The female Diadem (bottom left) mimics the African Queen (top left). The male Diadem (right) keeps a distinct pattern to attract mates
This is the second in a sudden spate of research papers that casually and unintentionally refute creationism without even trying, simply by revealing the facts. It deals with the evolution of Batesian mimicry in a species of butterfly.
Scientists working at the universities of Exeter, Edinburgh and Cambridge, and Mpala Research Centre in Kenya have discovered the genetic basis for the clear example of Batesian mimicry to be found in the female of the pantropical species of butterfly, the Diadem butterfly, Hypolimnas misippus, which closely resembles the toxic African queen butterfly, Danaus chrysippus.
Batesian mimicry is the natural phenomenon where an otherwise harmless species evolves to resemble a harmful or distasteful species as a defence mechanism. The prerequisite for Batesian mimicry to evolve is that a prey species is predated upon by the predator of a harmful species which coexists in the same locality. The predator learns to avoid the dangerous or distasteful species so any other species that comes to resemble the harmful or distasteful species might be mistaken for it and avoided. The more closely it comes to resemble the avoided species, the more likely it is to survive and reproduce.
Give me a short essay on Batesian mimicry, with some examples, please. Batesian Mimicry: Nature's Deceptive ArtWhat the team found was that local populations of female Diadem butterflies have modified genes at two different loci in their genome to give different wing patterns according to the local colour form of the African queen, to produce closely similar wing patterns and colours, and have repurposed atavistic genes inherited from ancestral species. Naturally, this refutes the ludicrous creationist claims that all mutations are deleterious because these modifications are very clearly advantageous and so will enable the carrier to produce more descendants - the only relevant test of beneficial/deleterious for any mutation.
In the intricate dance of survival that unfolds within the natural world, species have evolved an array of strategies to navigate the relentless pressures of predation. Among these strategies, Batesian mimicry stands out as a remarkable phenomenon, where harmless or edible species mimic the appearance of harmful or inedible ones, thus gaining protection against predation through deception. Named after the British naturalist Henry Walter Bates, who first documented this phenomenon in the Amazon rainforest during the mid-19th century, Batesian mimicry represents a compelling example of evolutionary arms races and the power of adaptation.
At its core, Batesian mimicry hinges upon the principle of visual deception. Mimic species adopt the appearance, often through coloration or body shape, of a model species that possesses some form of defense mechanism, such as toxicity, spines, or other deterrents. By mimicking these traits, the mimic species effectively trick potential predators into perceiving them as undesirable or dangerous, thereby avoiding predation despite lacking any actual defenses.
One classic example of Batesian mimicry can be observed in the relationship between certain non-venomous snakes and venomous snakes. The harmless milk snake (Lampropeltis triangulum) bears a striking resemblance to the venomous coral snake (Micrurus fulvius) with its pattern of red, black, and yellow bands. This mimicry allows the milk snake to deter predators by capitalizing on the learned avoidance behaviors of predators that associate the distinctive color pattern with danger. In reality, the milk snake poses no threat, but its visual similarity to the venomous coral snake affords it a measure of protection.
Another well-documented instance of Batesian mimicry is found in certain butterfly species. The viceroy butterfly (Limenitis archippus), for instance, closely resembles the monarch butterfly (Danaus plexippus) in appearance. Monarchs are unpalatable to predators due to the toxic compounds derived from their larval food source, milkweed. By mimicking the bright orange coloration and wing pattern of the monarch, the viceroy gains protection from predators that have learned to avoid the toxic model species.
Batesian mimicry is not limited to individual species but can extend to entire communities or ecosystems, where multiple harmless species converge in appearance upon a single model species. This convergence amplifies the effectiveness of mimicry, as predators encounter a greater number of mimics resembling the same unpalatable model, reinforcing the learned avoidance response.
In conclusion, Batesian mimicry exemplifies nature's ingenuity in the realm of adaptation and survival. Through the deceptive art of mimicry, vulnerable species gain a crucial advantage in the ongoing struggle for existence, exploiting the sensory perceptions of predators to evade harm. As our understanding of evolutionary dynamics continues to deepen, Batesian mimicry stands as a testament to the remarkable strategies that have emerged from the complex interplay between organisms within Earth's diverse ecosystems.
It's also a lovely example of how environmental selectors, in this case predation, can push evolution in a particular direction to mitigate their effects, and also of how atavistic, i.e., redundant, genes, can be exapted for new purposes. Of course, no intelligently designed species would carry redundant genes in the first place and would have no reason to repurpose anything.
The team's findings are published open access in the journal Molecular Biology and Evolution and are explained in a University of Exeter news release: Scientists have discovered how female Diadem butterflies have evolved to look like African Queen butterflies to deter predators.
African Queens are toxic, making them poor food for predators such as birds.Technical details and background to the research are given in the team's open access paper in Molecular Biology and Evolution:
Diadems are actually good prey for birds – but they have evolved colours and patterns that closely match those of African Queens, making them appear toxic.
The new study – by a team including the universities of Exeter, Edinburgh and Cambridge, and Mpala Research Centre in Kenya – found that, surprisingly, different genes control these patterns in the two species.
Different patterns are found on African Queen butterflies in north, east, south and west Africa – and the patterns on female Diadem butterflies in each area match these.Since the time of Darwin, Wallace and Bates, people have wondered how different butterflies have evolved to appear the same – and now we know. Our findings present a compelling instance of convergent evolution, whereby species independently evolve similar traits. We also find evidence of adaptive atavism in the Diadem – when a species reverts to a state found in its ancestors.
In this case, Diadem butterflies have re-evolved an ancestral wing pattern and repurposed it to mimic the Africa Queen, providing a major advance in our understanding of how tasty species mimic those that are toxic.
Professor Richard H ffrench-Constant, co-author
Centre for Ecology and Conservation
University of Exeter, Penryn Campus, Cornwall, UK.
In contrast, male Diadems have distinctive dark wings with large white patches – possibly because the need to be recognised by the female outweighs the need to hide.
The study used “haplotagging”, a linked-read sequencing technology, and a new analytical tool called Wrath to study the genomes of multiple butterflies from the two different species.This is amazing, as the males and females look like totally different butterflies, even though they share the same genome.
Dr Dino J Martins, co-author
Turkana Basin Institute
Stony Brook University, Stony Brook, NY, USAThe paper, published in the journal Molecular Biology and Evolution, is entitled: “Transposable element insertions are associated with Batesian mimicry in the pantropical butterfly Hypolimnas misippus.”These new techniques can give us unique insights into the molecular population genetics of this fascinating example of Batesian mimicry.
Dr Simon H Martin, co-author
Institute of Evolutionary Biology
University of Edinburgh, Edinburgh, UK.
Abstract
Hypolimnas misippus is a Batesian mimic of the toxic African Queen butterfly (Danaus chrysippus). Female H. misippus butterflies use two major wing patterning loci (M and A) to imitate three color morphs of D. chrysippus found in different regions of Africa. In this study, we examine the evolution of the M locus and identify it as an example of adaptive atavism. This phenomenon involves a morphological reversion to an ancestral character that results in an adaptive phenotype. We show that H. misippus has re-evolved an ancestral wing pattern present in other Hypolimnas species, repurposing it for Batesian mimicry of a D. chrysippus morph. Using haplotagging, a linked-read sequencing technology, and our new analytical tool, Wrath, we discover two large transposable element insertions located at the M locus and establish that these insertions are present in the dominant allele responsible for producing mimetic phenotype. By conducting a comparative analysis involving additional Hypolimnas species, we demonstrate that the dominant allele is derived. This suggests that, in the derived allele, the transposable elements disrupt a cis-regulatory element, leading to the reversion to an ancestral phenotype that is then utilized for Batesian mimicry of a distinct model, a different morph of D. chrysippus. Our findings present a compelling instance of convergent evolution and adaptive atavism, in which the same pattern element has independently evolved multiple times in Hypolimnas butterflies, repeatedly playing a role in Batesian mimicry of diverse model species.
Introduction
Butterfly wing patterns are a classic example of adaptive evolution. Evolutionary genetic studies have dissected the loci controlling wing pattern in several species of butterflies from a wide range of ecotypes and families, providing extensive information on the evolution of adaptive traits (Jiggins 2017; Beldade and Brakefield 2018). The genetic architectures uncovered are varied, from supergenes formed by inversions encompassing multiple loci in Heliconius numata (Joron et al. 2011) to transposable element (TE) insertions in the peppered moth (van’t Hof et al. 2016) or a gene duplication in the wood tiger moth (Brien et al. 2023). Key insights on the genetic basis of butterfly wing patters come from the Heliconius genus of tropical butterflies (Jiggins 2017). These are best known for the multiple instances of Müllerian mimicry in which several pairs of unpalatable sympatric species converge to the same wing pattern sharing the costs of teaching predators. Numerous studies have looked at the genetic basis of their mimetic patterns, identifying the main genes contributing to these adaptive phenotypes and describing their genetic architecture (Joron et al. 2011; Reed et al. 2011.1; Martin and Reed 2014; Nadeau et al. 2016.1; Westerman et al. 2018.1). Although much is known about the genetic basis of mimicry in Heliconius, exploring other systems, particularly those with other evolutionary dynamics such as Batesian mimics, in which palatable mimics resemble toxic models, will provide crucial knowledge on the evolution of adaptive phenotypes.
The Hypolimnas genus of tropical butterflies is diverse in wing pattern phenotypes (Fig. 1B). Interestingly, the genus presents many instances of Batesian mimicry, with the main models being Danaid species of the Danaus, Amauris, and Euploea genera (Vane-Wright et al. 1977). Despite the diversity in phenotype and model species being mimicked, some wing pattern elements are common in most Hypolimnas, exemplified by the black-and-white forewing tips found in most species (17/21 species with phenotype data) or the common black or brown background color. These common wing patterns are often adaptive, and it is not known whether they have independently evolved multiple times or are shared through common ancestry. A less likely hypothesis is that these phenotypes are ancestral but have been lost and re-evolved in some species through convergent evolution. This hypothesis is similar to atavism, in which mutations or recombination events recreate an ancestral phenotype using existing developmental machinery, but differs from it in that atavism is often maladaptive. Hypolimnas therefore offer an opportunity to study the evolution of adaptive phenotypes in a group that has not been well studied to date.Hypolimnas misippus or Diadem is a pantropical butterfly with complex Batesian mimicry. Females are mimetic and polymorphic, with detailed resemblances to three of the morphs of the toxic African Queen, Danaus chrysippus (Fig. 1A; Smith 1973). Despite the striking mimicry, a puzzling mismatch exists in the geographical distribution of H. misippus and D. chrysippus morphs across Africa, in that the most abundant models are not reflected in the frequency of mimics at a given location (Gordon et al. 2010). This, together with the fact that maladaptive intermediate morphs of H. misippus are commonly found, suggests that current selection for mimicry might be weak and raises the question of how the polymorphism is maintained (Gordon and Smith 1998; Gordon et al. 2010). Clarifying the genetic underpinnings of wing mimicry in H. misippus will shed light on this complex case of Batesian mimicry and the forces maintaining polymorphism in the population.Fig. 1.Mimicry in Hypolimnas missippus and the Hypolimnas genus. A) Female morphs of H. misippus side by side with their matching model morphs of D. chrysippus. Names of the forewing morph of H. misippus are specified below each photo. Although morphs matching the bottom-right H. misippus (immima forewing and white-spotted hindwing) exist within the D. chrysippus hybrid zone, they are considered maladaptive intermediates outside of it. D. chrysippus is not sexually dimorphic; individuals shown are all males. Non-mimetic H. misippus male at the bottom. B) Phylogram of the Hypolimnas genus extracted from Sahoo et al. (2018.2) (concatenated Bayesian inference tree) showing that black-and-white forewing tips are common through the genus and most likely ancestral. For presentation purposes, one specimen is shown per species, although not all species are monophyletic. Choosing other specimens would not change the conclusion on the ancestrality of black-and-white wing tips. All species shown are sexually dimorphic and/or polymorphic except antevorta, dexithea, inopinata, and usambara. Species showing Batesian mimicry are indicated by a small dark dot. Recurrent forewing phenotypes are indicated by wing drawings. Male and female signs indicate the sex of the individual photographed.Butterfly photos are reproduced from Moore (2023.1) under CC-BY.
Wing coloration in H. misippus is determined by two loci of large effect, the M and A loci, determining forewing and hindwing patterns, respectively (Smith and Gordon 1987; Gordon and Smith 1989; VanKuren et al. 2019). The existence of a third locus, the hindwing white suppressor S, has also been hypothesized (Gordon and Smith 1989). The M locus is a Mendelian locus with two alleles, with the dominant M allele (diploid genotype M-) producing the mimetic black-and-white forewing tips in the misippus morph (Fig. 1A); whereas recessive homozygotes (mm) have mimetic orange or intermediate forewings, known as the inaria and immima morphs, respectively. Epistasis exists between the M and the A loci, producing the intermediate immima forms in mm genotypes when the dominant A allele for white hindwings is present (mmA-genotype). Previous work has identified the M locus to an intergenic region of 10 kb near genes of interest such as pink and Sox 5/6 (VanKuren et al. 2019). However, not much is known about the structure of the locus itself, which of the alleles is derived, and whether it arose through de novo mutation or introgression.
Structural variation forms a large part of the genetic variation observed in wild populations and can play a key role in adaptation and speciation (Auton et al. 2015; Wellenreuther et al. 2019.1). Structural variants (SVs) are typically defined as events larger than 50 bp and include various combinations of gains, losses, and rearrangement of genetic material, which can have extensive effects on gene content, as well as genetic contiguity (reviewed in Ho et al. 2020). These effects have major roles in adaptation and speciation in many species (reviewed in Hoffmann and Rieseberg 2008; Kondrashov 2012; Faria et al. 2019.2) as well as human disease (Weischenfeldt et al. 2013; Zeevi et al. 2019.3). For example, inversions have often been associated with complex phenotypes, as reduced recombination at the inversion promotes the joint inheritance of co-adapted alleles (Kirkpatrick and Barton 2006). Examples of this are seen in elytra coloration in ladybirds and reproductive morph switches in the ruff (Küpper et al. 2015.1; Lamichhaney et al. 2016.2; Ando et al. 2018.3; Gautier et al. 2018.4; reviewed in Thompson and Jiggins 2014.1; Orteu and Jiggins 2020.1). In other cases, gene duplications might give rise to adaptive loci through neo-functionalization as seen in heterostyly in Primula plants and in the complex phenotypes of the wood tiger moth (Li et al. 2016.3; Brien et al. 2023).
Despite the importance of SVs in phenotypic variation, their study is limited by the difficulty of detecting them using high throughput “short-read” DNA sequencing (Mahmoud et al. 2019.4). SVs involve the rearrangement of otherwise identical DNA sequences, so their detection often requires sequencing molecules that span the rearranged sequence junction. Relative to the size of an SV (often >50 kb), the fraction of read molecules (typically 300–500 bp) that span junctions can be vanishingly small. This problem is made worse by ambiguous mapping due to repetitive elements, which contribute to the formations of SVs (Sharp et al. 2005; Carvalho and Lupski 2016.4; Payer et al. 2017.1). Nevertheless, a number of programs exist to detect SVs from short-read sequencing (Rausch et al. 2012.1; Sindi et al. 2012.2; Layer et al. 2014.2; Iakovishina et al. 2016.5). Long-read sequencing, in contrast, has improved our power to detect SVs via reads that span repetitive and problematic regions, but is limited by cost (Sedlazeck et al. 2018.5; Ho et al. 2020).
Linked-read sequencing has emerged as an alternative that combines the scalability of short-read sequencing while retaining linkage information (Marks et al. 2019.5). The newly developed “haplotagging” is a simple, linked-read technique that can be used to sequence entire study populations with hundreds of individuals (Meier et al. 2021). In this approach, large DNA molecules are barcoded as they are broken up for short-read sequencing. To detect SVs, the barcoded, larger DNA molecule greatly boosts the fraction of junction-spanning molecules, thus improving detection power. Importantly, haplotagging can be easily scaled up to population level by multiplexing, which makes it possible to track the frequency of polymorphic SVs in single individuals, making it an ideal tool for the study of adaptation and speciation in non-model organisms (Meier et al. 2021).
Here, we dissect the genetic architecture of an adaptive polymorphism in H. misippus using haplotagging data. First, we describe our custom program, WRapped Analysis of Tagged Haplotypes (Wrath, github.com/annaorteu/wrath), and validate in two ways: (1) we run Wrath on published Heliconius haplotagging data with known SVs and (2) we test it against simulated Heliconius data. Thereafter, we focus on the H. misippus case by first performing an association study using hundreds of whole genome haplotagging sequences to pinpoint the candidate locus controlling mimicry in this system. We then use the linked-read information to dissect the genetic structure of the locus by applying Wrath. Finally, we perform a cross-species comparison within the genus Hypolimnas to investigate the evolutionary history of the wing pattern mimicry alleles.
The discussion section of the paper will make disturbing reading for creationists, if they understand it, because it explains how so much of the observable evidence can be explained by things such as mutation, gene doubling and inversion, and other mutations that creationists dogma deems impossible or maladaptive and therefore deleterious, yet here we are with demonstrably advantageous mutations. And there is the evidence of repurposed atavistic genes that, if intelligent design had been a factor, would not have been there:
DiscussionLots there for creationists to ignore or lie about:
Here, we present a case of adaptive atavism in the diadem butterfly, H. misippus, in which the derived allele is associated with a reversion to an ancestral yet adaptive phenotype. Atavisms are caused by mutational or recombination events that enable the pre-existing developmental machinery to reproduce the ancestral character (Hall 2010.1). Crucially, they are often maladaptive, as the lost phenotype has been selected against, such as hind limbs in whales and teeth in birds, or are associated with a malfunctional state such as cancer (Thomas et al. 2017). In line with this, Stephen Jay Gould revisited Dollo's law, which refers to the paleontological observation that morphological traits that are lost in an evolutionary lineage do not later on re-evolve in that lineage (Gould 1970). We present a case where the atavistic phenotype is adaptive, with the derived allele of the M locus in H. misippus producing a mimetic wing phenotype. We show that two large insertions of 2.4 and 4.3 kb are found in the dominant allele of the M locus and that these are formed by multiple TE insertions. By comparison to other Hypolimnas species, we show that the insertions are derived. Our results suggest that, from an ancestral black-and-white forewing morph, an orange morph evolved in H. misippus by a mutation in an unknown locus, and that this morph reached fixation in the population. Following that, TE insertions at the M locus created the M allele, which reverted the phenotype to the ancestral black-and-white forewing morph. Melanised apexes in the forewing with subapical white bands (i.e. forewings with black-and-white tips) are a common wing phenotype in Hypolimnas present in 81% of the species (17 out of 21 with phenotype data; Fig. 1B) and in Nymphalids such as Danaids or some Nymphalinae, including Antanartia and Vanessa species (e.g. Vanessa cardui; Fig. 4D). Here, we can understand the phenomenon of “evolutionary reversion” in the H. misippus butterfly as a molecular example of convergent evolution that is the re-evolution of the same (ancestral) phenotype via regulatory rewiring. Under this model, the original mutation that caused the change to orange wings would not be identifiable by sampling wild H. misippus, as this mutation fixed deep in the past, prior to the emergence of the M allele.
In summary, we show that H. misippus is an example of adaptive atavism in which the TE insertions in the derived M allele cause a reversal to an ancestral phenotype, the black-and-white phenotype, which has an adaptive function in Batesian mimicry. Adaptive atavism is a rare event with only a few known examples such as the re-evolution of wings in stick insects (Whiting et al. 2003) and aphids (Saleh Ziabari et al. 2023.2), sexual reproduction in oribatid mites (Domes et al. 2007), and shell coiling in gastropods (Collin and Cipriani 2003.1). Alternatively, it could be that the TE insertions are not directly causal but in linkage disequilibrium with the causal mutation …
Anna Orteu, Marek Kucka, Ian J Gordon, Ivy Ng’iru, Eva S M van der Heijden, Gerard Talavera, Ian A Warren, Steve Collins, Richard H ffrench-Constant, Dino J Martins, Yingguang Frank Chan, Chris D Jiggins, Simon H Martin
Transposable Element Insertions Are Associated with Batesian Mimicry in the Pantropical Butterfly Hypolimnas misippus
Molecular Biology and Evolution, Volume 41, Issue 3, March 2024, msae041, https://doi.org/10.1093/molbev/msae041
Copyright: © 2024 The authors/ Society for Molecular Biology and Evolution.
Published by Oxford University Press. Open access.
Reprinted under a Creative Commons Attribution 4.0 International license (CC BY 4.0)
Firstly, there is evidence of evolution in response to environmental selection pressures. Then there is the evidence of mutations creating new information for environmental selectors to work on.
Then there is the evidence of atavistic genes, that shouldn’t be there is the butterfly had been intelligently designed, being repurposed by natural selection to give an advantageous strait.
And lastly, there is the complete absence of doubt on the part of the researchers that the observable evidence would be better explained by creationism in place of the Theory of Evolution by Natural Selection.
And there is more to come yet...
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