quantified mimetic resemblance from predators’ perspective, which showed that female butterflies were better mimics than males. Mimetic resemblance in female‐limited mimics was comparable to that in sexually monomorphic mimics, suggesting that intersexual genetic correlations did not constrain adaptive response to selection for female‐limited mimicry. Mimetic resemblance on the ventral wing surface was better than that on the dorsal wing surface, implying stronger natural and sexual selection on ventral and dorsal surfaces, respectively. These results suggest that mimetic resemblance in butterfly mimicry rings has evolved under various selective pressures acting in a sex‐ and wing surface‐specific manner.

Comparative molecular species delimitation in the charismatic Nawab butterflies (Nymphalidae, Charaxinae, Polyura).

The charismatic tropical Polyura Nawab butterflies are distributed across twelve biodiversity hotspots in the Indomalayan/Australasian archipelago. In this study, we tested an array of species delimitation methods and compared the results to existing morphology-based taxonomy. We sequenced two mitochondrial and two nuclear gene fragments to reconstruct phylogenetic relationships within Polyura using both Bayesian inference and maximum likelihood. Based on this phylogenetic framework, we used the recently introduced bGMYC, BPP and PTP methods to investigate species boundaries. Based on our results, we describe two new species Polyura paulettae Toussaint sp. n. and Polyura smilesi Toussaint sp. n., propose one synonym, and five populations are raised to species status. Most of the newly recognized species are single-island endemics likely resulting from the recent highly complex geological history of the Indomalayan-Australasian archipelago. Surprisingly, we also find two newly recognized species in the Indomalayan region where additional biotic or abiotic factors have fostered speciation. Species delimitation methods were largely congruent and succeeded to cross-validate most extant morphological species. PTP and BPP seem to yield more consistent and robust estimations of species boundaries with respect to morphological characters while bGMYC delivered contrasting results depending on the different gene trees considered. Our findings demonstrate the efficiency of comparative approaches using molecular species delimitation methods on empirical data. They also pave the way for the investigation of less well-known groups to unveil patterns of species richness and catalogue Earths concealed, therefore unappreciated diversity.

Adaptive Genetic Exchange: A Tangled History of Admixture and Evolutionary Innovation

Genetic exchange between divergent evolutionary lineages, from introgressive hybridization between locally adapted populations to insertion of retroviral sequences into eukaryotic genomes, has now been documented. The detection of frequent divergence-with-gene-flow contrasts the neo-Darwinian paradigm of largely allopatric diversification. Nevertheless, of even greater significance is the growing wealth of data suggesting that the recipients of the transferred genomic material gain adaptive phenotypes from the donor lineages. This adaptive enrichment is reflected by changes in pathogenicity in viruses and bacteria, the transformation of ecological amplitude in eukaryotes, and adaptive radiations in extremely diverse lineages. Although genetic exchange may produce maladaptive consequences, most of the recently reported examples suggest increases in fitness, and many such adaptive trait transfers have been identified in our own species.

The Wildlife (Protection) Act and conservation prioritization of butterflies of the Western Ghats, southwestern India

Krushnamegh Kunte Various schedules of the Wildlife (Protection) Act, 1972 (henceforth WPA), dictate the level of legal protection given to species of Indian animals. Shortcomings of the schedules of the WPA with respect to insects have been pointed out, but no solutions have been suggested. Here I have used butterflies of the Western Ghats as a case study, analysed their conservation values with multiple species attributes and then compared my findings with the species listed under the WPA. Analysis shows that a large proportion of species with high conservation values, many of them narrowly endemic and endangered, are not listed under the WPA, indicating the need to expand the listings. This methodology can be used to objectively assess conservation values of other animals and their inclu-sion in the WPA.