Butterfly mimicry rings – a case of natural selection?

Since Darwin’s time mimicry is presented as one of the best example of the efficiency of natural selection. Several species should have been shaped by natural selection to resemble or mimic dangerous or poisonous species. It is supposed that protected by their shape and coloration they deceive their predators. Thus mimicry confers them survival advantage. In many cases mimicry is believed to be found among butterflies where palatable species mimic unpalatable ones (so called Batesian mimicry). In some cases two or more unpalatable species look alike. In this case they should be protected more effectively because their predators learn to avoid them only once. This is called Müllerian mimicry. And in some cases there is a whole bunch of Batesian and Müllerian mimics that look alike. This is called the mimicry ring.

One of the most famous mimicry rings are so called Heliconius mimicry rings from South America. According to M.Joron species 1-16 form “tiger” mimicry ring:

1,Eueides isabella; 2,Heliconius pardalinus; 3,H. hecale; 4,Melinaea menophilus; 5,Tithorea harmonia; 6,Chetone histriona; 7,Napeogenes larina; 8,Mechanitis lysimnia; 9,Mec. polymnia; 10,Mec. mazaeus plagifera; 11,Ceratinia tutia; 12,Hypothyris cantobrica; 13,Dismorphia amphiona; 14,Eresiasp.; 15,Pterourus zagreus; 16,Consul fabius

According to M.Joron and J.Mallet (1998) who discussed the tiger mimicry ring :

Visual mimicry is a textbook case of natural selection because it is both intuitively understandable and has repeatedly evolved in a range of organisms: it is the ultimate example of parallel evolution. In many mimetic groups, particularly butterflies, a huge variety of colour patterns has arisen, even in closely related species.

This is a similar picture of the tiger mimicry ring by Seward, A. C. in “Darwin and modern science” (1909). See species 1-8:

EXPLANATION OF FIGS. 1-12.
Figs. 1-4 represent a Mimicry-ring from Eastern Brazil composed of four immune species belonging to three different sub-families and four different genera.

Fig. 1. Lycorea halia (Danainae).
Fig. 2. Heliconius narcaea (eucrate) (Heliconinae).
Fig. 3. Melinaea ethra (Ithomiinae).
Fig. 4. Mechanitis lysimnia (Ithomiinae).
Figs. 5, 6. Perrhybris pyrrha, male and female, S. American “Whites” (Pierinae). The female mimics immune Ithomiines, while the male shows only an indication of the mimetic colouring on the under surface.
Figs. 7, 8. Dismorphia astynome, male and female, also belonging to the family of S. American “whites,” and mimicking immune Ithomiines; a white patch on the posterior wing of the male and another on the corresponding surface of the under side of the upper wing, remain as traces of the original “white” coloration.
Fig. 9. Elymnias phegea, W. Africa, of the sub-family of Satyrines, mimics the succeeding species (Fig. 10).
Fig. 10. Planema epaea (gea), an immune West African species belonging to the Acraeinae.
Fig. 11. Danaida genutia, an immune Danaid from India, Burmah, etc.
Fig. 12. Elymnias undularis, female, one of the mimics of Fig. 11.

In the text we can read that “The strongest of all proofs of the theory (e.g. of origin through selection), however, is afforded by cases of true mimicry,… we can hardly hope to find more convincing proof of the actuality of the processes of selection than these cases put into our hands.”

The picture might be of interest, because it was used also by entomologist Franz Heikertinger, a strong critic of Darwinistic natural selection. It can be found in his book “Das Rätsel der Mimikry und seine Lösung: eine kritische Darstellung des Werdens, des Wesens und der Widerlegung der Tiertrachthypothesen.” (1954).

Notice that he put the word “Mimikryring” between quotation marks:

I have highlighted two species: Perrhybris pyrrha., male and female by red and Dismorphia astynome male and female by blue. Males of Perrhybris Pyrrha are white, whereas males of Dismorphia astynome have white spots on their hind wings. The question is why natural selection has not acted on them. Males of other species in the mimicry ring look like females e.g. protected. Yet we can see that some species may thrive with males not being protected at all:

So called “female limited mimicry” – dimorphic female (top) and male (bottom) of Perrhybris pyrrha.

Franz Heikertinger strongly criticized those who saw natural selection as the cause of the similarity in the mimicry ring. He named natural selection as “die Hypothese” and the proponents of such a view as “Hypothetiker”. According to his opinion several questions must be answered before natural selection can be accepted as a plausible explanation of the phenomenon.

1) What are butterflies vision-oriented predators that select them? Do they exist?
2) Are unpalatable insects rejected by predators?
3) Are those rings maintained by natural selection or is the similarity between the species just a consequence of their relatedness?
4) Is such a coloration something that is beyond natural variation of the species?

Needless to say that Heikertinger answered to the all previous questions negatively:

Ad 1) and 2) These questions had been discussed by Heikertinger very thoroughly and repeatedly in many of his publications. He had dismissed birds as the predators of butterflies. I hope I will summarize his arguments in another place. In the case discussed I just quote J.Mallet (1994):

Heliconius(especially the erato taxonomic group) are renowned for roosting gregariously; and co-mimics roost gregariously with each other more often than with non-mimics. Gregarious roosting is therefore common between species, as well as within species.The paradoxical correlation between nocturnal roosting and visual mimicry is presumably explained by bird predation at dusk when roosts are forming, or at dawn before they have disbanded. Direct evidence of predation is lacking, but there are high rates of disturbance by birds at these times.

Ad 3)
It is important to notice that mimicry is supposed to exist only between unrelated taxa. No one will be surprised seeing two closely related species looking alike (for instance tiger and leopard, family Felidae). There are plenty of cases where butterflies of non-overlapping and distant regions look similar. Their similarity is explained by their relatedness and not by convergent evolution driven by natural selection. Even though natural selection is sometimes mentioned as well:

Hypolimnas misippus (Nymphalidae), “model” from Southeast Asia

Limenitis albomaculata (Nymphalidae), “mimic” from West China

According to Edward Poulton the selective agent here are some unspecified migratory birds. Even Komárek (2003) named such an explanation something between a folk tale and “positive science”.

The species in the tiger mimicry ring belong predominantly to family Nymphalidae (and especially to subgroup Ithomiinae). Two exceptions have been already mentioned: Dismorphia astymone and Perrhybris Pyrrha (species with non-mimetic males). Dismorhiinae is subgroup of family Pieridae (“Whites”). Yet Heikertinger refutes such a categorization. In his view categorization based on tarsal claws and numbers of segments on butterfly forelimbs might be misleading. He noticed that we often observe reduced number of segments in butterfly males (as a consequence of Eimer’s Orthogenesis. Theodor Eimer claimed that males are more “developed” than females, which tends to retain original features of the species). Such a categorization would lead to two different groups with males and females separated. Heikertinger compared venation on wings and concluded that according this feature Dismorhiinae are more related to Nymphalidae (the base of the mimicry ring) than to Pieridae.

In the first row is the similarity between veins of 22.Dismorphia arsinoe and 23.Mechanitis polymnia (Ihtomiinae). The last row are veins of Perrhybris malenka (Pieridae).

In the case of Perrhybris Pyrrha Heikertinger quoted Eimer, Piepers, Dixey and Van Bemmelen that the ancestor of the species was not white (as it might be commonly believed), but varicolored. Consequently the supposed transition of P.pyrrha into varicolored mimic somehow loses its mysteriousness. On the other hand there isn’t any pattern on P. Pyrrha wings upon which natural selection could act towards the mimicry pattern. Quite the opposite – the males of P.Pyrrha have left or receded from the common pattern in the mimicry ring – despite the supposed unified pressure of natural selection. He refers to Eimer observation that females in Pieridae are often colored whereas males are not – Pieris brassicae, Harpaenia eriphia and others.

Perrhybris. Heikertinger quotes Dixey according to whom the transition goes from males of P.locusta. P.phaloe, P.lypera, P.lorena to P.pyrrha (some of them by red arrow). Those forms make a connection but there is nothing that could resemble Ithomiinae and consequently to be of a selective value upon which selection could have acted.

Ad 4)
This is a point which Heikertinger often addresses. He recommends to readers to open an atlas of butterflies and compare related species. There is an abundance of varicolored butterflies in each taxa. Heikertinger claims that picking up just one species from a series doesn’t make case for natural selection. A resemblance can be explained by Vavilov’s homologous sequences as well. In the case of the tiger mimicry ring he recommends to open Seitz’s Butterfly atlas volume V and see that the mimicry pattern is actually recurring in many variants across many taxa.

One should compare all the fantastic coloration and patterns of Heliconius (family Nyphalidae) with tiger mimics – table 75 -78 from Seitz atlas volume V:

and see the discussed recurring type also among Actinote:

or the same type on the table 91, 92 the row C:

Table 103, the row E:

Table 143, the row B:

or Phycoides Table 90, the row h:

Dismorphia, table 30:

and others.

According to Heikertinger the coloration and pattern types on insects are often recurring phenomena. The resemblance repeats. Why there should be a different explanation for some arbitrary chosen resemblances than for thousands of other patterns and coloration?

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Literature:

Theodor Eimer: Orthogenesis der Schmetterlinge (1897)

Franz Heikertinger: Das Rätsel der Mimikry und seine Lösung: eine kritische Darstellung des Werdens, des Wesens und der Widerlegung der Tiertrachthypothesen. (1954)

Adalbert Seitz: Die Gross-Schmetterlinge der Erde (1906-1928)

Mathieu Moron: Mimicry (2003)

Click to access joron02mim.pdf

Mathieu Joron, James L.B. Mallet: Diversity in mimicry: paradox or paradigm? (1998)

Click to access diversity%20and%20evolution%20mimics.pdf

James Mallet: Why are there so many mimicry rings? Correlations between habitat, behaviour and mimicry in Heliconius butterflies.(1995)

Click to access Mallet%26Gilbert95.pdf

Michael Braby, Roger Vila, Naomi Pierce: Molecular phylogeny and systematics of the Pieridae(Lepidoptera: Papilionoidea): higher classification and biogeography. (2006)

Click to access 2006_Braby_et_al.pdf

Stanislav Komarek: Mimicry, aposematism and related phenomena. Mimetism in nature and the history of its study. (2003)
http://stanislav-komarek.cz/mimicry/