An Adaptive Walk with Monarchs

 “The first step…shall be to lose the way.”  Galway Kinnell

(At left, monarch emerging from chrysalis, photo A. Budyak)

Throughout the summer, young citizen scientists in Madison watch the life stages of monarchs and protect vulnerable young butterflies from early predation.  They learn how to see, how to be gentle, and how to let go.  They also learn that bright coloration often says, “I don’t taste good.”  

Why don’t monarchs taste good, or worse?  Their larvae feed on milkweed leaves, and milkweeds contain toxic cardiac glycosides, such as cardinolides and galitoxin, that are poisonous to most vertebrates (think cows, sheep, birds, humans).  These compounds can cause heart rhythm changes, weakness, confusion, seizures, respiratory paralysis, diarrhea, even death in large amounts.

Indigenous medicine incorporated milkweed into treatments for respiratory and gut issues, as well as rashes and swellings, but their safe recipes aren’t widely known.  Also, what is helpful at one concentration can be harmful at another (as in arrow tips dipped in milkweed juices for hunting).  

Monarch larvae are able to eat and tolerate the toxins in milkweed leaves, and adult butterflies retain enough chemical to be a very unpleasant meal for birds.  Yes, some birds (species of orioles and grosbeaks) do more or less happily eat monarchs that are overwintering in Mexico.  They seem to know where in the butterfly the poisons are least concentrated, and likely have some tolerance?  In addition, the toxins in monarch adults break down over time.  (Photo at right of young scientist hand releasing “Ziggy,” by Amanda Budyak.)

Milkweed cardinolides work by interfering with (binding to) the mammalian sodium pump whose function is to re-set nerve cells after they fire.  Spent nerve cells with inoperative sodium pumps are therefore unable to re-charge, resulting in hearts beating irregularly or not at all.  

How did monarchs gain the capacity to eat toxic milkweed?  (See article by Tim Vernimmen of Knowable Magazine October 2, 2019 “How Monarchs Evolved to Eat a Poisonous Plant.”)  It turns out that cardinolides are unable to bind to monarch sodium pumps.  Why?  Apparently, they have three altered genes that carry instructions for making resistant pumps.  How did that evolve?  Can we know?  

(Butterflyweed with Black Swallowtail pollinator, by A. Budyak)

Well, scientists (Noah Whiteman et.al., 2012 in Nature 17 October 2019 v. 574) were able to produce fruit flies that had the same pumped-up pumps by introducing these three gene mutations, one by one.  The first mutation allowed the flies (and original monarchs it is assumed) to tolerate some toxin.  The second repaired damage that the first gene product caused, and the third allowed the flies (and butterflies) to tolerate an even higher toxic dose.  Such a multistep evolutionary gain is called an “adaptive walk,” and my analogy is that you first build a bridge, some cars (toxins) come across, cars cause some damage, you fix it, then even more cars can cross.  This “walk” allows a species to become more fit through time even though each mutation gives only a relatively small advantage.

“The order in which the substitutions evolved was explained by amelioration of antagonistic pleiotropy through epistasis.”

Vernimmen/Whiteman

As much of a mouthful as a monarch.

(At right, a Red Milkweed Beetle on common milkweed flowers at Black Earth Prairie, by S. Slapnick)