Monday, April 11, 2016

The small population paradigm: The be-all and end-all for small populations in nature?

[ This post is by Jackie Wood; I am just putting it up.  –B. ]

What is the fate of small populations in nature?

This question (and its answer) has critically important implications for the conservation and management of wild species considering that many natural habitats now exist only as small and isolated fragments due to human activities.

With only a cursory glance at the scientific literature, we might understandably become convinced that we absolutely, without a doubt, know the answer to this question. There are a suite of well-known threats that include habitat loss and fragmentation, exploitation, and now, increasingly, climate change that have conspired to yield widespread reductions in the population size of many natural species. As these threats continue to exact their toll on the population size (N) of an isolated population (isolation is a key point since such populations no longer benefit from an influx of genetic material from neighboring populations), breeding between related individuals becomes more common (inbreeding) and genetic variation that enables a population to respond to environmental change is lost more rapidly (genetic drift). Together, these can potentially lead to reduced reproduction and increased mortality, resulting in further decreases in N. This, in turn, results in even more inbreeding and greater genetic drift – and just like that, the population is caught in a downward spiral of ever-decreasing N until a point at which the population is so small that a chance event such as a bad winter can deliver the coup de grâce that finally drives the population out of existence. This process, called the “extinction vortex” by Gilpin and Soulé in 1986, is a hallmark of Caughley’s conservation genetics small-population paradigm; it is cited in virtually every textbook and taught in every undergraduate course on conservation biology. There are certainly several well-known cases of natural populations that have suffered the grip of the extinction vortex, but how pervasive is it in general?

Spoiler alert: it turns out that this classic extinction vortex might not be so pervasive after all!

King of the Cape: a brook trout at Cape Race, the system in which we studied these questions (as described below).  Photo credit: Cyndy Desjardins.

A key factor driving the extinction vortex is “genetic stochasticity”: the random loss of genetic variation necessary to enable a population to adapt to environmental change. In populations that are small and declining, neutral genetic variation (i.e. genetic variation that is not currently contributing to the fitness of individuals and is therefore not affected by natural selection) is predicted to be lost increasingly more rapidly, an expectation that has been confirmed in both laboratory and natural populations. But in the case of adaptive potential, what we are more interested in is the genetic variation that underlies traits that are related to fitness, which is known as quantitative genetic variation (QGV; which can be estimated using one of several different metrics including VA, h2, and CVA). The specific connection between QGV and adaptive potential originates from the breeder's equation (R = h2S), where response to selection (R) is directly proportional to the strength of selection (S) and the QGV (h2) of a trait (or multiple traits using the multivariate form of the breeder’s equation, the G-matrix).

In theory and under certain simplifying assumptions, loss of QGV is predicted to occur at the same rate as loss of neutral variation with decreasing N, and this has been found to be the case in laboratory populations for certain kinds of traits. In the nature, however, the relationship between QGV and N remains unresolved, and there are a number of reasons why this is the case.

One reason is that many traditional assays of genetic variation in natural populations have used neutral genetic variation as a surrogate for QGV even though the correlation between these metrics has been found to be weak, and the studies also didn’t account for how selection acts on variation. And this does matter; for example, stabilizing selection can actually favour the maintenance of genetic variation within small populations. Similarly, loss of QGV might be buffered to some extent if small populations can respond to changing environmental conditions in the short term by plasticity (the ability of a single genotype to produce different phenotypes in different environments), a trait which might reasonably be favored under certain types of environments occupied by small populations, but this possibility has often been overlooked. Laboratory studies of QGV and response to selection relative to N have largely been restricted to a small number of species including bacteria and fruit flies, and both the environmental conditions used in these studies and genetic characteristics of these species may not adequately portray what happens under many conditions in nature. For example, the relationship between genetic variation and N might reasonably differ between fruit flies and vertebrates because vertebrates can exhibit behaviours such as inbreeding avoidance and complex mate choice. Laboratory experiments also tend to use similar, simplified, or benign starting conditions across populations even though this is unlikely to occur regularly in nature. Among small natural populations, conditions immediately after habitat fragmentation likely vary, and this will ultimately influence the fate of each population in terms of QGV and response to selection.

Typical weather conditions at Cape Race, our research site.  Alternate title: “Lost in the fog of quantitative genetics.”

How the process of habitat fragmentation might alter environmental conditions as fragment size and N is reduced has potentially important evolutionary consequences because this will determine the kind of selective regimes that populations are exposed to, and hence will influence the adaptive genetic make-up of fragmented populations (see diagram below). One possibility, which represents the more or less classic view of habitat fragmentation, predicts a systematic directional change in environmental conditions with decreasing fragment size and N (the Directional Hypothesis). In the Directional Hypothesis, large fragments are typically assumed to be high quality, whereas small fragments are expected to represent marginal habitat due to increasing edge effects including increasing parasitism, predation, and more widely fluctuating climatic conditions.

However, this might not be the only possibility. An alternative prediction is that evolutionary effects of habitat fragmentation might depend on initial starting conditions within the fragments themselves (the Variable Hypothesis). Simply put, where you end up will depend quite a bit on where you started. Here, large fragments are presumed to be similarly complex and consist of multiple habitat types, and small habitat fragments are expected to simply be random samples from the larger ones. For example, microclimate conditions or distribution of food in a large fragment may differ both spatially and in time, such that fragmentation will result in patches that become increasingly dissimilar as they are reduced in size – possibly also resulting in increased variability in selective regimes. Collectively, the Variable Hypothesis suggests if that we were to compare multiple large habitats, they would be similar in a containing a large number of different habitat types, whereas if we compared multiple small habitat fragments there would be less variability in habitat types within the fragments (since logically a small fragment would have less room for many different habitat types), but more between-fragment variability. For example, the most extreme version of this hypothesis, and perhaps the most easily visualized, is a scenario in which we have many very small fragments with each fragment containing only one type of habitat, and the habitat type is completely different for each fragment.

Two alternatives for the effect of habitat fragmentation on environmental conditions within and among fragments occupied by populations of differing N.

In 2010 our lab initiated a multi-year research program aimed at testing the assumptions of the conservation genetics small-population paradigm in nature. Using the Directional Hypothesis and the Variable Hypothesis as our points of departure, we set out first to quantify the relationship between N and variability in habitat conditions for a series of pristine, naturally fragmented, and isolated brook trout populations located at Cape Race, Newfoundland, that varied widely in N.

Most Cape Race streams end in waterfalls emptying into the ocean so we can confidently say the populations are isolated! But, like, watch your step.


From detailed habitat surveys wherein we collected data for a range of habitat parameters across 14 and 19 streams in two consecutive summers, we observed a little evidence for increased variability in mean habitat parameter values among small compared with large populations, but much more evidence that habitat parameter CVs (a measure of variance around the mean) were more variable at small than large N. Taken together, our findings suggested at least some support for the Variable Hypothesis in Cape Race streams. These patterns naturally raised the possibility that the small trout populations might be subject to more varying selective regimes than large populations. If true, and if such patterns in environmental conditions were stable over time, we hypothesized that population-level characteristics including phenotypic plasticity and QGV might also vary more among small than large trout populations.

To test this, we conducted two common-garden experiments, but we found no evidence for consistent differences in plastic response to changing temperature from large to small N for 8 Cape Race populations, and there were also no systematic differences in the level of QGV (for any of three different QGV estimators: VA, h2, and mean-scaled evolvability) in relation to N for the populations. Using genome scans, we also looked for signals that adaptive genetic differentiation was related to N (adaptive genetic differentiation simply refers to how far apart two populations are in terms of genetic markers that are linked to fitness-related traits). In contrast to the plasticity and QGV studies, here we found evidence to suggest that small population pairs tended to be more different than pairs of large populations, not only suggesting that selection is at work in small Cape Race populations, but also providing another line of evidence that suggests that small populations might be exposed to a variety of environmental conditions. In this study we also found that small-large population pairs were more different than pairs of large populations, so there was support for the Directional Hypothesis as well! The result of increased adaptive differentiation among small populations is notable given that we also found that neutral genetic variation increased with increasing N, which is consistent with pronounced genetic drift in the small populations.

Our results were clearly not concordant across the board; they provided support for the Variable Hypothesis in terms of habitat conditions, for both the Directional and Variable Hypotheses in regards to adaptive differentiation, and for neither hypothesis for plasticity and QGV in relation to N. Nevertheless, they are encouraging in suggesting that (i) populations of 100 adults can be as genetically robust as populations with 1000–10000 adults in some contexts, (ii) small populations may have the ability to deal plastically with environmental change to some extent, and (iii) selection may very well operate at small N resulting in adaptive population differentiation even at very fine scales. In other words, many small populations may not be evolutionary dead ends, as commonly thought, but rather, may constitute locally adapted populations that contain potentially unique adaptive genetic variation (by virtue of inhabiting unique environments and being exposed to unique selection regimes).

Of course, one thing we can’t rule out is that the small populations we study are merely the lucky ones that are left; perhaps other small brook trout populations were present at some point in time but were extirpated due to the suite of genetic problems usually associated with small N. We’ll never know.  Still, our general observations of Cape Race populations are that brook trout are quite resilient little fish as long as their key habitat requirements are met. Brook trout can be found in virtually any isolated ditch or tiny pond on the Cape, and seem to do just fine at small N provided there are cold-water refugia to escape warm summer temperatures, and upwelling groundwater for spawning and egg incubation.

Yes, there is a stream in there. Yes, it contains a naturally reproducing brook trout population.

If there’s a main point to be made based on the results of our work at Cape Race, it’s the critical importance of habitat quality for population persistence at small N; our results also suggest that in many cases environmental stochasticity might be a more immediate threat than genetic stochasticity for small brook trout populations. On the other hand, the idea that brook trout are fairly robust to the effects of small N may not be all that surprising given their capacity to colonize new habitats, an affinity for small headwater stream environments, and a partially duplicated genome which may act to buffer the loss of genetic diversity at small N.

What about other types of species? How do they do when populations are reduced to a finite number of individuals? It’s hard to say; we can certainly make inferences based on what we know about species ecology, life history, behaviour, and conservation-genetic theory, but the truth is that there are currently no other natural vertebrate systems that have been studied as extensively as Cape Race in this regard. In a recently published meta-analysis, we attempted to shed some light on this question by extracting data from previously published articles dating back to 1980 which estimated h2 or selection (strength, direction, and form) for natural populations for which N data was also available. Using this data, we looked for evidence of systematic differences in h2 and selection with N, pooling data across a variety of species. Looking at h2 and selection together also enabled us to infer adaptive potential in a very crude sense using the breeder’s equation (recall that R = h2S; we couldn’t formally test N vs. adaptive potential since h2 and selection data weren’t typically available for the same population). What we found was, well, not much.  There was little evidence for differences in h2 or the extent of natural selection across the various species and N that we included in the analysis. As for brook trout at Cape Race, these results suggest, at least indirectly, that while genetic drift and selection operate simultaneously in nature, drift may not always overwhelm selection at small N and that populations of varying size may respond to environmental change. Evidence supporting the efficacy of selection despite small N has also been found in a recently published study by Labonne and colleagues for a brown trout population originating from only three founding individuals.

Overall, however, it’s extraordinarily difficult to draw definitive conclusions regarding the status of small populations in nature in general based on our findings from collating data from scientific articles. That’s because the other take-home message from our meta-analysis is that there are several glaring information gaps that hamper our ability to say anything with certainty.  For example, we weren’t able to account for the degree of isolation of populations (due to a lack of information on gene flow); this is a critically important point since even small amounts of gene flow can help small populations to retain genetic variation that would otherwise be lost by persistent genetic drift and inbreeding depression. Data was also biased towards widespread, generalist species. We found no studies which estimated selection or h2 for amphibian populations of known N, despite being one of the planet’s most threatened taxonomic groups. Other rare, specialist species (species that might reasonably be most likely to fall prey to the small-population paradigm), or entire taxa (reptiles, invertebrates) were similarly poorly represented in our databases. There is also a need for greater adoption of multivariate approaches to studying evolution in natural populations. Most studies focus on single traits; however, many traits do not evolve independently, but rather are correlated with other traits. This means that direct selection resulting in an increase in the value of one trait can result in indirect selection on a correlated trait to increase it, decrease it, or even constrain it; thus, focusing on single traits may not adequately detect constraints to evolution in small populations.

Keeping these gaps in mind, we very cautiously suggest that response to selection at small N might be more extensive than previously assumed in evolutionary and conservation biology. But even if we could be sure about this, it still wouldn’t mean that small populations are equal to large populations. Even if some small populations have been lucky enough to land in habitats that can support them and retain the capacity to cope with changing conditions to some degree by plasticity or evolution, they still have a greater risk of extinction from environmental and demographic stochasticity. Only large numbers can buffer against such threats. And of course, other small populations won’t be so lucky, and will end up in marginal environments where they will inevitably fulfill the expectations of the conservation genetics small-population paradigm.

What is the fate of small populations in nature?

Well, it is probable that things simply become more unpredictable at small N, including evolution. This means that we may only be able to address this question on a case-by-case basis. As suggested by the late David Reed in regards to the minimum amount of genetic diversity required for populations to persist for a given length of time, the answer will intimately depend on factors such as habitat quality, the rate and magnitude of environmental change, and the history and genetic characteristics of the population or species of interest.

Just completely casual, totally normally lounging. Nothing out of the ordinary happening here.

Literature Cited:

Wood, J. L. A., Yates, M. C., and D. J. Fraser. 2016. Are heritability and selection related to small population size in nature? Meta-analysis and conservation implications. Evolutionary Applications. doi: 10.1111/eva.12375.

Labonne, J., Kaeuffer, R., Guéraud, F., Zhou, M., Manicki, A., and A. P. Hendry. 2016. From the bare minimum: genetics and selection in populations founded by only a few parents. Evolutionary Ecology Research 17(1):21–34.

Wood, J. L. A., Tezel, D., Joyal, D., and D. J. Fraser. 2015. Population size is weakly related to quantitative genetic variation and trait differentiation in a stream fish.  Evolution 69:2303–2318.

Wood, J. L. A., and D. J. Fraser. 2015. Similar plastic responses to elevated temperature among different-sized brook trout populations. Ecology 96:1010–1019.

Fraser, D. J., Debes, P. V., Bernatchez, L., and J. A. Hutchings. 2014. Population size, habitat fragmentation, and the nature of adaptive variation in a stream fish. Proceedings of the Royal Society of London B: Biological Sciences 281(1790): 20140370.

Wood, J. L. A., Belmar-Lucero, S., Hutchings, J. A., and D. J. Fraser. 2014. Relationship of habitat variability to population size in a stream fish. Ecological Applications 24:1085–1100.

Reed, D. H. 2010. Albatrosses, eagles, and newts, Oh My!: exceptions to the prevailing paradigm concerning genetic diversity and population viability? Animal Conservation 13:448–457.

Caughley, G. 1994. Directions in conservation biology. Journal of Animal Ecology 63:215–244.

Gilpin, M. E. and Soule, M. E. 1986. Minimum viable populations: processes of extinction. Pages 19–34 in: Conservation Biology: The Science of Scarcity and Diversity (ed. Soule, M. E.). Sinauer Associates, Sunderland, MA.

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