Tiny microbe turns tropical butterfly into male killer

Scientists from Kenya and the United Kingdom have helped to identify a male-killing microbe in a common East African butterfly called the African Queen (also known as the African Monarch), which leads to the death of all sons when a mother butterfly is infected.

This discovery was made by a group of scientists including Dr. David Smith and Dr. Ian Gordon who have worked on this butterfly species for many years in East Africa, working with Professor Richard ffrench-Constant of the University of Exeter, Professor Walter Traut from the University of Lübbek, Dr Jeremy Herren from the International Centre of Insect Physiology and Ecology (icipe), Steve Collins of the African Butterfly Research Institute (ABRI), Kennedy Saitoti, a student affiliated with the National Museums of Kenya, Piera Ireri of Kenyatta University and Dr. Dino J. Martins who chairs the Insect Committee of Nature Kenya and is the current Executive Director of the Mpala Research Centre.

Tiny microbe turns tropical butterfly into male killer
African Queen Butterfly. Photo credit: Dino J. Martins

In most of Africa this microbe, called Spiroplasma, infects African Queen butterflies but has no effect on their offspring.  However, in a narrow zone around Nairobi in Kenya, where two sub species of butterfly live and breed, the scientists noted that the microbe infection caused all their sons to die. In fact the male eggs never hatch and are often consumed by their hungry sisters.

The authors of the paper, published in the Royal Society journal Proceedings of the Royal Society B, believe that the phenomenon, which takes place where two sub species meet, is the first step in the transition of the two sub-species into two true, non-interbreeding, species.

Professor Richard ffrench-Constant, from the Centre for Ecology and Conservation at the University of Exeter’s Cornwall campus, and a team of British, Kenyan and German scientists, have found that the chromosomes of the females in which male-killing occurs have changed dramatically with a non sex chromosome fusing with a sex chromosome to form a new chromosome called ‘neo W’.

Professor ffrench-Constant, Professor of Molecular Natural History, said: “We tend to think of new species coming about due to environmental changes but here its clearly the microbe that is driving these two sub species apart.

“Whilst we don't understand the precise molecular mechanisms behind this chromosomal merger, this means that no males are made in the hybrid zone, and that mating success in the zone is effectively zero, thereby creating a barrier with a new species on either side.”

This paper represents the culmination of over 30 years of field work in which the sex and colour pattern of butterflies around Nairobi was painstakingly recorded by a team led by Dr Ian Gordon based in Nairobi. Ian Gordon explained that “Some of the field data came from students at the University of Nairobi who collected and reared wild butterfly eggs in the 1980’s during their coursework in Evolutionary Biology”. The breakthrough came when female butterflies from the all- female zone were sent to Germany to have their chromosomes examined and where Professor Walther Traut from the University of Lübbek discovered that two of the chromosomes had fused.

Dr David Smith, formerly from the Natural History Museum at Eton College, first author on the paper, said: “The neo-W effectively acts as a genetic sink for all males, and butterfly populations around Nairobi are nearly all female. Our results demonstrate how a complex interplay between sex, colour pattern, male-killing and chromosomes has set up a genetic ‘sink’ that keeps two subspecies apart.”

Professor Walther Traut, from the University of Lübbek, said: “This is like a smoking gun for the way in which species become distinct. It is rare that we can find the molecular basis for how species develop.”

Professor ffrench-Constant added: “It appears that the butterfly’s susceptibility to the male-killing microbe is driving the separation of the two butterflies into two true species. These tiny microbes are therefore having a major effect on sex and death in this fascinating butterfly.”

This study shows how much we can learn from insects and the natural world, and from butterflies in particular. Nairobi is home to two of the largest and most important collections of African butterflies housed at the Entomology Section of the National Museums of Kenya and at ABRI. This also highlights the importance of these collections as reference material for understanding the natural world.

Steve Collins of ABRI said, “this study shows new ways of thinking about evolutionary processes in animals, and highlights how amazing butterflies are as a model for this type of basic, cutting edge research.”

Kennedy Saitoti, who has worked on this study for over two and half years, says “Many people are aware of the incredible biology of the North American Monarch Butterfly, but few know that the African Monarch (aka African Queen) is just as fascinating and it would be great to see more Kenyans taking an interest in the natural world and biodiversity we have in our country”.

Dr Jeremy Herren, of icipe, who worked on the Spiroplasma aspects of the study, said “This study nicely demonstrates the complexity of interactions between insects and maternally-inherited bacteria that manipulate their reproduction. Many researchers believe these bacteria might be useful as a strategy to control insects that transmit diseases and destroy crops and therefore it is very important that we better understand how they affect their hosts.”

Citation for this article:

Smith DAS, Gordon IJ, Traut W, Herren J, Collins S, Martins DJ, Saitoti K, Ireri P, ffrench-Constant R. 2016 A neo-W chromosome in a tropical butterfly links colour pattern, male-killing, and speciation. Proceedings of the Royal Society B 283: 20160821.

Funding:

This research has partly been funded through a grant from the Wellcome Trust Sir Henry Wellcome Postdoctoral Fellowships awarded to Dr Jeremy Herren (icipe), and by the National Geographic Society, Princeton University and Turkana Basin Institute, which have supported Dr. Dino J. Martins’ contribution.

For further information in Kenya, please contact:

Dr Jeremy Herren, ICIPE (+254 716 660 160)
jherren@icipe.org

Steve Collins, ABRI  (+254 722 701 021)
collinsabri@gmail.com

Kennedy Saitoti (+ 254 727 301 275)
kensai5@ymail.com

Dr Dino J. Martins, Nature Kenya/Mpala Research Centre (+254 733 673 493)
dino.martins@gmail.com