Friday, 28 September 2012

Experimental taxonomy at home.

Ernst Mayr pioneered the biological species concept, an idea that brought taxonomy of species into line with population genetics and evolution.  The idea is that a species is defined by the genetic relationships among its members; they’re all part of one big potentially-interbreeding population.  In Linnaeus’s day people sought to classify species based on what they looked like, rather than who they could breed with.
Using appearance is a pretty good proxy for the ability to interbreed, and much of the time it’s what taxonomists still do, simply because doing the breeding experiments or measuring genetic relationships among individuals is just too time-consuming.
But there are two classes of concerns that arise.
On one hand, individuals belonging to the same species can look very different.

Sometimes juveniles are hugely different from adults, like caterpillar and butterfly, elva and eel, or juvenile vs adult lancewood.  In a New Zealand plant example, Jim Le Comte and Colin Webb (Le Comte & Webb 1981) showed experimentally that the speargrass Aciphylla townsonii is actually the juvenile form of A. hookeri.  Different juveniles seem to be a feature of New Zealand plants, but they're common elsewhere too.
Juvenile (left) and adult foliage of mataī (Prumnopitys taxifolia)
 Secondly, small genetic differences can lead to quite big visible differences in plants or animals that belong to the same species.  Some of these are simple polymorphisms, like eye colour in humans.  In Veronica amplexicaulis, a hairy form used to be distinguished as a separate species (Garnock-Jones & Molloy 1983, under the old name Hebe amplexicaulis).  But it turns out this difference is the product of two alleles of a single gene, as are occasional flower colour variants in many plants.
White and blue viper's bugloss, Echium vulgare, growing side by side (Black Birch Range, Marlborough).
Thirdly, local populations might adapt to special conditions.  On mine tailings, where toxic heavy metals pollute the soil, plants may acquire tolerance, and this could involve some differences in form or in underlying physiology, yet they still freely mate with the non-tolerant individuals nearby.  These are classified as ecotypes, but not as separate species.  The differences are maintained by strong selection, even in spite of free gene flow between the tolerant and intolerant plants.
The form of Veronica albicans that grows on the dolomite outcrop at Mt Burnett looks a little different from other populations of this variable species; it might have adapted to its substrate, yet there's no evidence that it can't exchange genes with the rest of its species.
 Fourthly, some plants and animals are able to alter their form to cope with different environments they find themselves in or to escape predators—phenotypic plasticity or polyphenism.  Some inchworm caterpillars develop different appearances to blend in with the foliage of whatever host plants they’re living on (Greene 1989).  The underwater and aerial leaves of aquatic plants can be hugely different.  Plants can have very different leaf shapes, or even leaf anatomy, depending on the amount of sunlight they’re receiving or even what season they’re in.
Eryngium vesiculosum has very different leaves in summer (above) and winter (Webb 1984).
In all four of these situations, the result is two different looking plants growing together side by side, giving the appearance of two distinct species that aren’t interbreeding.  That’s just the sort of thing that gets taxonomists and field botanists excited, because we always like to discover a new species.
On the other hand, the reverse situation can arise.  Two species can look so similar that their existence isn’t even suspected until genetic tests are done.  These are called cryptic species.
It’s important to be aware of these possibilities, and in fact to rule them out as explanations before jumping to the conclusion that the variation we’re observing is due to the existence of more than one species.  The idea that two different-looking plants growing side by side must be different species is simplistic, yet "side by side" has become a bit of a mantra in some circles.
One way to test these potential new species is by growing different-looking plants together in uniform environments—common garden experiments—and also growing genetically identical plants in different environments—reciprocal clone transplants.  These approaches were pioneered in the first half of last century by Swedish botanist Turesson and by American botanists Clausen, Keck, & Hiesey.
Veronica lanceolata in flower, Rimutaka Range.
The speedwell hebe Veronica lanceolata is widespread in the North Island of New Zealand and a few parts of the South Island.  Each region has its own form of the species and, in general, adjacent populations are quite similar.  With some familiarity, it’s possible to tell from its appearance where a plant has come from.  These differences are maintained in common garden experiments, but I don’t regard these forms as different species because they can cross freely, their flowers and fruits are very similar, the differences are quantitative rather than qualitative, they have the same chromosome number, and the changes are mostly gradual and continuous from place to place.
Each leaf is from a different population of Veronica lanceolata.
However, there are places where two very different-looking forms grow together side by side, and this is exactly the sort of situation where a simplistic "side by side" approach might lead a botanist to the view that two species are involved.  In the Ruahine and Kaimanawa Ranges, especially on limestone cliffs, there are low-growing small leaved plants growing together with bushier large-leaved plants.  Although their leaves and stems are different in size and stature, their flowers and fruits are the same, which is a bit of a clue that these plants are responding in a plastic way to their environments, that there are no underlying genetic differences, and no breeding barriers between them.  I’d always assumed so at any rate, even though some field botanists made numerous collections of both forms, mounted them as separate accessions, and labelled them to highlight the differences and the fact they grew together side by side.  The hint was implicit: these might be different species.  Perhaps fortunately, nobody had the confidence in their hunch to give them different names.
South end of the Maungaharuru Range.
A couple of summers ago I was in the Maungaharuru Range in central Hawkes Bay with my colleague Heidi Meudt from Te Papa.  We were looking for forget-me-nots along the tops for a detailed genetic study she's conducting into their taxonomy and evolution.  Along the cliffs at the south end of the range we found Veronica lanceolata growing in mostly shady sites among mosses and algae.  But when we stumbled into some sink-holes things got interesting.  Here were moist shady sites with quite large-leaved plants, very close to sunny outcrops with tiny creeping plants.  It was an ideal opportunity to test my hunch that these were just plastic responses to moisture and shade.

There wasn’t room in the garden at home for a large randomised trial, so I sampled just a couple of plants of each type from sites only a few metres apart, and brought them home to grow in pots.  I also pressed branches of each, to record and preserve how they had looked in the wild.
Collection 2834, small and large leaved plants just after potting, Feb 2011.

Collection 2836, a small leaved plant just after potting, Feb 2011. The white plastic labels are 13 mm wide.
They’ve been growing now for about 18 months, and some, but not all, of the changes are quite dramatic.  For 2384, the small-leaved plant now has somewhat bigger leaves, but it's still distinctly smaller than the large-leaved plants.  For 2836, leaves are now up to 20 mm long, whereas they were about 5 mm before.
Both surfaces of the largest leaves from each of the three plants (two from 2836 small), Sep 2012.
So the results are a bit mixed, and this shows how important it is to use large samples, not just a couple of plants, and to randomise the trial properly.  The plants have exhibited some phenotypic plasticity but that doesn't account for all the differences.  Note also the two very different leaf shapes from the same plant of 2836: more evidence of plasticity.  Maybe both phenotypic plasticity and ecotypic differentiation are happening in this population.  Next time I'm in a position to collect a bigger sample and repeat this experiment I will do so.  In the meantime, I can try crossing the small- and big-leaved plants this summer.  My expectation is the offspring will be fully fertile.
With these speedwell hebes, the differences in growth form and leaf shape are striking, but they aren’t sufficient to compel rejection of the hypothesis that they’re the same species, because there are two different and simpler explanations—phenotypic plasticity and ecotypic differentiation—for that pattern.  My simple experiment hasn't clearly demonstrated which is happening, because the experimental design and sampling are insufficient.  But it's important to note also that these are quantitative differences—leaf shape and size—just the sorts of things that often vary in natural populations.
I'm sure it’s possible to test species status scientifically and explicitly.  That means starting with a testable hypothesis.  It’s better to start with the hypothesis that the two entities are conspecific, because any differences are evidence to the contrary that would compel us to reject the hypothesis.  If instead we start with the hypothesis that they’re different species, it’s hard to imagine how many similarities between them would compel us to reject that idea.  And if we start with the hypothesis that there are two species, and then seek evidence to support the hypothesis, then we're not doing science, at least not as it was formulated by Karl Popper.

Garnock-Jones, P.J.; Molloy, B.P.J. 1983.  Polymorphism and the taxonomic status of the
Hebe amplexicaulis complex (Scrophulariaceae).  New Zealand Journal of Botany 20: 391–399.

Greene, E. 1989. A diet-induced developmental polymorphism in a caterpillar. Science 243: 643-646.

Le Comte, J.R.; Webb, C.J. 1981.   Aciphylla townsonii — a juvenile form of A. hookeri (Umbelliferae).  New Zealand Journal of Botany 19: 187–191.

Webb, C.J. 1984.  Heterophylly in Eryngium vesiculosum (Umbelliferae). New Zealand Journal of Botany 22: 29–33.

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