Relaxed selection can lead to surprising outcomes

Our understanding and expectations of how natural selection should lead to adaptive evolution in the wild is heavily informed by predictions derived from theoretical and laboratory studies. These, although useful in expanding our understanding of evolutionary processes, tend to consider only a single source of selection, and thus do not encompass the complexity of natural environments where multiple sources of selection interact simultaneously. Field surveys, on the other hand, do integrate the complexity of nature, but are limited in their ability to disentangle cause and effect. As a result, field studies often do match our predictions – but sometimes our predictions totally miss the mark, and it is difficult to figure out why. A way of bridging these two approaches is to experimentally manipulate an environmental factor of interest in nature, allowing cause and effect to be connected even in a complex system.

Evidence that drastic changes in an organism’s environment can lead to rapid adaptive evolution has proliferated in the past 20 years.These drastic changes come in many forms and flavours, but they generally involve the emergence – or, less frequently, the loss – of a selective factor. Several studies in the wild report that introducing new predators, contaminants, competitors, or parasites can lead to an increase in the ability of the affected populations to deal with the new stressors; the population adapts to the new source of selection. We commonly assume that the reverse should also be true: the loss of a source of selection (i.e. relaxed selection) should lead to the loss of the ability to deal with that stressor. However, there is good evidence suggesting that traits might not change for relatively long periods of time after the loss of a source of selection (see Lahti et al. 2009), perhaps because change might be driven only by drift, if the cost of the adaptation to the stressor was very low.

Through a series of field introductions in collaboration with the FIBR Guppy Project we tested whether removing Gyrodactylus spp., a common and deleterious ectoparasite of wild guppies, would lead to the evolution of decreased resistance in their guppy hosts. As it turned out, this experiment was one of those studies where predictions totally missed the mark, and because of that it broadened our understanding of the evolution of resistance to parasites in the wild.In a nutshell, theory suggests that individuals that invest more in defence against parasites are expected to do so at the cost of investing in other fitness-enhancing traits. When parasite-induced mortality increases in a population, those individuals that are better able to resist infection will have a higher genetic representation in future generations. On the flip side, when the negative effects of parasitism decrease, those individuals that, for example, invest more in reproduction than defence will have a competitive advantage over resistant individuals. A number of elegant laboratory experiments support these predictions, but these mostly focus on “simple” organisms (typically bacteria and protozoans, although there are some important arthropod studies).

The rain forest of Trinidad: home to guppies and their parasites
(Photo A. Hendry)

Given these clear predictions, we set out to test whether, under the complexities of a natural environment, removal of parasites would lead to the evolution of decreased defence to parasites in a vertebrate host with a complex immune system. What we found was surprising. Both four and eight generations after being released from parasitism, our female guppies had repeatedly increased – yes, increased! – their resistance to the parasite relative to the ancestral population (read the paper here).

This increase in resistance could have been due to various methodological artefacts, and we thought of some biological hypotheses for the outcome as well. We ruled out methodological artefacts such as differences among populations in mortality (it was not the case that less-resistant individuals died earlier, albeit with less parasites, than more-resistant individuals) or size (it was not the case that that the ancestral individuals were larger and thus provided more resources for a larger parasite load which would have made them appear to be less resistant). Among the biological explanations that we discarded was the possibility that we were actually seeing the effects of selection for tolerance, not for resistance. In the parasite literature, resistance refers to the ability of hosts to reduce the number of parasites they have, while tolerance is the ability to reduce the damage caused by a given number of parasites. Resistance and tolerance are expected to trade off against each other: high resistance means that parasite numbers are low, so investing in reducing their negative effects would be a waste of resources; high tolerance means parasites cause little damage, so investing in reducing their number would also be a waste of resources. If parasite removal was causing selection for decreased tolerance, then resistance could be indirectly increasing as a response. But we found that tolerance did not change much – if anything, it also increased after parasite removal.

Experimental guppies, parasites and me in the lab (Photo: G. Capurro)

We present several lines of evidence that suggest that this increase in resistance after decreasing selection from parasites is also a common outcome in wild guppy populations. We think this has to do with one of the “interacting factors” present in natural systems: predation. As part of the experimental translocations our guppy populations faced a strong shift not only in parasite pressure, but also in predation-induced mortality, since they were translocated into sites where major predators were absent. Changes in predation have been shown to induce rapid evolution of life-history traits in guppies, and some life-history traits such as life expectancy are known to correlate with resistance to parasites. In our case, it seems that release from predation and the evolved increase in life expectancy that it brings could be pleiotropically producing increased resistance (an idea known as the pace-of-life hypothesis). In the wild, parasites generally don’t just disappear, so this pleiotropic connection between lifespan and resistance would be adaptive: when predators are present,an early death is likely and resistance to parasites is an unnecessary luxury, so individuals might use all their resources in reproducing as early as they can, but when early death due to predation is unlikely, low parasite resistance might greatly reduce your fitness.

Like all good research, this study has led us to new questions. For example, how often does the pace-of-life hypothesis apply in other systems, and under what circumstances? And more generally, is predation always a stronger selective force than parasitism, even for traits such as resistance that are directly related to parasites?

The paper:

    Dargent F., Scott M.E., Hendry A.P., Fussmann G.F. 2013. Experimental elimination of parasites in nature leads to the evolution of increased resistance in hosts. Proc R Soc Lond B Biol Sci 280(1773). (doi:10.1098/rspb.2013.2371).

One Direction as a metaphor for the benefits of genetic diversity

I am currently in Fukuoka, Japan, at a workshop organized by Tet Yahara, Makiko Mimura, and others that is focused on developing a Genetic Diversity Report. The basic idea is that biodiversity science and policy currently focuses on species and their benefits to humanity, such as ecosystem services. This perspective misses the critical point that genetic diversity within species is incredibly important to those species and to their benefits to humanity.

Every day during the workshop, we have been taking the subway from our hotel to Kyushu University and, every time, we have been saturated with posters of five young men (boys, really) who are clearly pop stars of some sort or other. The posters are all over the walls and hang every few meters along the ceiling of every subway car. During each commute, we probably saw 100 posters (surely a dozen would have sufficient). But what was the message? Who were these guys and what were we supposed to be buying? Having seen these posters a few hundred times (so maybe a dozen posters wasn’t sufficient after all), I started to get curious and looked for a hint on the poster – but everything was in Japanese, except for two small words “One Direction.” Oh, I had heard of them – the current generation’s boy band, like N’Sync or The Backstreet Boys or New Kids on the Block of previous generations. It seems One Direction was to “perform” soon in Fukuoka – although we couldn’t figure out the date.

One Direction (top) and No Direction (bottom). From left to right: Peter Prentis, Bruce Walsh, Andrew Hendry, George Roderick, and Peter Hollingsworth. (Photo: Chris Kettle.)

This got me to thinking. One of the key features of boy bands (and girl bands – Spice Girls!) was that they were carefully constructed for diversity. One boy was the sensitive type, one was the bad boy, one was the jock, and so on. Here is how Wikipedia explains it:

Seen as important to a "boy band" group's commercial success is the group's image, carefully controlled by managing all aspects of the group's dress, promotional materials (which are frequently supplied to teen magazines), and music videos. The key factor of a boy band is being trendy. This means that the band conforms to the most recent fashion and musical trends in the popular music scene. Typically, each member of the group will have some distinguishing feature and be portrayed as having a particular personality stereotype, such as "the baby," "the bad boy," or "the shy one." While managing the portrayal of popular musicians is as old as popular music, the particular pigeonholing of band members is a defining characteristic of boy and girl bands.

Our main goal as a group is to convince people, including policy makers, who don’t normally think about genetic diversity that they should be doing so. We came up with a list of the benefits that seemed quite clear to us – but how to convince people who weren’t already converts? I suggest the One Direction metaphor:

Complementarity: By carefully assembling alternative stereotypes into the band, the manager seeks to appeal to various “diverse” segments of teenage girldom. If all of the boys were the same (clones of each other, for example), then presumably some girls would not be interested and the records and concerts would make less money. The same concept applies in biodiversity. If a diversity of phenotypes/genotypes exists in a population, then the population might use a greater diversity of habitats and thereby increase in total abundance. Similarly, a more diverse set of genotypes will be more resistant to the negative effects of diseases, which can’t then evolve to specialize on any single genotype. A great example is provided by the diversity of rice types in Chinese agriculture increasing resistance to pathogens (Zhu et al. 2000).

Portfolio effect: The appeal of different boy stereotypes to young record-buying and concert-going girls presumably varies through time. In some years, bad boys might be more popular, in other years, the sensitive types might be more popular. Or perhaps each girls goes through their own preference arc as they get older – maybe they like the shy one at first, grow into the cute one, and graduate to the bad boy. By having multiple types in the band, the overall popularity of the band might remain more consistent/stable through time. The same effect again applies to biodiversity. If a number of different types are present in the population and those different types are differentially susceptible to environmental conditions that vary through time, then a more diverse group will have greater stability through time. A great example is how the diversity of sockeye salmon populations in Bristol Bay, Alaska, buffers the entire production of the bay (and therefore harvesting by humans) in the face of considerable environmental variation through time (Schindler et al. 2010).

Option values: By having a diversity of boy types in a band, managers can increase the chances that some future popularity trend will be captured by existing membership in the band. Perhaps the shy type isn’t popular now but it will be next year. In biodiversity science, option values can work something the same. For instance, some types in a population might not be of much benefit for the population (or humans) now but perhaps they will be under future environmental change. Or perhaps certain types that aren’t obviously useful to humans in the present will eventually become so as we better understand their beneficial properties.

Potential for change: Related to option values – but with a different emphasis – diversity within a band can increase the potential for future change. Perhaps the preferences of future pre-teen girls are not well foreseen by the current stereotypes in the band but one of the key features of boy bands is that the producers can modify them to try to match changing trends – and the greater diversity of types to start with the greater the chance they can be modified into a future preferred type – and the greater the chance the band (or parts of it) will persist into the future. (Justin Timberlake is still here.) In biodiversity, a good example is that greater amounts of genetic diversity in the present will allow more rapid and flexible evolutionary change in the future, which will aid population persistence (evolutionary rescue!).

Having just closed out two days of discussion, we now have to write this report – but how to do so? Should we write a nice glossy document that we hand out to policy makers and publish online, or should we edit a special issue of a journal, such as Evolutionary Applications. Either approach seems fine to me but I think that whichever route we go, we should put One Direction on the cover. Doing so would be certain to reach more people – and what better way to influence policy makers than by first convincing their daughters that genetic diversity is the way to go. By virtue of One Direction and N’Sync and The Backstreet Boys and even the Jackson Five, they are already primed to accept it.

Darwin Day - Rap Tribute by Baba Brinkman

Baba Brinkman strikes again - with an awesome rap tribute to Charles Darwin on his birthday. 

Evolution coming undone in Galapagos: human impacts on Darwin's finches

I just returned from a short trip (my tenth) to Galapagos. New experiences during the trip prompted further speculations on a phenomenon we had earlier described: human influences on the adaptive radiation of Darwin’s finches.

An oft-repeated mantra is that remote oceanic islands (never connected to the mainland) are natural laboratories for studying evolution. Part of the reason is that they tend to be simple environments, making it easier to disentangle otherwise overly-complicated ecological and evolutionary relationships. One way in which islands are simple is that they often lack human populations, which contributed to the evolution of strange forms that proved to be utterly unsuited for a life with colonizing humans. As a result, the settlement of remote islands by humans often leads to the extinction of local life forms. However, not all isolated populations go extinct when humans colonize, instead they often evolve to suit the new conditions.

A spectacular male Darwin's finch.

My own foray into island life involves Darwin’s finches in Galapagos. This work obviously follows closely from the insights and work of Peter and Rosemary Grant, and was made possible by an impromptu postdoc I did with Jeff Podos at UMass Amherst. In general, the adaptive radiation of Darwin’s finches is thought to have been driven by specialization of different species on different food types, which has led to reproductive isolation (speciation) through assortative mating by beak size (beaks, songs, and mate preferences are all linked) and natural selection against hybrids (which are poorly suited for either parental diet). With respect to this last point, different “adaptive peaks” are thought to exist in the Galapagos as a result of different food types. For example, large-beaked species evolve to use large/hard seeds and small-beaked species evolve to use small/soft seeds but intermediate beak sizes are rare because intermediate seeds are rare. (I just made and posted a video illustrating this phenomenon.) Darwin’s finches thus diverge onto different adaptive peaks and the few hybrids they produce have intermediate beaks that lack appropriate intermediate seeds on which to feed, and therefore suffer low survival – thus keeping the two species separate.

Yum - a native food!

Our contribution to this story has been the study of two beak size morphs within a single species (the medium ground finch, Geospiza fortis) on the island of Santa Cruz. We (originally Jeff Podos, Sarah Huber, Luis De Leon, Antony Herrell, and myself) have shown that these large and small G. fortis morphs at one site (El Garrapatero) have a bimodal beak size distribution (many large and many small individuals with relatively few intermediates), have different diets, manifest different feeding performances (bite force), sing different songs, show different responses to songs, mate assortatively (large females with large males and small females with small males), experience disruptive selection (intermediate birds have lower survival), and show limited gene flow (based on microsatellite DNA). Stated plainly, these two morphs seem to be part of the way to becoming separate species, presumably through the same mechanisms as those that drove the radiation as whole.

The two El Garrapatero G. fortis morphs.

All of the above effects were demonstrated at a site (El Garrapatero) that is removed from any human settlements and therefore experiences little direct human influence (although indirect influences from introduced species are present). What happens when these two morphs – on their way to potentially become separate species – contact a growing human population? We were able to explore this question in a paper published in PRSB in 2006 by obtaining long term records (1964-2005) of G. fortis beak sizes from Academy Bay, a site immediately adjacent to the rapidly growing town of Puerto Ayora on Santa Cruz Island. This analysis was made possible through data collected by David Snow in 1963-1964, Hugh Ford in 1968 (data was being collected for me as I was being born!!!), the Grants and their colleagues (1970s-1980s), and our own samples (2004 and onward). Analysis of these data showed that the beak size bimodality currently seen in G. fortis at El Garrapatero was also present at Academy Bay in the 1960s but not thereafter. The two morphs at Academy Bay thus seemed to have fused together into a single hyper-variable population in concert with the dramatic increase in human population density at that site.

That is not a native food!

We proposed in the 2006 paper that fusion of the two G. fortis morphs at Academy Bay was the result of humans introducing food types that were accessible by finches of all beak sizes, thus turning the separate adaptive peaks into a long adaptive ridge spanning different beak sizes. On such a ridge, selection against intermediate birds should disappear and their increasing abundance should eliminate the bimodality. We provided support for this hypothesis in a paper in Evolution in 2011 that showed how the naturally strong (confirmed at El Garrapatero) associations between diets, beak sizes, bite forces, and gene flow that presumably drive finch diversification had all become weaker at Academy Bay. In short, humans were causing “reverse speciation” or “despeciation” by turning a formerly rugged adaptive landscape with distinct fitness peaks into a broad ridge without the gaps (fitness valleys) necessary to maintain species distinctiveness.

Our 2011 paper.

This finding was where we left the story until recently. This year, we (spurred mainly by Luis) took up the problem again by making more extensive surveys in the town of Puerto Ayora to see how many finches were using human resources. Various teams of researchers and Earth Watch volunteers would walk through town in the mornings counting birds and determining what they were feeding on. Although I was already suspect the outcome, I was still rather shocked by how many finches were present in the town (more than in nature) and their incredible use of human foods – although they still found natural foods in vacant lots and gardens. I saw finches eating waffles, chips, plantains, rice, corn, fruit, ice cream cones, and many other items. I thereby gained a personal confirmation of our original intuition that finches in Puerto Ayora (Academy Bay) had access to many food types that were usable by finches of any beak size. Then came the real kicker – at El Garrapatero.

Dozens of finches of many species eating rice.

We have been work at El Garrapatero for 12 years now. During that time, the site has transitioned from a difficult-to-access and rarely used site to a very popular destination for locals and tourists. The road has been paved and extended closer to the beach, the path to the beach has been cobbled, buses and taxis roar up and down the road, and gaggles of kids and adults play on the beach. My first hint of possible impacts was the appearance of non-native fruits (passion fruit) along the roadside. I was willing to accept that this would not have a major influence on finch evolution until recently. In 2012, we filmed Galapagos 3D IMAX – narrated by David Attenborough (no I didn’t meet him – but it was cool to hear him say my name on air) – at El Garrapatero. The film crew felt that our normal site, which was away from the beach, was not very picturesque – so they asked us to set up our nets at the beach itself. I was initially skeptical because we had never netted therefore and I couldn’t be sure we could get finches. However, we quickly caught lots of finches – they even seemed more abundant than at our normal site several hundred meters inland. And they seemed attracted to us. At one point, we were waiting to film something and noticed about 20 finches that landed right beside our banding station. We pointed this out to the film crew and they quickly swung their camera boom to film the finches at close range – this became the scene that opens the finch sequence in the film. We also saw several finches attacking the food we had brought for lunch. I was intrigued by this from a filming perspective but didn’t dwell on it much from the perspective of evolution. This year, however, my opinion changed.

Team Pinzones IMAX 3D (Photo by Aspen Hendry)

A few days ago, we walked with the Earth Watch volunteers down to the beach and came across a place where finches were everywhere. We sat down and they swarmed us. Jeff would crinkle a chip bag and they would come running. Then Luis would do the same in a different place and they would run over to him, jumping up on his bag and even into his hand in hopes of getting free handouts. Nearby, other finches of several species were fighting over some plantains someone had left out. It seems that the beach is now an accepted place to feed the finches. This got me to thinking that the direct human influence at El Garrapatero is increasing dramatically and that we might – in the near future – see impacts on the finch bimodality. In particular, we documented disruptive selection (selection against intermediate beak sized birds) in 2004-2006 before all these human changes were so dramatic. My prediction is that selection now will be less disruptive– and perhaps even less so in the future as human use of the site continues to expand.

An El Garrapatero G. fortis enjoys a cracker - when it shouldn't. 

Evolution is coming undone in Galapagos. Human influences are pervasive in some places and they are expanding to new places. This is exciting as a scientist because we can now test evolutionary hypotheses using whole-ecosystem “experiments” – we can add humans and see how evolution changes. But it is depressing as a nature lover because a unique set of island life might well change dramatically. Finches will still be present, of course, but they might no longer be so diverse – at least not in sites where human influences are strong. Fortunately the government limits those impacts to restricted sites, leaving much of the archipelago free of direct human impacts (indirect effects can remain strong). This policy is reassuring because it would be a travesty if unique forms such as the “vampire finch” on Wolf Island were to disappear.

I will report back in another decade or so.

We were even besieged by finches during our breakfast (and they ate our chocolate bread, damn it).

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Thanks to our 2014 team so far: Diana Sharpe, Jaime Chaves, Kiyoko Gotanda, Joost Raeymaekers, Luis De Leon, Sofia Carvajal, Jeff Podos, and 16 Earth Watch volunteers.

Pictures and videos: 

• Galapagos 2014 videos: finches, marine iguanas, Sally Lightfoot crabs, lava lizard.

• Galapagos 2014 images on FLICKR

• All my past Galapagos images on FLICKR

Related posts: 

• My earlier post about the IMAX 3D filming of our research: Team Pinzones IMAX 3D.

• Kiyoko's blog from this year's Earth Watch expedition.

• A finch post from earlier this year: The Living Dead: Darwin's finches and Museums

Some earlier Galapagos posts on this blog:

• More Galapágos Adventure

• The distant baseline

• Blood sucking maggots

• Suskewiet: finchy parallelisms

Human influences on sea lion evolution?

Carnival of Evolution #68

Carnival of Evolution #68 is out now.  Check it out for all sorts of evolution-y goodness.  We didn't have any guest posts last month (Zach and Patrik's post arrived after the deadline and will be a contender for next month's Carnival), so our entry for this Carnival is Andrew's recent post on climate change and evolution, which was about a new Special Issue in Evolutionary Applications.

Since the theme of this Carnival is different spatial scales, here's the old Powers of 10 video, which is still pretty cool even after all these years.