The Small White Butterfly's Reproductive Tract Which Also Digests

Small white butterfly (Pieris rapae)

Today I have a little story based around a research paper which I just read. It turns out that female butterflies have an organ in their reproductive tract that is similar in some ways to a stomach/intestine.  This organ, called the bursa copulatrix, digests the male butterfly's spermatophore proteins but little was known about how it functioned before this study.

The study was carried out on the small white/small cabbage white/white butterfly (Pieris rapae).  The small white is not a New Zealand native, but was introduced to New Zealand long ago and is now well established throughout the country, even reaching the subantarctic islands.  The small white caterpillar eats human agricultural crops (cabbage and other brassicas in particular), and so has been able to spread from its native range in Europe, Asia, and Africa across the globe following human agriculture and is now found in North and South America and Australia as well as countless islands around the globe.  It was accidentally brought to New Zealand in 1929 or 1930 and within a very few years had spread across the country.  It is now incredibly common and can be seen easily in agricultural areas in particular.  It is the only species of butterfly with primarily white wings in New Zealand (the great white butterfly (Pieris brassicae) was accidentally introduced to the Nelson area in 2010 but was exterminated in 2016- the first extermination of an invasive population of a butterfly species in the world).  The caterpillars of the small white eat our crops and so became a pest immediately.  Shortly after their arrival in New Zealand steps were taken to reduce the impact of the little white, in the form of the introduction of the parasitoid wasp Pteromalus puparum in 1933 which parasitises the pupal stage of the little white and the introduction of another parasitoid wasp, Cotesia glomerata (formerly Apanteles glomeratus), in 1938-1939 which parasitises the larval stage of the little white.  Unfortunately, the assumption that P. puparum would also attack the native New Zealand red admiral butterfly (Bassaris gonerilla) was not considered to be of great concern at the time but turned out to be accurate.  Since that time the native red admirals have become much less common, likely as a result of very high parasitism from another wasp parasitoid (Echthromorpha intricatoria) which apparently self-introduced from Australia around 1900 combined with lower parasitism rates from the aforementioned P. puparum.

Enough about the small white's history in New Zealand- time to get back to the interesting aspect of their digesting reproductive tract.  A little background information first: we often think about male and female mated partners working together to help each other to produce offspring which will pass their genes on to future generations.  This is an accurate depiction but is not necessarily all that is going on.  There is often (or perhaps usually, or maybe even always) competition between the male and female, with each trying to ensure that they maximise their own genetic survival in future offspring.  This can happen in many ways.  One of the most obvious ways is "cheating" on your partner.  When a male does this, he creates the possibility that he will produce some offspring with other partners as well as potentially producing more offspring in total than if he stayed faithful to one female.  When a female does this, she will (potentially) not produce more offspring in total but, like the male, improves the chances that she will produce some of those offspring with other partners.  Increasing the number of partners which parent your offspring is a good way to hedge your bets genetically.  If one partner has a serious genetic defect, as long as the other partners do not you will produce at least some offspring without the defect.  Also, if some partners have genes that will be advantageous under certain conditions, while other partners have genes that will be advantageous under other conditions, you are likely to have descendants that will survive regardless of the conditions prevalent if you are producing offspring from different partners, while that may not be the case if you stick with one partner.  So, in summary, it is often advantageous for an animal to cheat on its partner.  It is also advantageous for that animal to minimise the amount of cheating that its partner engages in to maximise its own genetic investment in the offspring it is raising.  Hence, conflict between the partners.  Now it should be borne in mind that this explanation in no way is meant to be an in-depth description of the science of the conflict between males and females over parental investment.  It is stupefyingly over-simplified. People have written entire books on the subject and have barely scratched the surface.  Conflict between the sexes presumably goes back as far as there have been sexes.  This short explanation is purely to give novices a brief grasp of an aspect of the science so that we can follow through to the next part about butterfly anatomy together.

In the small white, when a male mates with a female he deposits a spermatophore inside the female's reproductive tract.  From that spermatophore, the sperm are moved to a specialised sperm-holding area (the spermatheca), while the rest of the spermatheca is digested by the bursa copulatrix.  In many butterflies, the spermatophore has several important functions after the sperm are removed from it.  The spermatophore is a good source of protein for the female, as she digests it in her bursa copulatrix, providing her with extra nutrients to produce better eggs which helps increase the genetic fitness of both the male and female. The spermatophore also takes up space in the female's reproductive tract, preventing other males from mating with the female until most of it is removed.  The longer it remains, the higher the percentage of the offspring are likely to be that male's, so there is an advantage for the male to keep the spermatophore in place as long as possible.  It turns out that is just what we find.  In species where females mate with more males, males produce tough exteriors around the softer, more easily digestible, parts of the spermatophore.  Females of those same species on the other hand have been found to have toothy adaptations to the bursa copulatrix to counter the tougher exterior of the spermatophore, helping to reduce digestion time.  The study I read looked at the digestive capacity of the bursa copulatrix in small whites, and their findings are incredibly cool.  They discovered that the small white's bursa copulatrix had a wide array of digestive enzymes and that the digestive rates occurring within the bursa copulatrix are as high, or in most cases higher, than is found in the digestive tract of the caterpillar stage of the same species.  Think about that for a moment: their digestive tract is less efficient at digesting than an organ in their reproductive tract.  The digestive tract's entire job is to digest food for the growth and survival of the animal.  For a part of the reproductive tract to be digesting at a higher level suggests very strongly that there is a really important reason for the female to break down the spermatophore as quickly as possible.  That reason appears to be that it is more advantageous for her to have offspring sired by more than one male.  There are innumerable amazing interactions going on throughout biology, and so many of them are at levels that we are only just beginning to be able to look into with newer technologies.  The living world is crazy cool, and the more that we learn the more we realise that we do not yet know.

One of the things I enjoy the most about reading scientific articles and books is that they get me thinking about possibilities.  This paper got me wondering about what you would find if you looked at a butterfly species which wasn't polyandrous (where a female mates with several males).  I am guessing that the bursa copulatrix would have a much lower rate of digestion, since there would be no real hurry to get the spermatophore out of the way.  It has also gotten me wondering about how many species of native New Zealand butterflies are polyandrous.  Currently I have no idea.  Perhaps that will be a blog for another day, if I don't get distracted by something else first, which I almost certainly will.

If you think this is as cool as I do, check out the references below that I used and learn much, much more about it (click the links on each to go to the source).  Then follow the references in each of the references and see how far down the rabbit hole you feel like going.  Science rocks!

J.W. Ashby & R.P. Pottinger (1974) Natural regulation of Pieris rapae Linnaeus (Lepidoptera : Pieridae) in Canterbury, New Zealand, New Zealand Journal of Agricultural Research, 17(2), 229-239. https://doi.org/10.1080/00288233.1974.10421002

M.C. Barron, S.D. Wratten & N.D. Barlow (2004) Phenology and parasitism of the red admiral butterfly Bassaris gonerilla (Lepidoptera: Nymphalidae). New Zealand Journal of Ecology, 28(1), 105-111. http://www.jstor.org/stable/24058217

P.J. Cameron, R.L. Hill & W.P. Thomas (1993) Analysis of importations for biological control of insect pests and weeds in New Zealand. Biocontrol Science and Technology, 3, 387-404. http://doi.org/10.1080/09583159309355294

P.J. Cameron & G.P. Walker (2002) Field Evaluation of Cotesia rubecula (Hymenoptera: Braconidae), an Introduced Parasitoid of Pieris rapae (Lepidoptera: Pieridae) in New Zealand. Environmental Entomology, 31(2), 367-374.  https://doi.org/10.1603/0046-225X-31.2.367

Department of Conservation. (n.d.). Great white butterfly. Retrieved from http://www.doc.govt.nz/nature/pests-and-threats/animal-pests/great-white-butterfly/

M. Hasenbank, A. Brandon & S. Hartley (2011) White butterfly (Pieris rapae) and the white rust Albugo candida on Cook’s scurvy grass (Lepidium oleraceum). New Zealand Journal of Ecology, 35(1), 69-74. http://www.jstor.org/stable/24060633

M.S. Plakke, A.B. Deutsch, C. Meslin, N.L. Clark & N.I. Morehouse (2015) Dynamic digestive physiology of a female reproductive organ in a polyandrous butterfly. The Journal of Experimental Biology, 218, 1548-1555. http://doi.org/10.1242/jeb.118323

V. Sánchez & C. Cordero (2014) Sexual coevolution of spermatophore envelopes and female genital traits in butterflies: Evidence of male coercion? PeerJ, 2, e247. http://doi.org/10.7717/peerj.247

V. Sánchez, B.E. Hernández-Baño & C. Cordero  (2011) The evolution of a female genital trait widely distributed in the Lepidotera: Comparative evidence for an effect of sexual coevolution. PLoS One, 6(8). http://doi.org/10.1371/journal.pone.0022642