The shrinking sloths of Panama

Anderson and Handley (2002) presented an analysis of the evolution of three-toed sloths on the islands of Bocas del Toro, Panama. These islands were part of the mainland during the last glaciation, and became isolated by rising sea levels during the past 10,000 years. Some of the islands remained connected to the mainland, and to each other, for longer than others. On each of five islands, the living sloths are much smaller than the average size of sloths on the mainland. On one of the islands, this size reduction is so great (seven standard deviations) that Anderson and Handley (2001) suggested that the island population be assigned to a new species.

The example is the closest to a controlled experiment in island dwarfing that we are likely to find. The time that each island was isolated has been well established based on ancient sea levels and the ages of depth-sensitive corals between them. All of the islands have the same ecology, with the exception of species lost after the islands were isolated. The sloths are represented by subfossil deposits as well, which provide samples of their evolution over time.

Hence, it is a very important example for testing mechanisms and patterns of evolution when continental species are isolated on islands. The paper includes many valuable brief reviews of issues related to evolution in this context. I'm finding this paper tremendously useful to me right now, so I'm taking a number of notes and also including some of the bibliographic references. Several of these are references I've used before, but this is a convenient topic to gather together some references on evolutionary rates as well as biogeography.

The first valuable mini-review in the paper is a paragraph that surveys hypotheses for the dwarfing phenomenon itself. Beginning with the well-worn observation that small species evolve larger size on islands while large species dwarf, Anderson and Handley (2002:1045-1046) discuss the interpretations of the causes for these changes in a number of review articles:

Reviews differ in which and how many mechanisms drive that change in body size and under what circumstances each is relevant. Some (Lomolino 1985; Roth 1992; McNab 1994) conclude that insular populations of small species become larger to use broader resource bases in the absence of former competitors (competitive release of Lomolino 1985), and large mammals are often resource-limited on islands, favoring smaller size (resource limitation of Lomolino 1985). Recently, Marquet and Taper (1998, p. 135) suggested that resource limitation may cause both dwarfism in large mammals and gigantism in small ones, due to changes in intraspecific competition that are related to home range size. In contrast, Adler and Levins (1994) put forward models invoking selection for larger body size in small species in response to higher intraspecific competition (see also Crowell 1983). Finally, Heaney (1978) proposed that island area determines which factor drives selection: resource limitation on small islands and competitive release on large islands. General models for the evolution of body size in insular terrestrial vertebrates have been proposed and a few notable exceptions investigated (e.g., Foster 1964; Case 1978; Lawlor 1982; Case and Schwaner 1993; Petren and Case 1997). Thus, while the overall causes of body size evolution in insular situations remain an open area of research, most reviews to date suggest that selection for smaller size in large mammals on islands is caused by resource limitation and strong intraspecific competition (Heaney 1978; Lomolino 1985; Roth 1992).

Upon reading this, I turned to a few other references that review the same topic. You can find them summarized to some extent in this post on ecogeographic research into the island rule, and this post on the recent work of Raia and Meiri on carnivore ecology and the island rule. This is a fluid field in theoretical terms; the evolution of sloths on these islands might contribute to it in some ways that haven't yet been assessed.

In any event, the authors don't really take a position in this paper concerning why the sloths dwarfed on these islands. The fact that these are sloths is maybe relevant -- they have relatively low energy expenditure and depend on slow movement and concealment to avoid predation. They are folivores, meaning that they are probably less sensitive to resource availability than mammals that depend on fruits and other foods with patchy distributions. The paper doesn't specify whether competition for leaves may have increased based on the behavior of other species on the island -- I might expect that howler monkeys would have become more intensive folivores, for example, but I don't know if they were present.

They do note later in the paper that the pattern of size reduction does not match what might be predicted based on selection in a new static environment -- where in this case, the "new" aspect is the isolation. So they present a number of suggestions for why the maximum selection intensity would not occur immediately upon the formation of the islands:

However, the linearity of the response does not fulfill theoretical expectations. If a particular smaller body size is optimal on islands, then selection should be strongest immediately after island formation, when the population is farthest from the new adaptive peak. Body size would then asymptotically approach the equilibrium (optimal body size) over time, as selection intensity decreased. This is clearly not the case in the Bradypus from Bocas del Toro, where sloths from the youngest islands (Isla Popa and Isla Cristóbal) are not significantly different in body size from mainland samples. Skulls of sloths from those islands do appear slightly more gracile than those of mainland individuals, however (Anderson and Handley 2001). One possible explanation is that the basis for changes in optimal body size lies with the disappearance of other species in the community, which does not occur immediately upon island formation. Alternatively, the adaptive peak for optimal body size might shift as a function of the population's average body size (presumably by some frequency-dependent mechanism; see Bürger and Lynch 1995). Because of these discrepancies, future work is necessary to reconcile the present results with theory or perhaps develop theoretical models regarding conditions under which morphological divergence would be linear for thousands of generations in new selective environments.

I would guess the frequency-dependent scenario myself, since an arbitrarily strong selection would drive the sloths extinct, but the advantages of small size would probably be less marked as the population became less numerous. Even the evolutionary bonus of late reproduction in a shrinking population -- predicted by Hamilton -- might come into play. Which would be novel, since populations generally don't reduce in numbers in such a way as to drive this evolutionary pattern.

This problem involves the authors in a discussion of evolutionary rates. There is a very long literature on this problem, which began with Simpson and Haldane; key papers in the more recent literature include work by Philip Gingerich (from the paleontological perspective) and Michael Lynch and Russell Lande (from the genetic perspective). The sloths don't present any particular problems in terms of rate estimation -- they are not unusually slow or significantly faster in their body size evolution compared to maxima based on observed intensity of selection in field populations. The authors problematize the sloths in terms of having a moderately high rate of selection that was sustained for a long time:

Clearly, scaling of evolutionary rates remains a controversial area of much current research. Perhaps the most salient feature of the present analyses regards the consistency of the pattern. Because the time series of sloths of Bocas del Toro provides an example of linear decrease in body size with increasing island age, they likely represent a system whose estimates of evolutionary rates and selection intensity are not diluted by intervening periods of stasis. Similar rates in haldanes have been reported over short time intervals (<100 years; Pergams and Ashley 2001). What is noteworthy is that such rates are evidently sustained in the sloths of Bocas del Toro. We detected no slowing of evolutionary rates in the four geologically independent populations of dwarf sloths (regression of loge haldanes on loge island age following Gingerich 1993, 2001; P = 0.692, R2 = 9.5%). Thus, this example may represent continuity between micro- and macroevolutionary processes, as the differentiation in body size has been an integral part of the speciation process in the oldest insular population (see Anderson and Handley 2001). The archipelago of Bocas del Toro clearly constitutes an outstanding system for similar studies of other taxa, as well as complementary work examining genetic differentiation among the various populations.

There's something interesting there. More on evolutionary rates later.

References:

Anderson R. P., C. O. Handley Jr. 2001. A new species of three-toed sloth (Mammalia: Xenarthra) from Panamá, with a review of the genus Bradypus. Proc. Biol. Soc. Wash. 114:133.

Anderson R. P., C. O. Handley Jr. 2002. Dwarfism in insular sloths: biogeography, selection, and evolutionary rate. Evolution 56:1045-1058. doi:10.1554/0014-3820(2002)056[1045:DIISBS]2.0.CO;2

Bürger R., M. Lynch. 1995. Evolution and extinction in a changing environment: a quantitative-genetic analysis. Evolution. 49:151163.

Gingerich P. D. 1983. Rates of evolution: effects of time and temporal scaling. Science. 222:159161.

Gingerich P. D. 1993. Quantification and comparison of evolutionary rates. Am. J. Sci. 293A:453478.

Gingerich P. D. 2001. Rates of evolution on the time scale of the evolutionary process. Genetica. 112/113:127144.

Haldane J. B. S. 1949. Suggestions as to the quantitative measurement of rates of evolution. Evolution. 3:5156.

Lande R. 1977. Statistical tests for natural selection on quantitative characters. Evolution. 31:442444.

Lande R. 1979. Quantitative genetic analysis of multivariate evolution, applied to brain:body size allometry. Evolution. 33:402416

Lynch M. 1990. The rate of morphological evolution in mammals from the standpoint of the neutral expectation. Am. Nat. 136:727741.