Functional extinction of birds drives rapid evolutionary changes in seed size

Galetti et al. Science 340(6136): 1086-1090. DOI:0.1126/science.1233774. Functional extinction of birds drives rapid evolutionary changes in seed size

Birds only disperse what they can carry! From Galetti et al.

Birds only disperse what they can carry! From Galetti et al.

Will Pearse

Will Pearse

Wam-bam, this is a paper I would have loved to put in my undergrad essays. Plants need birds to disperse their seeds, and so when large birds go locally-extinct, plants evolve smaller seeds that smaller birds can carry. This happens really, really fast (within the last 75/100 years!) and so is a great example of rapid evolution.

A nastier man than I would point out that this is somewhat inferred; with no data on what seed size was like 100 years ago there’s a fair bit of supposition going on here. However, their variance decomposition (34% due to birds in forest, 0.1% differences among sites) is really quite striking, so I’m quite happy to go along with this. There’s such a clear link between seed size and probability of being dispersed (figure 2b) that I’m quite happy to accept the smoking gun of a huge selective pressure and observable differences.

Which leaves me with a slight problem, because I always assume that we can ignore both intraspecific variation and rapid evolution when doing ecosystem service work. If trait can evolve this rapidly, treating species’ ecosystem services and traits as fixed is no longer acceptable. Indeed, the situation is doubly problematic because there are going to be a lot of downstream effects of changing seed size, not just on the plant species itself (it’s now shifted on the simplified on the r vs. k selection spectrum), but also other species that interact with that plant. There is a huge literature on how phenology shifts are worse in tri-trophic interaction networks because not every component of the system can keep up with change – I see no reason for this not to be a concern here.

Lynsey McInnes

Lynsey McInnes

This is to all intents and purposes a very neat demonstration of purported rapid evolutionary change in the face of a new selective pressure brough about by human-mediated loss of large-gaped frugivores from forest fragments. One could quibble on whether the frugivore loss is driving the contraction in seed size variation, or whether fragmentation caused the frugivore loss, and so on, but the authors do a thorough job of dismissing other possible correlates….environmental differences among sites, checking the time needed for such a response, and I’m pretty convinced the relationship holds.

This is bad news! It suggests many of those stacks of papers predicting responses to climate change or habitat fragmentation that brush evolutionary responses under the carpet are probably missing key elements of the response game, Similarly, how does this two trophic level result cascade to additional trophic levels. Without big palm seeds and thus big healthy palms, what grows in their place? What effect do these newly dominant plant species have on other pieces of the forest ecosystem.  Ah, its frightening.

What is the next step? Can we rejoin the forest fragments and get the large-gaped frugivores back? Is there enough genetic variation left to get back the large seeds?

This must have been a time-consuming study and its just not feasible to initiate tons of new studies at similar scales to ascertain how pervasive such rapid evolutionary responses are. I would naively guess that it might be better to continue with this system and see if we can work out this change’s effect on additional chunks of the forest ecosystem. Perhaps the authors are already working in that.

The macroecologist in me also ponders the feasibility and merits of expanding the scope of such studies. Perhaps to a mesoscale at least. I am reminded of Phillimore et al‘s very slick mesoscale studies on variation in phenological responses across space in British frogs. Here, the authors were looking to distinguish local adaptation vs. plasticity governing the spatial variation that they saw in order to predict how populations would cope in the face of climate change that will alter the timing of temperature cues. In short, the authors conclude climate change is expected to outpace the frogs’ ability to respond. However, they ignored the potential for microevolutionary change, as the timescales they were thinking of were so short. The challenge now seems to be to incorporate this possible response? Admittedly, easier said than done…


Developmental trait evolution in Trilobites

Fusco et al. Evolution 66(2): 314-329. DOI:10.1111/j.1558-5646.2011.01447.x. Developmental trait evolution in Trilobites

This is a guest post with Tim Astrop. Below, we give our first impressions of this article. Please comment below, or tweet TimWill or Lynsey (maybe use #pegejc). Think of this as a journal club discussion group!


Figure 1 from Fusco et al. – trilobite moult cycle

Tim Astrop

Tim Astrop

This paper is a wonderful example of how innovative thinking and an integrative approach to the fossil record continues to discover new keys with which to unlock the unknown biological information held within. The Trilobitomorpha is arguably the most diverse and abundant extinct arthropod subphylum, there is certainly no shortage of palaeontological research on these critters, that’s for sure. But despite such popularity and interest in the group we still know very little about them as biological organisms. In this respect it is very apparent that preserved remains are not representative of the living animal, there is much interpretation to be done (see the recent ‘spotted trilobite’ described by McRobets et al 2013).

By looking at different ontogenetic stages represented by the different instars (discrete developmental stage of arthropods ‘bookended’ by ecdysis, or molting) preserved for over 60 species of trilobite for which adequate data is available, the authors then derive new metrics to treat growth rate via average per molt growth increment (AGI) and conformity to Dyers rule (IDC), while the former metric is self explanatory, the latter is less intuitive. The IDC quantifies the fit of observed ontogeny to that of a constant growth rate, deviations from Dyers rule would be indicative of accelerated/decelerated growth at particular ontogenetic stages (readers with a thing for shape analyses may also have noted that allometry would upset this metric via modular differentiation of growth rates within an organism, well done, have a gold star).

What is particularly cool is that the authors use this info not just to look at the evolution of this group but also to shed light on early euarthropod development, as the Trilobitamorpha are basal arthropods. Euarthropod evolution is a very active area of research (see Yang et al 2013 for interesting recent discovery) and held by many as something of a rosetta stone for understanding arthropod origins and diversity.

The meat of this article has a little too much math for than I would normally elect to tackle, but after making it through the results the discussion highlighted the findings really well.

In a nutshell, it seems that trilobites conform to Dyers rule overall, with some smaller deviations occurring in early (protapsid) development. However, the particularly interesting thing, for me at least, is that there appears to be less phenotypic integration in later stages that enables very unique, differing morphologies to evolve that deviate from standard cut-and-paste metamerism (segment repetition) seen in many trilobites (but probably most evident in the familiar Myriapoda) and calls forward to the future of arthropod diversity in all it’s mis-matched-crazy-appendage glory. It also infers that that similar morphologies may be converged upon via different developmental pathways, to me this indicates that trilobite morphology is not restricted to an adaptive peak but provides a method to move between peeks via morphological lability, something the authors refer to as ‘evolutionary dynamism’, a trait that likely contributed to their success as a group.

In summary, I think this article is a wonderful example of how valuable palaeobiological approaches can be to understanding organismal evolution. Here we have a novel approach to an existing dataset using linear measurements (and complex stats) to derive new information about the evolution and biology of an extinct arthropod subphylum.

In my opinion, the true integration of biological and palaeontological principles allows fossils to be treated as the cryptic remains of biological entities that old-school paleontology can often overlook in favour of a ‘stamp-collecting’ mindset. Thankfully there appears to be something of movement among palaeobiologists at the moment back to a more synthesized ‘Simpsonian’ concept of the fossil record. Something I look forward to hearing more about, and to hopefully contribute to!

Will Pearse

Will Pearse

I normally hate people who loudly shout “yay science” on Facebook and the like, but this paper really was one of those moments for me. We can track the development of growing trilobites using fossils? We can robustly test hypotheses about the evolution of that development? Yay science!

The most parsimonious evolutionary model of these species’ traits is one where phylogeny doesn’t matter (a star phylogeny), so it’s hard to argue that there’s any constraint to trait evolution here, despite the phylogenetic signal of some of these traits. The authors suggest this reflects the influence of particular outlier clades that are biasing model fit; I completely agree. I spend much of my time doing analyses of ‘plants’, and it’s always struck me as rather strange that I lump all these diverse and divergent species under one label and then examine their evolution altogether. I imagine the same is true of trilobites – the devil is in the detail, and understanding exactly what clades are varying (and why) will probably give us a better handle on what drives the evolution of these traits.

In passing, I wonder what the consequences of doing morphological analyses on phylogenies of extinct species that have to be built from morphological data. What if some of these traits, or traits that are strongly coupled with these traits, were used to define the phylogeny of these species – after all, ‘ontology recapitulates phylogeny’, and information about how species develop would seem (to a person ignorant of paleontology) like useful data. Could this be why the authors find stronger phylogenetic signal in the earlier developmental stages, or does this actually reflect the biology of the system? Does more evolutionary constrain in juvenile growth suggest juveniles were competing more strongly than adults (mortality does tend to decrease as species get older)? The authors give very detailed supplementary information on the phylogeny’s construction, but I’m really nowhere near qualified to comment. Can anyone help me out?

Lynsey McInnes

Lynsey McInnes

You can’t deny that Will and I like to stretch ourselves in the diversity of papers that we discuss on this site. Who knew the coverage of the terms phylogeny, ecology, geography and evolution was so broad. This week we take another foray into paleo research, this time without the potential to incorporate any extant data, these things are extinct!

My first reading of this paper was definitely made while wearing a cynical hat, and I was unconvinced that the data were adequate to ask these questions, particularly regarding the patched together phylogeny. A bit more time with the paper though, and I was becoming more and more impressed with the authors’ ability to extract conclusions, all appropriately caveated given the antiquity and patchiness of the available data. Perhaps we are all becoming too obsessed with perfect datasets, Bayesianed up and with no room for interpretation based on slotting in genuinely new findings with an already amassed body of research. This paper is a great example of the latter approach. Neat!

I’m most acquainted with adaptive zones in terms of diversity dependent cladogenesis…clades diversify until a zone is full, diversification rate declines until some upstart clade pops off into a new zone to start the process again. Sadly, a lot of contemporary ‘adaptive zone’ research remains a numbers game with little detailed investigation in what adaptations a clade possesses to occupy their zone. In contrast, this paper makes a concerted attempt to actually think about the adaptations necessary to occupy different zones and finds strong evidence for these traits in the Trilobite lineages studied. Impressive given these things went extinct millions of years ago! Not only that but the authors also successfully distinguish between intrinsic and extrinsic drivers of the patterns that they find! I’m a bit obsessed with the landscape or environmental drivers of macroevolutionary patterns and was really pleased to see this angle tackled in this paper.

So, I’m no paleontologist or developmental biologist, and appreciated this paper mostly as it reminded me that science need not be all about the perfect dataset producing good model fit in a standalone clincal model, it can be messy and incomplete, but illuminating.

Convergence, adaptation, and constraint

Jonathan B. Losos. Evolution 65(7): 1827-1840. DOI:10.1111/j.1558-5646.2011.01289.x. Convergence, adaptation, and constraint

Are these Anolis dewdaps constrained? Maybe more than you’d think… (PLoS One; click for source)

Will Pearse

Will Pearse

We’ve covered too many data papers recently (that’s not a joke, but it does read like one), and so I picked this paper to help us step back a little and think. I’m pleased with the result: this is an excellent essay, that really made me think about what convergent evolution actually is. I’m particularly keen to hear what you all think of my comments about history!

Losos argues convergence is scale-dependent: there are many ways to evolve a long beak, and while there may be divergent evolution of the actual genes involved, the resulting phenotype (a long beak) is convergent. We’ve covered convergent evolution in bacteria, where the same genes (but different regions of those genes) mutated in parallel in separate lineages. I like this scale-dependency – it allows us to define convergence so that it’s amenable to study at all levels from phenotype to genetic mechanism.

I think we can push this framework further, and compare very different systems in meaningful ways. For instance, maybe examining constraints to evolution in responses to predation in Daphnia is easier when you consider what constrains their tolerance of the abiotic environment. Maybe seeing particular stressors and evolved responses as analogous to one another allows us to better compare evolution among clades, and view constraints to evolution in a more holistic way..

Apparently, there are some who take the view that evolutionary changes are incomparable historical events, and so the whole idea of convergence is a nonsense. I think this is rather peculiar; while there is a debate in history as to whether the field is a science (I think it is, but I’m not a historian!), every historian I know compares periods and events in history, with the precise aim of drawing parallels among periods. Thus I think the argument that evolution is the study of history, and therefore will not allow us to compare events, is not one even a historian would agree with!

Lynsey McInnes

Lynsey McInnes

Commenting on a Losos paper is always going to be tricky, as this is a man who knows his evolutionary biology! You can tell this in two ways, first simply by the breadth of examples he draws on and second by his daring to question the be all and end all of phylogenetically-informed analyses, another recent examplesof his critique of such analyses can be found here.

Like Will, I appreciated having a week off from data bashing and am currently juggling all the different issues that Losos brings up on what is and is not convergence, parallelism, adaptation, exaptation, etc. The biggest take home message I got from the essay was that, as always, scale matters. Birds and bats both have wings that let them fly, are these convergent traits? Depends on your scale of comparison. It seems like identifying instances of convergent evolution would be simplified immeasurably if the researcher concerned just set out the scale across which he is looking and perhaps also mentions whether he is worried about the trait being the ‘same’ at the genetic, phenotypic, morphological and/or morphological level. Hey presto, confusion and agro could be gotten rid of.

I can’t help comparing the issues brought up here to the ones Losos, and plenty of others, have attempted to deal with concerning identifying instances of niche conservatism. Again, it all depends on scale. Cooper et al. provide an excellent roadmap for conducting analyses on nice conservatism, I’d like to see a companion piece to this essay detailing the practical approaches to sensible analyses of putative instances of convergent evolution.

I’ve recently shifted the scale of my own analyses to incorporate (currently to deal exclusively with) intraspecific variation. In practice, this has meant starting to think about different models of mutation (infinite site, infinite allele, shitty recombination raising its ugly head begging to be dealt with) so I find my scale of analysis shifting to the genetic level, wanting to see mutations in same genes, indeed at the same sites to qualify as parallel evolution. For this reason, I really appreciated this essay as it forced me to address my newfound genetics-only bias and realise that interesting, valid and evolutionarily important convergent changes at the functional (or even just phenotypic) level need not be produced from identical genetic changes.

The recent bacteria study that we discussed here at PEGE was a brilliant example of a standalone set-up for studying evolution across these different levels (genetic, phenotypic, etc.), the next step, as always, is to devise a set-up that facilitates similar inference in systems where access to all these levels might be patchy. Losos’ essay will undoubtedly be helpful in this regard.

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