Evolution

Taste of quals: on the relationship between diversification and key innovations

This is the last post on the series “Taste of Quals” with examples of questions and answers given in the qualifying exams of the Ecology, Evolution and Systematics program at the University of Missouri St Louis. In this post you’ll find another answer written by Robbie Hart (find more about him here and here) in which he explains why, when and how key innovations can be associated to evolutionary diversification. The reason why I love this text and think it’s a great read is that even though this was written back in 2010, and since then the ‘omics’ era has overloaded us with tons of data, we are yet to understand several of the relationships between innovations and diversification that Robbie mentions. Enjoy the read!

Describe the relationship between diversification and key innovations

For half a century, rapid evolutionary diversifications have been conceptually linked to key innovations. Especially in the case of adaptive radiations, features associated with the diverging lineage have been held to have a causal effect in the diversification. However, the generality of this phenomenon has come under criticism from empirical, theoretical, and philosophical standpoints. Recent, careful studies have utilized detailed phylogenies and quantitative comparisons with null models, connected proposed innovations to genetic and developmental mechanisms, and examined replicated cases of radiations, to move the concept of the key innovation beyond “plausible suggestions” (1).

Definitions

In the Simpsonian model of evolution, the essence of diversification is entry into a new adaptive zone, or way of life complete with characteristic adaptive pressures (2). Entry is only possible if three criteria of access are met: physical or geographic access, ecological access (the zone must be empty of competitors), and evolutionary or morphological access. To a large part, Simpson’s definitions have been retained. The first two criteria are now often lumped as ‘ecological opportunity’ (3, 4, 5) in contrast with the final criteria, now often termed a ‘key innovation’. Of the many definitions given for key innovation (Hunter lists seven (6), a small subset), Galis gives one that is in accord with modern ideas of macroevolution: “A key innovation is an innovation which opens up a new character space (or breaks constraints) that potentially allows the occupation of more niches” (7). Key innovations, then, open up adaptive space and expose many characters of an organism to a diverse new suite of selective pressures.

Other definitions accentuate different aspects of key innovations, but there are two that especially contrast with this definition. The first is a definition of key innovations in a phylogenetic context taken to mean any trait responsible for increasing diversification (8). The emphasis is explicitly on tempo rather than mode. Analyses of proposed key innovations differentiate this tempo and various mode definitions more or less (or not at all). The second is the concept of correlated progression, which proposes that coordinated suites of traits are the key features (6). Correlated progression is in clear contrast with the ‘constraint-breaking’ definition of Galis; but not incompatible with the tempo-only definition. At its root, correlated progression is getting at the individuation of key innovations, discussed in more detail below. For now, I’ll say that increasing phylogenetic resolution may ‘smear’ what we think of as one key innovation into several – a concept that has similarities to that of correlated evolution.

Necessary and sufficient conditions for diversification

The biggest potential problem with the concept of key innovations, the idea that they are a necessary and sufficient condition for an adaptive radiation, is easily dispelled. Examples showing the contingency of any causation between key innovations and diversification include the drilling radula in naticid gastropods. The drilling radula is an excellent candidate for a key innovation – it opened the door to many opportunities for specialized predation on shelled bivalves, and was associated with a major diversification of naticid lineages. However, the same feature was found to have evolved previously in the Triassic, and quickly disappeared for the extent of the Jurassic (9). Perhaps the most famous adaptive radiation of all, that of Rift Valley lake cichlids, has been attributed in part to the key innovation of recruiting the pharyngeal jaw for food processing, freeing the oral jaws for diversification (10) – a nice example of a constraint-breaking key innovation. However, Embiotocids also have pharyngeal jaws and Tilapiine cichlids share both structural and behavioral traits with the diverse clades of cichlids, but neither the Embiotocids nor Tilapiine cichlids have undergone a comparable adaptive radation (7).These examples illustrate that key innovations per se are at best necessary but not sufficient to spur diversification. This is the case even when it is combined with a an open niche, as with the Triassic drilling naticids.

Andean lupines, which show record levels of fast speciation and morphological change without identified key innovations or ecological opportunity (3), and plethodontid salamanders, which similarly exhibit an incredible burst of lineage diversification, but without key innovations, particular ecological opportunity, or even significant morphological difference (11), are two examples that bring the necessity of key innovations for rapid diversification into serious doubt. Hunter defends key innovations, however, as important conditions for radiations:
“ ‘environmental challenge’ cannot be sufficient to produce a radiation because, in the absence of [available ecological space ability to use that space via key innovations], any environmental challenge that destroys a species’ habitat is likely to result in extinction not radiation” (12).

All of this raises the question – are adaptive radiations even something that we need key innovations to explain? Are they a “thing” at all? Raup, Gould, Schopf and Simberloff published one of the early null models for phylogenetic diversification, and questioned the notion that there deterministic forces like key innovations significantly structured phylogenetic diversity at a macroevolutionary timescale (13). More recent work is often carefully tested against null models (1, 11, 12) , but criticisms on that basis remain (5), including a recent and suggestive model showing that many of the same phylogenetic patterns interpreted as adaptive radiations could in fact be produced by cryptic mass extinctions (14). Of course, sometimes the comparison with a null model finds no differences pervasive enough to indicate key innovations. This is the case for passerine birds (11), and presumably many more unpublished, as suggested by Donoghue (8)).

Conceptual criticisms: individuation, methodology, diversity patterns

Cracraft (15) offers a comprehensive critique of key innovations, citing them for failing on three themes: ontological (non-individuated ‘innovations’), methodological (failure to trace genetic and developmental mechanisms), and empirical (inappropriate comparisons with clade diversity measures). The first point questions whether a proposed evolutionary novelty is in fact a single character with an individuated identity independent of the observer, or whether it is merely a typological construct. Cracraft offers the example of avian flight, a frequently proposed key innovation that certainly offers access to a new adaptive zone, and a host of structures to differentiate and elaborate. However, flight requires a host of characters, stretching back across 50 million years of evolution to Archaeopteryx or before; it’s hard to argue that this amalgamation is a discrete innovation.

Nevertheless, Bond and Oppel could be doing just that when they write “If a key innovation is defined as the appearance of a new capability that facilitates the proliferation of the lineage that possesses it, then one or more characters may contribute to the key innovation. In the case of character complexes, a key innovation is not functional and therefore not present until all of its components are present. Thus, the key innovation appears at the point in a group’s phylogeny where the last of the functionally linked suite of characters appears” (1). Theirs is more a definitional assertion than an argument. Donoghue has a slightly different take on the issue – working with a tempo definition (Bond and Oppel’s was based on apomorphy) he notes that with increasing phylogenetic resolution many traits that researchers formerly lumped as a key innovation are now best understood as “sequences of character change, no one element of which can cleanly be identified as … responsible for shifting diversification rate”(8). Donoghue, pursuing Cracraft’s methodological theme, notes that this shift in what we think of as a key innovation often leads to surprising developmental features as the first steps towards key innovations – for instance, at the root of the compound feature “macrophyllous leaves” we find overtopping growth.

Photo by Alan Cressler.

Yucca moths in yucca flower. Photo by Alan Cressler.

Pellmyr and Krenn’s work on yucca moths (16) elegantly addresses Cracraft’s methodological theme (as well as the ontological and to some extent the empirical). Building off of a large body of prior research, they identify a unique limb (the yucca moth tentacle); associate it with the adaptive radiation of yucca moths, show that it is integrally related to the mechanism driving that radiation, ie. the pollinating co-evolution with yucca1; convincingly argue for the developmental origin of the tentacle as a heterotopic expression of a proboscis element; hypothesize on a genetic basis for the change; and show that it occurred as an abrupt change at the base of the pollinating yucca moth clade.

Finally, Cracraft’s empirical theme explores the difficulty in connecting an evolutionary novelty causally with patterns of species diversity, including problems of: assuming that higher taxa are comparable, making an arbitrary choice of a certain rank of taxa to compare, ignoring counterexamples, correlating a proposed key innovation and number of species, and qualifying clades as “diverse” or “not diverse” rather than quantifying diversity. This final theme has its roots in the very nature of key innovations. They are novelties, unique or at least rare, and this makes it extremely difficult to test causation. “Suppose that we agree wings are a key adaptation of bats. How can we show that they are responsible for there being ca. 870 species as against, say, 87 or 8,700?” (Raikow 1988 qtd in (10)). Cracraft specifically criticizes the comparative- functional argument as based on a correlation driven by an arbitrary choice of taxonomic or phylogenetic level of comparison. This is an issue that shares some conceptual similarity to the concern about null models. Bond and Opell (1) attempt to address the empirical theme by identifying unbalanced bifurcations in a semiautomated, a priori way across a well-resolved tree of all spiders, and only then locating the functional innovations at the nodes that emerge as exceptional; however their basic procedure remains qualitatively what Cracraft criticizes: “to qualify as a key innovation, our analysis requires that a feature: (1) be a synapomorphy; (2) be functionally advantageous; and (3) be capable of facilitation a change or an expansion of adaptive zone [and be associated with one side of an unbalanced bifurcation].”

Another way to address the empirical theme is through replicated examples of key innovations driving adaptive radiations. Unfortunately, replicated adaptive radiations themselves are few, in part because of the necessary conditions for geographic replicates. Islands and island- like habitats are promising; but candidate ‘archipelagos’ must be small enough to be replicated2 and at the same time large enough to show any speciation at all3. Caribbean anoles (17), Galapagos snails (4, 18), Mesozoic semionotid lake fish (19), and Hawaiian spiders (20) are rare examples; but are not strongly associated with key innovations (although toe pads and dewlaps have both been suggested for anoles (21)). Rift Valley lake cichlids, are one of the few examples of a replicated adaptive radiation with a fairly well-supported key innovation – the pharyngeal jaw (10).

Contingency

Even the classic cichlid example, however, demonstrates the highly contingent nature of the connection between diversification and key innovations. The failure to radiate of closely related groups that share the pharyngeal jaw and other innovations with the species-rich groups of cichlids (7); phylogenetic reconstructions that show sexual selection, habitat selection, and trophic diversification as each driving a separate mini-radiation (10); and the possibility that much of the cichlid speciation may be due to peripatric speciation in geologically ephemeral satellite lakes and multiple colonizations from riverine lineages (19, 22) all emphasize this contingency.

Haplochromis (Pundamilia) nyererei, one of the species that is part of the outstanding species pool of Lake Vitoria, which contains more than 500 cichlid taxa.

Haplochromis (Pundamilia) nyererei, one of the species that is part of the outstanding species pool of Lake Vitoria, which contains more than 500 cichlid taxa.

De Queiroz (23) formalizes this contingency by breaking it into three parts: the effect of other taxa; the effect of other traits; and the effect of the environment. ‘Other taxa’ may be seen as more or less equivalent to Simpson’s ‘ecological access’ – one reason that a key innovation could arise and not lead to adaptive radiation is lack of an empty niche. De Queiroz advances image-forming eyes as a possible example of this contingency; the first three clades (vertebrates, arthropods, and cephalopods) in which this innovation emerged all diversified greatly; but it has subsequently evolved 15 times in various taxa without spurring comparable radiations (23). A less hypothetical example is presented in Hawaiian tertragnathid spiders, where ecomorph niches are present on an island or volcano either through immigration or diversification (20). No ecomorph is represented by two sympatric species, so a niche filled by immigration will presumably not spur radiation.

‘Other traits’ gets at individuation and complexes of traits. Functional modules may constrain evolution of their parts (24); and key innovations may often be, or result from, decoupling features from modules to, in effect, add parameters for diversification – this is seen in a number of key innovations from cichlid jaws (7) to avian flight musculature (6). At the same time; features that have a proximal connection to fitness (eg. macrophyllous leaves) may spring from from distal innovations (eg. overtopping growth) (8). Some distal innovations (baupläne) may offer much better ways of ‘solving’ evolutionary ‘problems’ than others – Donoghue gives the example of repeated convergence on ‘tree’ life forms in plants that seem to have not spurred radiations or been particularly efficient until it occurred in lineages with bifacial cambium.

Finally, ‘environment’ is clearly a key contingency; and is often associated with other biogeographic factors that may swamp patterns of adaptive radiation driven by key innovations; through patterns produced by other mechanisms of speciation (as in the possible peripatric speciation of cichlids) (22); ‘tier II’ or ‘tier III’ historical phenomena such as species selection and mass extinction (perhaps responsible for the disappearance of the Tertiary drilling naticids (9)); or environmental changes such as global CO2 change (which affects the ‘keyness’ of the C4 innovation (23)) and climatic cycles (which drove repeated local mass extinctions of radiating semionotid lake fish (19)).

The relationship between diversification and key innovations could, perhaps, be summed up in one word: ‘contingent’. I’m inclined to think of this a more of a ‘profound insight’ than a ‘truism’ (23); and agree with the forecasts of de Queiroz (23), Donoghue (8), and Losos (4); that a careful study of how key innovations can drive diversification is rich ground for evolutionary insight, even lacking a strict deterministic framework.

Footnotes

1 The related Raven-Ehrlich hypothesis of key antagonistic/defensive coevolutionary synchronization driving adaptive radiation through escalation has received somewhat equivocal support (25, 26).

2 Continent-scale comparisons are of course limited in number.

3 One of the most intriguing patterns to emerge from studies of island speciation is a threshold island area, below which no inferred speciation events are seen (18).

Works cited

1. Bond JE, Opell BD (1998) Testing Adaptive Radiation and Key Innovation Hypotheses in Spiders. Evolution 52:403.

2. Simpson G (1953) Major Features of Evolution (Columbia University Press, New York).

3. Hughes C, Eastwood R (2006) Island radiation on a continental scale: exceptional rates of plant diversification after uplift of the Andes. Proceedings of the National Academy of Sciences of the United States of America 103:10334-9.

4. Losos JB (2010) Adaptive Radiation, Ecological Opportunity, and Evolutionary Determinism. The American naturalist 175.

5. Masters J, Rayner R (1998) Key innovations? Trends in Ecology & Evolution 13:281.

6. Hunter JP (1998) Key innovations and the ecology of macroevolution. Trends in Ecology and Evolution 13:31-36.

7. Galis F (2001) in Character Concept of Evolutionary Biology, Wagner GP, pp. 581-605.

8. Donoghue MJ (2005) Key innovations, convergence, and success: macroevolutionary lessons from plant phylogeny. Paleobiology 31:77-93.

9. Fürsich FT, Jablonski D (1984) Late Triassic Naticid Drillholes: Carnivorous gastropods gain a major adaptation but fail to radiate. Science 224:78-80.

10. Danley PD, Kocher TD (2001) Speciation in rapidly diverging systems: lessons from Lake Malawi. Molecular ecology 10:1075-86.

11. Kozak KH, Weisrock DW, Larson A (2006) Rapid lineage accumulation in a non- adaptive radiation: phylogenetic analysis of diversification rates in eastern North American woodland salamanders (Plethodontidae: Plethodon). Philosophical transactions of the Royal Society of London. Series B, Biological sciences 273:539-46.

12.  Ricklefs RE (2003) Global diversification rates of passerine birds. Proceedings. Biological sciences / The Royal Society 270:2285-91.

13. Raup DM, Gould SJ, Schopf TJ, Simberloff DS (1973) Stochastic models of phylogeny and the evolution of diversity. Journal of Geology 81:525-542.

14. Crisp MD, Cook LG (2009) Explosive radiation or cryptic mass extinction? Interpreting signatures in molecular phylogenies. Evolution 63:2257-65.

15. Cracraft J (1990) in Evolutionary Innovations, Nitecki MH, pp. 21-44.

16. Pellmyr O, Krenn HW (2002) Origin of a complex key Innovation in an Obligate Insect-Plant Mutualism. Science 99:5498-5502.

17. Losos JB (1998) Contingency and Determinism in Replicated Adaptive Radiations of Island Lizards. Science 279:2115-2118.

18. Losos JB, Parent CE (2010) in The Theory of Island Biogeography Revisited, Ricklefs RE, Losos JB (Princeton University Press, Princeton), pp. 416-438.

19.  McCune AR, Thomson KS, Olsen PE (1984) in Evolution of Fish Species Flocks, Echelle A, Kornfield I, pp. 27-44.

20. Gillespie R (2004) Community Assembly Through Adaptive Radiation in Hawaiian Spiders. Science 303:356-359.

21. Jackman T, Losos JB, Larson A, de Queiroz K (2000) in Molecular Evolution and Adaptive Radiation, Givnish TJ, Sytsma KJ (Cambridge University Press), pp. 535-557.

22. Genner MJ et al. (2007) Evolution of a cichlid fish in a Lake Malawi satellite lake. Philosophical transactions of the Royal Society of London. Series B, Biological sciences 274:2249-57.

23. De Queiroz A (2002) Contingent predictability in evolution: key traits and diversification. Systematic biology 51:917–929.

24. Wagner GP, Pavlicev M, Cheverud JM (2007) The road to modularity. Nature reviews. Genetics 8:921-31.

25. Agrawal AA, Lajeunesse MJ, Fishbein M (2008) Evolution of latex and its constituent defensive chemistry in milkweeds (Asclepias): a phylogenetic test of plant defense escalation. Entomologia Experimentalis et Applicata 128:126-138.

26. Berenbaum MR, Favret C, Schuler MA (1996) On defining “key innovations” in an adaptive radiation: cytochrome p450S and Papilionidae. The American Naturalist 148:S139-S155.

Hope that's you now, after having read all these posts on how to nail your quals!

Hope that’s you now, after having read all these posts on how to nail your quals!

Taste of quals: do phylogenetics and conservation biology walk side by side?

Photo by Letícia Soares.

Robbie Hart writes on the relationships between conservation biology and phylogenetic trees, systematics and species concepts. Photo by Letícia Soares.

Here I am again, with another example of a qualifying exam question, from the Ecology, Evolution and Systematics program of the University of Missouri-St Louis. This time, I’ll post a sample from the quals of Robbie Hart, a PhD candidate (very soon PhD to be) in our program. Robbie’s quals answers were pointed out by a former faculty faculty member as one of the best through out years of evaluating the quals from several student cohorts. When I told Robbie the great things I heard on the quality of his answers, I asked him if I could post a few of them in the blog, and that was his reaction:

Robbie Hart gives us a sample of his own qualifying exam. He is also a pro when it comes to crack nuts. Courtesy of Robbie Hart.

“Awwwww don’t make me blush! That’s certainly a nice complement, though it seems unlikely! Quals was upsetting and difficult for me as it is for everyone…and it involved an early version of dropbox eating one of my answers. […]. I found them [the answers], but can barely understand them now. I think I’ve spent too long in the field. I’ll share with you […] my excessively wordy evolution major and my superficial and incomplete conservation bio minor.”

So here it is, a conservation biology minor question, answered by Robbie Hart. If you want to catch up with this topic on how to prepare yourself for qualifying exams in ecology and evolution, check out our previous posts!

What information in classifications and phylogenies may help – or hinder – efforts in conservation?

To prioritize conservation actions, one must first ask the existential question of conservation biology: ‘what are we trying to conserve when we protect biodiversity?’. One answer to this question is based in utility to humans: the goal is ecosystem services (1), and in an uncertain world, continued diversity conserves ‘option value’ – net benefit of keeping various possibilities open (2). Another is based on evolutionary history – an organismal lineage is seen as taking a certain amount of time to evolve, and a loss of that lineage (extinction) is lost evolutionary time (3,4). Both of these may be seen as preserving distinctive features of organisms; most modern approaches to quantifying biodiversity take genetic diversity as a proxy for a multitude of unknown (and perhaps unknowable) ‘features’ (1,2). Phylogenies and classifications, therefore, are central to setting the units of conservation, as they are both maps of the diversity to be conserved.

Species are historically the units of conservation for the public, scientists and legislators. However, their very importance may make them especially unstable categories – driven by biological evidence, legislative criteria, or the adoption of different species concepts, species number may change drastically, often leading to confusion or changes in prioritization (“taxonomy as destiny”(5), also see (6, 7, 8)). Different species concepts may work better for the different taxonomic goals of listing and management (7), and even the quality of the species level as a uniquely real grouping has been called into question as another just another lump in the continuum (6,9). Infra-specific groupings have fared even less well; they are subject to differing taxonomic cultures across different taxa, and have little relation even to genetic subdivisions of species (10). Higher taxa are also commonly used, and to some advantage: they offer deeper insight into loss of evolutionary history, and they are potentially more stable than specific and infraspecific levels. It could be argued that evolutionary taxa sensu Simpson are to some extent based on features themselves. However, the arbitrary nature of the higher divisions make them less suitable for quantitative, comparative analysis (1,3).

In light of these troubles, other units have been proposed for conservation. Units may be ‘management’, consisting of any population groups differing in allele frequency (1); ‘designatable’, designed with pragmatic policy issues in mind (11); ‘evolutionarily significant’, defined either as historically isolated (12), reciprocally monophyletic (1), or more broadly defined (13); or any of a large set of distinct or partially overlapping terms. As classifications, these terms share an unfortunate dichotomy – a group is either a unit, or not (13).

Phylogenetic diversity methods move beyond this dichotomy and treat distinctness or originality as a continuum. Methods are similarly diverse here, but generally apportion to each organism the amount of tree for which they are responsible. This offers a detailed look at exactly how much phylogenetic history is lost with each species that goes extinct; and is a measure with significant stability to taxonomic revision. This method can be extended in various ways: to probabilistic measures that take into account each sister node’s threat levels (14); or combined with complementarity principles to quantify hotspots of phylogenetic endemism (15, 16).

In the past, taxonomies and classifications have posed hindrances to conservation efforts. Newer phylogenetic diversity methods show great promise in moving past dichotomous categories and quantifying the threat to the shared evolutionary history of organisms. The virtue and immediacy of these are highlighted by studies showing that nonrandom extinction can pose a particularly severe threat to evolutionary history (4, 17).

Works cited

1. Crozier RH (1997) Preserving the information content of species: genetic diversity, phylogeny, and conservation worth. Annual Review of Ecology, Evolution, and Systematics 28:243-268.

2. Faith DP (1994) Phylogenetic pattern and the quantification of organismal biodiversity. Philosophical transactions of the Royal Society of London. Series B, Biological sciences 345:45-58.

3. Avise JC, Johns GC (1999) Proposal for a standardized temporal scheme of biological classification for extant species. Proceedings of the National Academy of Sciences of the United States of America 96:7358-63.

4. Vamosi JC, Wilson JR (2008) Nonrandom extinction leads to elevated loss of angiosperm evolutionary history. Ecology Letters 11:1047-53.

5. May RM (1990) Taxonomy as destiny. Nature 347:129–130.

6. Isaac NJ, Mallet J, Mace GM (2004) Taxonomic inflation: its influence on macro ecology and conservation. Trends in Ecology and Evolution 19:464-9.

7. Mace GM (2004) The role of taxonomy in species conservation. Philosophical transactions of the Royal Society of London. Series B, Biological sciences 359:711-9.

8. Baker RJ, Bradley RD (2006) Speciation in Mammals and the Genetic Species Concept. Journal of mammalogy 87:643-662.

9. Mishler BD (2009) in Contemporary Debates in Philosophy of Biolgoy, Ayala FJ, Arp R (Wiley-Blackwell), pp. 110-122.

10. Zink RM (2004) The role of subspecies in obscuring avian biological diversity and misleading conservation policy. Philosophical transactions of the Royal Society of London. Series B, Biological sciences 271:561-4.

11. Green DM (2005) Designatable Units for Status Assessment of Endangered Species. Conservation Biology 19:1813-1820.

12. Moritz C (2002) Strategies to protect biological diversity and the evolutionary processes that sustain it. Systematic biology 51:238-54.

13. Crandall KA, Bininda-Emonds OR, Mace GM, Wayne RK (2000) Considering evolutionary processes in conservation biology. Trends in Ecology and Evolution 15:290-295.

14. Faith DP (2008) Threatened species and the potential loss of phylogenetic diversity: conservation scenarios based on estimated extinction probabilities and phylogenetic risk analysis. Conservation Biology 22:1461-70.

15. Rosauer D, Laffan SW, Crisp MD, Donnellan SC, Cook LG (2009) Phylogenetic endemism: a new approach for identifying geographical concentrations of evolutionary history. Molecular ecology 18:4061-72.

16. Faith DP, Reid CA, Hunter J (2004) Intergrating Phylogenetic Diversity, Complementarity and Endemism for Conservation Assessment. Conservation Biology 18:255-261.

17. Purvis A (2000) Nonrandom Extinction and the Loss of Evolutionary History. Science 288:328-330.

 

Taste of quals: understanding evolution through quantitative trait loci

This is the second post with examples of questions and answers from qualifying exams given in the graduate program of Ecology, Evolution and Systematics at UMSL. Here is another sample of my own quals, in this case, a question for a minor in Evolution. If you’d like to catch up with this discussion, read the initial post “The ultimate grad student guide to survive (and pass) qualifying exams“, and the first question/answer example on incomplete lineage sorting and species delimitations. I’ll post two more examples in the near future, from the quals of our dear peer, Robbie Hart. Stay tuned!

I remember that during my oral exam, my committee asked me to define epigenetics, which I do define in my text as you’ll see as you read, but I don’t coin the definition. So, here is another advice, make sure you give short and straightforward definitions for all concepts you use.

What are Quantitative Trait Loci and how are they relevant to the study of evolution?

The basic strategy behind mapping quantitative trait loci (QTL) is illustrated here for a | the density of hairs (trichomes) that occur on a plant leaf. Inbred parents that differ in the density of trichomes are crossed to form an F1 population with intermediate trichome density. b | An F1 individual is selfed to form a population of F 2 individuals. c | Each F2 is selfed for six additional generations, ultimately forming several recombinant inbred lines (RILs). Each RIL is homozygous for a section of a parental chromosome. The RILs are scored for several genetic markers, as well as for the trichome density phenotype. In c, the arrow marks a section of chromosome that derives from the parent with low trichome density. The leaves of all individuals that have inherited that section of chromosome from the parent with low trichome density also have low trichome density, indicating that this chromosomal region probably contains a QTL for this trait. Figure and legend taken from Mauricion 2001, Nature Genetics

The basic strategy behind mapping quantitative trait loci (QTL) is illustrated here for a | the density of hairs (trichomes) that occur on a plant leaf. Inbred parents that differ in the density of trichomes are crossed to form an F1 population with intermediate trichome density. b | An F1 individual is selfed to form a population of F 2 individuals. c | Each F2 is selfed for six additional generations, ultimately forming several recombinant inbred lines (RILs). Each RIL is homozygous for a section of a parental chromosome. The RILs are scored for several genetic markers, as well as for the trichome density phenotype. In c, the arrow marks a section of chromosome that derives from the parent with low trichome density. The leaves of all individuals that have inherited that section of chromosome from the parent with low trichome density also have low trichome density, indicating that this chromosomal region probably contains a QTL for this trait. Figure and legend taken from Mauricion 2001, Nature Genetics

Phenotype is the assemblage of observable characteristics, or traits, manifested by one individual as a result of the interaction between genes and the environment. Quantitative traits are phenotypic characteristics mediated by more than one gene (i.e. present polygenic control) (Erickson et al. 2004). Quantitative trait loci (QTL) are the several gene loci determining the expression of quantitative traits (Avise 2004). For instance, five QTLs determine morphological variation of male genitalia in Drosophila montana (Schafer et al. 2011), more than 800 QTLs are responsible the variation of 35 distinct traits in tomato, Solanum lycopersicum (Semel 2006), and few QTLs were described regulating the foraging choices in honey bees (Rüppell et al. 2004). The genetic base of ecologically and evolutionarily relevant traits has been described with QTL analysis. Evolution operates through heritable phenotypic variation, driving adaptation and diversity (Mauricio 2001). Describing QTLs supports the genetic background for understanding what determines phenotypic variation of quantitative traits, and how such variation is selected and fixed in populations (Erickson et al. 2004).

QTLs provide insights on the genetic mechanisms regulating phenotypic patterns, such as dominance, pleiotropism, epistasis or environmental interactions (Erickson et al. 2004, Avise 2004). Hybrids of S. lycopersicum with elevated reproductive fitness presented more overdominant (ODO) QTLs (Semel 2006). It seems that ODO QTLs (i.e. loci presenting heterozygous alleles with dominant expression over all homozygous alleles) were the genetic mechanism causing hybrids of Solanum sp. to present heterosis, a phenomenon in which hybrids outperform the most fit inbred parental lineage (Semel 2006). QTLs are also involved in pleiotropism, when a locus mediates the expression of multiple traits, and epistasis, when one locus suppresses the expression of alleles in a different locus (in an analogous way of dominance) (Phillips 1998). More than 60% of the phenotypic variation of body weight and fat accumulation in mice can be explained by QTLs in pleiotropy or epistasis (Brockmann et al. 2000). Moreover, the interaction of QTLs with environmental conditions explains phenotypic plasticity (i.e. habitat-dependent adaptive phenotype) in both barley and aphid populations (Tétard-Jones et al. 2011).

The basic procedure for QTL mapping in plants and animals is: 1) selection of two parental lineages that differ in the allele affecting a common trait; 2) generation of an F1 population by mating parents; 3) parental alleles are shuffled by creating a mapping population (F2); 4) traits are quantified and multilocus genotypes are identified (Mauricio 2001). Erickson et al. (2004) define three difficulties in identifying QTLs: 1) the genetic markers employed; 2) how the crosses of lineages are designed and 3) the magnitude of the QTL effect. For instance, if genetic markers are dominant, it will be harder to tell apart the effects of homozygotes dominants and heterozygotes. Random crossing of parental lineages might bias QTL identification towards alleles with large effects, but rare in natural populations (Pérez-Pérez et al. 2010). QTL identification is also biased towards the magnitude of its effect (i.e. genetic variance explained by the QTL) (Erickson et al. 2004); which is an issue in the presence of confounding factors, such as genotype-environment interactions, low heritability and imprecise estimation of genotypes and phenotypes (Erickson et al. 2004). One can overcome these problems by applying large sample sizes, adequate type and number of genetic markers, and carefully designed crosses. However, the current genomic era, with increasing number of whole sequenced genomes, overwhelms such problems by providing more markers, refining genetic maps and improving crosses due to reduction in genotyping costs (Mauricio 2001). QTL analysis detects and describes the regions of the genome responsible for the phenotypic variation under selection, shedding light on the mechanisms of evolution of complex traits.

References

Avise, J. 2004. Molecular markers, natural history, and evolution. 2nd edition. Sinauer Associates, Sunderland. 684 pp.

Brockmann, G. A., J. Kratzsch, C. S. Haley, U. Renne, M. Schwerin, and S. Karle. 2000. Single QTL Effects, Epistasis, and Pleiotropy Account for Two-thirds of the Phenotypic F2 Variance of Growth and Obesity in DU6i x DBA/2 Mice. Genome Research:1941–1957.

Erickson, D. L., C. B. Fenster, H. K. Stenøien, and D. Price. 2004. Quantitative trait locus analyses and the study of evolutionary process. Molecular Ecology 13:2505–2522.

Mauricio, R. 2001. Mapping quantitative trait loci in plants: uses and caveats for evolutionary biology. Nature Reviews Genetics 2:370–381.

Pérez-Pérez, J. M., D. Esteve-Bruna, and J. L. Micol. 2010. QTL analysis of leaf architecture. Journal of Plant Research 123:15–23.

Phillips, P. C. 1998. The language of gene interaction. Genetics 149:1167–1171.

Rüppell, O., T. Pankiw, and R. E. Page. 2004. Pleiotropy, epistasis and new QTL: the genetic architecture of honey bee foraging behavior. The Journal of Heredity 95:481–491.

Schäfer, M. A., J. Routtu, J. Vieira, A. Hoikkala, M. G. Ritchie, And C. Schlötterer. 2011. Multiple quantitative trait loci influence intra-specific variation in genital morphology between phylogenetically distinct lines of Drosophila montana. Journal of Evolutionary Biology 24:1879–1886.

Semel, Y. 2006. Overdominant quantitative trait loci for yield and fitness in tomato. Proceedings of the National Academy of Sciences 103:12981–12986.

Tétard-Jones, C., M. A. Kertesz, and R. F. Preziosi. 2011. Quantitative trait loci mapping of phenotypic plasticity and genotype-environment interactions in plant and insect performance. Philosophical transactions of the Royal Society of London. Series B, Biological Sciences 366:1368–1379.

Mastering scariness: the mechanisms behind hooding and growling in cobras

Snake charming is a very popular and ancient performance in Africa and Asia, which takes advantage of the natural defensive behavior of cobras of forming a hood.

Snake charming is a very popular and ancient performance found in Africa and Asia, in which flute players takes advantage of the natural defensive behavior of cobras of forming a hood. Picture from: http://cdn.fansided.com/wp-content/blogs.dir/75/files/2013/07/snake-charmer.jpg

The second Ultimate Vert Bio Challenge is a warm up for Halloween, about one of the most terrifying, albeit amazing, creatures in nature: Cobras! These reptiles found their place in the animal kingdom hall of fame due to snake charming, a very ancient and popular performance in African and Asian countries,  in which a flute player pretends to hypnotize a cobra. What snake charmers actually do is take advantage of the defensive behavior called hooding, which cobras naturally perform by standing vertically, flaring the neck laterally and compressing it dorsoventrally. But, precisely, what adaptations in the skeleton and musculature of the cobras allow them to perform such a scarring defensive hooding display? When comparing X-rays of king cobras displaying hooding to cobras in a relaxed state, one is able to see how, in order to flare the hood, these snakes can rotate the ribs in two planes, frontal and transverse. The rotating movement of the ribs allow these bones to protract (move towards the head), and elevate (flatten and move dorsally), anchoring the muscles associated to the hood. Rib rotation is initiated by contraction of two muscles in the head, followed by contraction of intercostal muscles to support the protracted and elevated ribs. How long cobras can keep up with the defensive display depends on the amount of visual stimuli, or how threatened they feel, as well as intra- and inter- specific variation. However, there is evidence from laboratory observations that they are able to maintain the hood flared for at least 10 min, and up to 80 min!

Young BA, Kardong KV. 2010. The functional morphology of hooding in cobras.J Exp Biol. 213, 1521-8.

Young BA, Kardong KV. 2010. The functional morphology of hooding in cobras.J Exp Biol. 213, 1521-8.

I wouldn't hold a king cobra for a million dollars...wait, maybe for that money I would..but I definitely wouldn't smile while doing it like this guy does.  Picture from: http-//static.panoramio.com/photos/large/100885070.jpg

I wouldn’t hold a king cobra for a million dollars…wait, maybe for that money I would..but I definitely wouldn’t smile while doing it like this guy does. Picture from: http-//static.panoramio.com/photos/large/100885070.jpg

If you think hooding is enough to make cobras one of the most frightful creatures out there, you probably haven’t seen a video of a cobra hooding and growling at the same time. Yes, growling. Super laud nasty scary growling. Check out the video bellow:

Most snakes are able to produce hissing-like vocalizations at a frequency of 7,500 Hz, whereas cobras’ vocalizations lie at much lower frequencies, around 700 Hz, which is what characterizes them as growlers. The production of low frequency sound is possible due to the presence of a structure called tracheal diverticula. These are sacs associated to the trachea, which work as low frequency resonating chambers for the air flushed down the respiratory passageway. Interestingly, the only snake that has tracheal diverticula and is also able to growl, is the cobra’s favorite snack, the mangrove rat snake. This is considered to be a case of vocal Batesian mimicry, in which the mangrove rat snake mimics the vocalization of the more threatening cobras. The venom of mangrove rat snake is not toxic to humans, whereas cobras can inject up to 7 ml of venom in a single bite, and can kill a person in less than half an hour. We’re aware that cobras are predated by honey badgers (because they just don’t care), but I wonder what was the actual evolutive pressure through time to select for such a nasty defensive apparatus! Any thoughts?

Just to prove that King cobras can also look cute! Picture from: http://www.snaketype.com/wp-content/uploads/king_cobra_200-623x200.jpg

Just to prove that King cobras can also look cute! Picture from: http://www.snaketype.com/wp-content/uploads/king_cobra_200-623×200.jpg

 

Herpes viruses got a friend: Helminth parasites can promote the reactivation of latent viral infections

In a fascinating story about co-infections and co-evolution, helminth parasites play a role in a two-signal reactivation pathway of latent infections of herpes-like viruses. 

The helminth Heligmosomoides polygyrus can re-activate latent herpes viruses through the modulation of transcriptior factors and inhibition of anti-viral cytokines. Photograph by Constance Finney.

The helminth Heligmosomoides polygyrus can re-activate latent herpes viruses through the modulation of transcriptor factors and inhibition of anti-viral cytokines. Photograph by Constance Finney.

We all know at least one person who has exhibited the signs of an infection by herpes viruses, as well as their complaints about how this inconvenient infection might re-occur after long dormant periods. In fact, more than 90% of the human population is accounted to latently carry viruses of the herpes family. Although most research on disease mechanisms and host immunity have focused on one-host-one-parasite systems, most vertebrates are known to carry a vast community of parasites, that can behave much like herpes viruses do, alternating between latent and active phases. There is evidence that parasites can interact when in co-infection, however little is known about the precise mechanisms through which these organisms deal with each other when exploring a common host.

In a study published this month in the Science magazine, researchers investigate how helminth parasites influence the end of the latency stages of herpes viruses in murine rodents. The researchers experimentally infect rodents with a herpes-like virus modified to express luciferase – a bioluminescent enzyme that can be used to track the viral replication inside the host. Then, they challenged the same rodents with infections of two different types of helminths, Heligmosomoides polygyrus and Schistosomiasis mansoni, and found out that both parasites promote viral reactivation. Interestingly, the helminths elicit viral ‘awakening’ through a cascade of cell-mediate immunity that starts with the activation of lymphocytes Th2. Once activated by helmintic infections, Th2 cells produce IL-4, which is the crucial factor on the re-activation of herpes viruses. The exit from the latency state is dependent on the expression of one viral gene (gene50), and such expression relies on the bond of a single signaling molecule to gene50. The misfortune of the host and the beauty of co-evolution come from the fact that IL-4, which synthesis is a product of the helminth presence, is the the activator of this one signaling molecule that promotes the expression of the gene necessary for the ‘awakening’ of the herpes virus. Also, IL-4 not only promotes viral gene expression, but also blocks the activity of anti-viral cytokines. Hence, the viruses only exit the latent state when the host immune system provides an ideal medium for their proliferation, by both stimulating viral re-activation and inhibiting anti-viral immunity – all thanks to helminths parasites. What a fine example of co-evolution and organismal adaptation! 

How helminths go viral: Helminth infection activates TH2 cells to release IL-4 and IL-13, both of which ligate the IL-4 receptor (IL-4R) on M2 macrophages. In M2 macrophages harboring latent herpesvirus, the IL-4R activates host cell STAT6, which then acts directly on the key viral gene that initiates viral replication. Figure and caption adapted from Maizels and Gause 2014.

How helminths go viral: Helminth infection activates TH2 cells to release IL-4 and IL-13, both of which ligate the IL-4 receptor (IL-4R) on M2 macrophages. In M2 macrophages harboring latent herpesvirus, the IL-4R activates host cell STAT6, which then acts directly on the key viral gene that initiates viral replication. Figure and caption adapted from Maizels and Gause 2014.

Reese et al, 2014. Helminth infection reactivates latent γ-herpesvirus via cytokine competition at a viral promoter. Science Vol. 345 no. 6196 pp. 573-577.

Darwin’s finches “reversing” their famous process of speciation

In a paper published this week on the American Naturalist, Kleindorfer et al. report on how one of the subgroups of Darwin’s finches, the insectivorous tree finches, are collapsing back via hybridization, and also suggest the extinction of the large tree finch, Camarhynchus psittacula.

The Darwin finches are some of the most iconic examples of adaptive evolutionary radiation, and consequently, speciation. There are some curious facts about the history behind Darwin’s finches that I think are interesting to share. History that which obviously involves our beloved blog namesake, Mr. Darwin.

Darwin finches, from Wikipedia.

Darwin finches, from Wikipedia.

Charles Darwin was known for his likings of hunting and avidity in collecting, and perhaps for that reason I always pictured Darwin happily shooting all kinds of finches in Galapagos and instantly recognizing how that was a major find, and making all the intricate connections between adaptive morphology and speciation. However, it was another shipmate of the Beagle, Syms Covington, who did most of the bird collections in Galapagos.

As with almost all breakthroughs, the “eureka” moment of this famous Darwin episode was an afterthought. Darwin didn’t even discuss the finches in the diary of his voyage on the Beagle at much length. At the time, Darwin thought those were blackbirds and gross-beaks. Only after being back in England is when the famous ornithologist John Gould identified those Galapagos birds as “a series of ground finches which are so peculiar [as to form] an entirely new group, containing 12 species.” After Gould had made his findings public is when Darwin associated their incredible morphological adaptation to the species divergence concept, when he noted that “seeing this gradation and diversity of structure in one small, intimately related group of birds, one might really fancy that from an original paucity of birds in this archipelago, one species had been taken and modified for different ends”. Also interesting is that, nowadays, we know Darwin’s finches diverged from a group of Tiaris birds, which originated in the Caribbean islands and then spread to Central and South America, and finally to the Galapagos.

Now, to add to their glorified fame as teachers of the workings of evolution, Darwin’s finches are showing us a snapshot of the reverse process. The paper of Kleindorfer et al – just hot off the presses on the American Naturalist (Feb. 24th) –  looked at the three Camarhyncus species, known as tree finches, in one of the Galapagos islands, Floreana, to test the mechanisms and functions of annual patterns of hybridization in these sympatric species.

Images of three sympatric tree finches from Floreana Island in 2010. A, genetic population 1; B, hybrid tree finch; and C, genetic population 2. From Kleindorfer et al (2014).

Images of three sympatric tree finches from Floreana Island in 2010. A, genetic population 1; B, hybrid tree finch; and C, genetic population 2. From Kleindorfer et al (2014).

“The three Camarhyncus species on Floreana Island are of special interest because Lack (1947) singled them out as a paradigmatic example of successful speciation in Darwin’s finches. The medium tree finch probably originated from a “small morph” of the large tree finch from Isabela Island, which was either followed by (Lack 1947) or preceded by (Grant 1999) separate colonization events of “large morph” large tree finches from Santa Cruz Island and small tree finches from another island. […] Evidence that we present here, however, suggests that these three species may represent a case of evolution in reverse …”

They had birds collected at three different time periods, 1900s, 2005, and 2010.  Their morphological and genetic analyses suggest that through time, species composition started to move away from the three distinct clusters (small, medium, and large), and by 2010, there were two species left, the small and the medium tree finches, along if a population of hybrids between the two.

“The results presented here go to the heart of evolutionary biology: by what criteria do we denote species, and by what criteria do new species form or collapse? Here we present evidence that three sympatric species of Darwin’s tree finches in the 1900s have collapsed, under conditions of hybridization, into two species by the 2000s.”

They argue that their results show a case of disassortative mating, where the females of the “small tree finches” (Camarhynchus parvulus) are choosing among the larger of the “medium tree finches” (Camarhynchus pauper), creating a hybrid population of intermediate morphology. As for the “large tree finch” species, Camarhynchus psittacula, they don’t appear in any of their collections during the 2000s, and authors suggest there is a chance the species has gone extinct.

On chickens, dinosaurs and a fake tail

Chickens with fake tails simulate the shift in the center of body mass through Tetrapod evolutionary history, shedding light on limb movement of bipedal dinosaurs. 

Chickens raised with fake tails can demonstrate how T-Rex and other bipedal dinosaurs moved. Researches added a prosthetic tail to chickens in order to experimentally demonstrate that shifts in the body’s Center of Mass (CoM) caused limb movement to gradually change from hip to knee driven. Wings caused the CoM to move towards a more anterior position, leading birds to present ‘knee-driven’ movement, in which the hind limb moves by knee flexion empowered by the hamstrings. When the prosthetic tail is added to the chick right after it hatches, CoM gradually shifts with the birds’ development, leading to a more ‘hip-driven’ hind limb movement. The study is a partnership between the Universidad de Chile, the University of Illinois at Chicago and the University of Chicago, and was published at PLoSOne, Grossi et al. 2014. Walking Like Dinosaurs: Chickens with Artificial Tails Provide Clues about Non-Avian Theropod Locomotion, http://www.plosone.org/article/info:doi/10.1371/journal.pone.0088458#s5).