The "Species" of White Sands

Ecotone Sceloporus undulatus

Dear attentive blog followers. As may be obvious, I have been slacking a bit lately. As such, this blog will focus on last-last week's reading on species concepts. I think that the three species in White Sands provide interesting examples of how we might define species. I'll start by posing the question:

Could any of the three White Sands lizard populations be considered distinct species from their dark-soils counterparts? If so, which ones?

Here I'll consider each of the three White Sands lizards in the light of the major species concepts illustrated on page 27 of SPECIATION. I will focus mainly on:

1. The Biological Species Concept (BSC)

2. The Genetic/Phenotypic Cohesion Species Concept (RSC, CSC)

3. The Evolutionary Cohesion Species Concept (EcSC, EvSC)

4. The Evolutionary History/Phylogenetic Species Concept (PSC).

Now... to the species:

Sceloporus undulatus

The strongest line of evidence that Sceloporus form good species is based on the fact that local White Sands Sceloporus do not recognize 'invading' males in their territory as members of their own species. Indeed, instead of engaging in antagonistic behaviour, the local males seem to get confused... trying out courtship, exploratory and other confused displays (Robertson and Rosenblum in prep). We don't know yet what confuses these males, but this does indicate that some degree of speciation has occurred. A further confounding factor is that Sceloporus are continuously distributed across the ecotone separating dark soils and White Sands. This discourages allopatric speciation between the two habitats as the presence of a 'hybrid-zone' allows gene flow.

Thus, we generally can conclude that White Sands Sceloporus forms a pretty poor species. The presence of 'hybrid-like' individuals at the ecotone rules out the group as good species according to the Genetic cluster species concept (GCSC). It is difficult to rule out the possibility of multiple invasions of White Sands from dark soils, such that we cannotconclude that White Sands Sceloporus are monophyletic (largely ruling out the Evolutionary and phylogenetic species concepts).

Furthermore, Kayla will be looking at the further possibilities of mate choice and recognition in Sceloporus, thereby in a way, examining elements of the Recognition species concept. I personally am looking at the ecological roles of White Sands and dark soils Sceloporus... thereby determining if either makes good Ecological species.

Aspidoscelis inornata

Less work has been completed on this species, but it's useful to consider if the White Sands populations make a good species compared to the other two. At the ecotone, unlike Sceloporus, Aspidoscelis individuals are actually dark. Again, it's likely that multiple colonizations of White Sands occurred. We have not performed recognition and mate choice studies, so it is difficult to quantify the degree of behavioural isolation between dark and white lizards. As such, it seems as though Aspidoscelis do not form very good species by any criteria.

Holbrookia maculata

Of the three White Sands colonist lizards, Holbrookia seems the most likely candidate for a new species, distinct from dark soils populations. Following are two main lines of evidence in support of this statement.

a. White Sands Holbrookia males more often choose local females, and both sexes recognize local mates over non-local mates (see Rosenblum 2008). This suggests behavioural (pre-mating) isolating mechanisms in effect.

b. White Sands Holbrookia populations are disjunct from ancestral dark soils populations. That is, there is no 'hybrid' zone at the ecotone (individuals at the ecotone are indistinguishable from inter-dune individuals). This limits gene flow into the White Sands populations from dark soils populations.

But are White Sands Holbrookia monophyletic?

Were there multiple invasions from dark soils?

How does this compare to the other species?

A new member of our lab, Tyler Hether will be looking at landscape genetics and perhaps we can begin to uncover some of these questions...

Again, Kayla and I will be looking at subjects related to the recognition and ecological species concepts (respectively)... hopefully we can find out more about the nature of species formation at White Sands.

Speciation models

In chapter three Coyne and Orr focus on allopatric and parapatric models of speciation. Allopatric speciation refers to the divergence of populations that are separated by some kind of physical barrier, so that there is no gene flow between populations. There are two models of allopatric speciation- vicariant speciation and peripatric speciation. The main difference between these two models is the relative sizes of the populations involved in speciation. In the vicariant model, a population is split into two or more large populations by a barrier or by extinction of intermediate populations. In the peripatric model, a small population becomes isolated from the main population either by physical barriers or when a new area is colonized by a few individuals.

Parapatric speciation refers to the divergence of populations between which there is some gene flow. One model of parapatric speciation is the clinal model. In this model a species is distributed continuously across a variable environment. Subpopulations adapt to local habitats, but adaptation is hindered by gene flow from nearby ecologically distinct populations. When populations have become differentiated enough, reinforcement may play a role in generating reproductive isolation. In the stepping stone model of parapatric speciation, there are discrete populations with restricted gene exchange. Since populations are discrete it is easier for selection or drift to result in reproductive isolation than in the clinal model.

Though white sands and dark soils lizards have not speciated, we can still think of which of these models is most applicable to divergence of these populations. The first question we should answer is how much gene flow is occuring between white sands and dark soils lizards. Previous research has shown that there is some gene flow, though the amount differs between the different species of lizards (Rosenblum 2006). This means that the parapatric models are more applicable than the allopatric models. Next question: are populations distributed continuously over a variable environment, or are there discrete populations? While the environment is definitely variable from white sands to dark soils, the amount of connectivity between populations is also different between different species of lizards. For example, Holbrookia maculata show the most genetic differentiation between populations, and also the largest color difference between white sands and dark soils populations. Sceloporus undulatus shows an intermediate level of phenotypic and genetic difference between populations, and Aspidoscelis inornata shows the least of both (Rosenblum 2006).

This evidence shows that Holbrookia populations are probably the most discrete, with Sceloporus populations occurring in a less discrete distribution, and Aspidoscelis distributed almost continuously. So maybe the stepping stone model is most likely for Holbrookia, clinal for Aspidoscelis, and some combination for Sceloporus? And if the models are different, does this mean that different types of reproductive isolation could be important for different species? Reinforcement is thought to be important for the clinal model, but in the stepping stone model premating isolation might evolve more easily as a byproduct of selection or drift. Hmmmmmm…

Barriers leading to reproductive isolation

Last week we read the first two chapters of Coyne and Orr’s book Speciation. Chapter 1 of Speciation spends quite a bit of time discussing and classifying reproductive isolating barriers. Though I have already focused on reproductive isolation in past blogs based on information given in The Ecology of Adaptive Radiation, I will spend some time now giving a more comprehensive overview of possible barriers leading to reproductive isolation. Coyne and Orr define pre- and postmating isolation, as well as the barriers that cause them, as follows:

1. Premating isolation barriers- barriers that impede gene flow before transfer of gametes to members of other species.
a. Behavioral isolation: Members of different species do not initiate courtship or copulation with each other due to a lack of “cross-attraction”.
b. Ecological isolation: Barriers to reproduction are direct byproducts of adaptation to the local environment. This category includes isolation because of differences in habitat preference, timing of breeding, and pollinator interactions.
c. Mechanical isolation: Members of different species do not reproduce because they have incompatible reproductive structures.
d. Mating system isolation: This barrier refers to the evolution of partial or complete self fertilization or the asexual production of offspring, which can result in the formation of new species.

2. Postmating, prezygotic isolation barriers- barriers that act after transfer of gametes but before fertilization takes place.
a. Copulatory behavioral isolation: The behaviors of individuals during copulation do not allow fertilization to occur.
b. Gametic isolation: The transferred gametes cannot effectively cause fertilization.

3. Postzygotic isolation barriers- barriers resulting in hybrid sterility and inviability.
a. Extrinsic barriers: Sterility and inviability are results of the biotic or abiotic environment. This category includes ecological inviability, where hybrids have a lower fitness because of a failure to find an appropriate ecological niche. Behavioral sterility, where hybrids cannot obtain mates, is also included.
b. Intrinsic barriers: Sterility and inviability are results of developmental problems. Hybrid inviability is a result of developmental problems causing full or partial lethality. Hybrid sterility may be physiological or behavioral; physiological sterility leads to problems in the development of gametes or reproductive organs, while behavioral leads to developmental problems causing hybrids to be incapable of successful courtship.

Which of these potential barriers could be acting currently among populations of lizards in white sands and dark soils? Of the premating isolation category, behavioral and ecological isolation both seem possible. In fact, it seems like a combination of these two types would be most likely. As discussed previously, behavioral isolation could be a result of either a preference for local mates that are phenotypically similar, or a lack of recognition of mates from populations adapted to living in different environments. Ecological isolation is certainly important in terms of habitat preference; if white lizards and dark lizards don’t encounter each other because they live in different areas, this will result in reproductive isolation. I think ecological isolation would be important over most of the habitat, while behavioral isolation may be important at the ecotone.

In terms of postzygotic isolation, extrinsic barriers seem most relevant to the white sands system. Depending on the genetic basis of dorsal coloration (which is different among different lizard species in white sands) hybrids could suffer from ecological inviability. The mutation that causes blanched coloration is dominant in one white sands species and recessive in another. Either way, if a hybrid finds itself not well matched to its substrate and can’t effectively choose a better niche, it won’t do as well (it will probably end up as food for someone else).

From reading about all these different isolation barriers I have come to the realization that as I continue on with my plans to investigate behavioral premating reproductive isolation in these lizards, I can’t overlook the possibility that other reproductive barriers could be playing an important role as well, and I need to be aware that many factors have likely shaped the system as it is today.

Genetic lines of least resistance, continued

Good explanation of the genetic lines of least resistance, Simone.

I just wanted to add a few comments on the subject. Schluter mentions that when traits covary (in the ways Simone described earlier) the amount that one trait covaries with another will affect how far evolution will be pulled away from the direction in which selection is at its strongest. Take the finch beak example that Simone gave, and imagine that selection is strongest in the direction favoring an extremely long, narrow beak. If beak width and length depend on each other to a great extent, so that selection on one automatically changes the other dramatically (selection for a longer beak leads to a wider beak too), then this interaction would lead to evolution in a direction that is greatly skewed off of the path of strongest directional selection. If the traits did not affect each other as much, the direction of evolution would deviate from the direction of strongest selection to a smaller extent.

Schluter mentions that over time this effect of genetic constraint can be overcome and a population may make it to the top of an adaptive peak. But the stronger the covariance between the traits is, the stronger the skew will be away from the direction of strongest selection, and the longer it will take to make it up the peak.

One cool result of this whole covariance thing is that the degree of covariance between traits can help you more accurately predict the direction of evolution. If you realize that selection is strongest in a certain direction on an adaptive landscape, you can examine phenotypic traits that would be affected by selection, and based on how these traits covary you could make predictions about the direction of evolution along the landscape. Neat!

Now that’s really it for the Ecology of Adaptive Radiation…Speciation here we come!

Divergence Along Genetic Lines of Least Resistance & Final Conclusions

Last week Kayla and I finished "The Ecology of Adaptive Radiation"- the first novel in our reading list this semester.

The final (non-concluding) chapter focused on Divergence Along Genetic Lines of Least Resistance and was perhaps the only title that I had no clue what would contain. I hadn't really heard of the concept of genetic lines of least resistance and perhaps that's why I had such a hard time ploughing through the forty or so pages in this chapter. So here's a definition as far as I can manage:

Phenotypic evolution by natural selection is primarily determined by genetic variance and covariance that bias evolution away from greater fitness.

I suppose I have a feeble hold on the concepts of quantitative genetics so this definition scared me. This was further complicated by my tenuous grasp of the idea of 'additive genetic variance'... which is evidently the variation we are talking about in this case. I've come to understand additive genetic variance as the variation in offspring that is a direct result NON-interacting genes from the parents. That is, the sum of genetic variance from the two parents, where there is no epistasis or other interactions.

We have another interesting definition here, that I have some trouble wrapping my mind around.

I find that thinking about lines of least resistance in terms of examples is most useful. The common one is that if you had two traits, beak broadness and beak length, these traits would always be tied to each other such that you could never get a really narrow long beak, even if this was the 'fittest' phenotype. Hence, the 'adaptive hillside' on which the population rests would be a combination of these traits that was genetically feasible, but not necessarily the 'fittest' given the landscape.

I suppose that white sands lizards could also have traits like this. Say colour. Say dorsal (cryptic) colour and ventral (signaling) colour vary in such a way that you can never get to be completely matched to your dark soil surroundings, unless you sacrifice some ventral colour. On the other hand, if you lose pigmentation on your dorsal surface, your ventral colour is enhanced (this appears to be the case in white sands, but the genetic correlation between ventral and dorsal colour, if it exists, is unknown). So if we go into dark soils, even though the best situation would be a bright ventral colour for signaling and a dark dorsal colour for camouflage, this combination can never be achieve... and essentially you have the lizards sitting on an adaptive peak that is below that which is optimum, fitness-wise.

Just a disclaimer here- I think this is a bad example because it is quite probable that selection on dorsal and ventral colour is mostly unrelated. Selection on ventral colour likely has more to do with the environment in which signaling takes place (bright white sands versus ancestral dark heterogeneous habitat).

~~~

Well that's about it for now. I wanted to conclude by saying that I tried to read this book in undergrad and couldn't make it through; however, I am very happy that I picked it up again in my second year of my PhD. This was a much more appropriate time to read it and Schluter has definitely enhanced my understanding of many topics as well as filled in large gaps in my understanding of evolutionary ecology and adaptive radiation, specifically.

... on to SPECIATION!

Reproductive isolation and ecological speciation

In chapter 8 of The Ecology of Adaptive Radiation, Schluter addresses the role of reproductive isolation in adaptive radiation, focusing on different ways that reproductive isolation between populations may arise. Mayr and Dobzhansky initially formulated the idea that pre- and postmating isolation could arise between populations evolving in distinct selection environments, with complete reproductive isolation resulting ultimately as a consequence of divergent natural selection.

There are two models of how divergent selection causes reproductive isolation and ecological speciation:

By-product speciation is the first model. In the case of by-product speciation, divergent natural selection on phenotypes causes reproductive isolation to evolve incidentally between populations in different environments. Reproductive isolation is considered a “by-product” because it is not directly favored by selection. Both postmating and premating isolation can occur through by-product speciation. Postmating isolation evolves when genetic changes favored in different populations in different environments are incompatible when recombined in hybrids (this is known as hybrid inviability). Premating isolation can occur if mating preferences are genetically correlated with morphological or physiological traits that are the targets of divergent selection.

The second model Schluter mentions is competitive speciation. When intermediate genotypes in a population are at a fitness disadvantage selection may favor a population split leading to reproductive isolation. Competitive speciation is considered to be reinforcement if a period of allopatry leads to incomplete pre- and postmating isolation, and then when the populations come back together hybrids are selected against because they are at a fitness disadvantage. The process is known as sympatric speciation when there is no allopatric phase, and speciation is initiated by disruptive selection in a population. These two versions of competitive speciation are distinct from the by-product model because reproductive isolation is directly favored by natural selection in the sympatric phase.

I am interested in investigating whether premating isolation has occurred in white sands and dark soils lizards. In the by-product model, premating isolation between populations can develop when populations are in different selection environments, and mate preferences are linked to traits that are affected by natural selection in these differing environments.

What would have to occur for premating isolation to evolve between white sands and dark soils populations? First of all, the populations would have to be diverging in different selection environments. Check. White sands populations differ dramatically from dark soils populations in skin color, among other things. Second of all, divergent natural selection would have to affect traits linked to mate preferences or recognition. Here’s where things get a little more ambiguous. All three lizard species in the area have social signaling patches that are used in inter- and intrasexual interactions. The colors of these patches are different between white sands and dark soils populations. We know that this difference in skin color is linked to differences in the Mc1r gene. Mutation of Mc1r in white sands lizards has led to adaptive blanched dorsal skin coloration, and this change has affected the coloration of the social signaling patches as well.

So yes, social signaling patch color, which is involved in social interactions, is diverging due to natural selection in different environments. But is social signaling patch color related to mate choice or recognition? Maybe mate choice is linked to chemical secretions or social interactions that are divergent between populations by chance, not because of divergent natural selection? Or, for that matter, is there even mate choice occurring in these lizards? Maybe they would just be game for mating with any conspecific they run into. These are questions I’m hoping to begin answering during my first field season this spring. Okay, this is getting long, so I’ll stop…but if anyone has any input on my ideas I would love to hear it!