DIVERGENCE FOLLOWING ISLAND COLONIZATION stems from the action of microevolutionary processes, including drift, selection, gene flow, and mutation (Mayr 1954, Lande 1980, Barton 1998, Grant 1998). The suggestion that all of these processes can play a role in divergence, potentially acting separately or in concert, is uncontroversial. However the relative importance of each in natural systems is not generally agreed (Provine 1989, Barton 1998, Price 2008). Islands are regularly referred to as natural laboratories, and as such, studies of island forms have made major contributions to the development of general evolutionary theory (Grant 1998). Although the microevolutionary processes mentioned above are not unique to islands, the way that particular processes operate in insular versus continental situations may be fundamentally different due to consistent biotic and abiotic differences between the two geographic circumstances (MacArthur and Wilson 1967). Given an accumulating number of empirical studies, we can assess if particular microevolutionary processes are of more general importance than others in generating the diversity of island forms.
In their landmark book formalizing island biogeography as a field in its own right, MacArthur and Wilson (1967) devoted a chapter to evolutionary changes following colonization. This chapter is rich with ideas about how microevolution could proceed on islands, with reasoning largely based on the limited empirical data available at the time. Since then, empirical evidence for the importance of various microevolutionary processes has appreciated considerably, allowing a reassessment of MacArthur and Wilson’s views. Here I discuss a number of mechanisms by which drift and selection can influence divergence of island-colonizing birds. I examine three concepts: (1) whether founder-mediated drift is more effective than long-term gradual drift in shaping levels of diversity and divergence as evidenced by neutral genetic markers, (2) whether morphological divergence is consistent with drift or selective mechanisms, and (3) how frequent shifts in competitive regimes on islands could affect common patterns of morphological divergence associated with insularity in passerine birds.
The establishment of a new population involves phases of founding and recovery leading to longer-term persistence. During each stage, the random sampling effect of drift has the potential to affect the degree of diversity and divergence exhibited by a population. The effects of drift are more pronounced when effective founding population sizes are smaller, recovery times are longer and long-term effective population sizes are limited (Wright 1931, Nei et al. 1975). Drift is particularly relevant to island populations as it has the potential to prevail over selective mechanisms due to the vulnerability of small isolated populations to stochastic events. The potential significance of founder-mediated drift was emphasized by Mayr (1942, 1954). MacArthur and Wilson (1967) considered how founder events could potentially impact the evolution of a newly established population, but in the absence of empirical data concluded that “the evolutionary effects of initially small population size can only be guessed at this time” (p. 154). However, their general skepticism of the relative importance of founder events is illustrated in the passage: “evolution due to genetic sampling error is an omnipresent possibility but one easily reduced to relative insignificance by small increases in propagule size, immigration rate or selection pressure” (p. 156). Despite this relatively unenthusiastic view, founder-effect ideas have had a prevailing influence on the development of divergence and speciation models on islands (reviews in Provine 1989, Grant 2001).
In the literature, the term “founder effect” has been applied very broadly, encompassing any change associated with population founding. These include changes in diversity measures or allele frequencies (e.g., Reiland et al. 2002, Abdelkrim et al. 2005, Hawley et al. 2006), the particular phenotypic attributes of the founders themselves (e.g., Grant and Grant 1995a, Berry 1998, Kliber and Eckert 2005, Baker et al. 2006) and more complex founder-induced speciation models that invoke a role of founder events in reorganizing quantitative genetic variation and catalyzing speciation (Mayr 1954, Carson and Templeton 1984). Debate has ensued over the theoretical grounding (Barton and Charlesworth 1984, Carson and Templeton 1984, Slatkin 1996) and empirical likelihood (Rice and Hostert 1993, Templeton 1996, Coyne and Orr 2004, Walsh et al. 2005, Templeton 2008) of specific founder-induced speciation models. However, when considering natural situations, it may be unfeasible to determine if all requirements of different founder-induced speciation models were met at the time of divergence (Barton and Charlesworth 1984). Many studies of founder effects have instead focused on the effects on neutral genetic variation as a tangible indicator of the strength of drift associated with founding. Two measures of diversity are usually considered, allelic diversity and heterozygosity, with the former being more sensitive to sampling effects due to the loss of rare alleles (Nei et al. 1975). Therefore, milder founder events are indicated by decreases in allelic diversity but not heterozyosity. Immediate and large-scale loss of both measures of diversity along with the appearance of instantaneous levels of differentiation would indicate a stronger perturbing effect of a founding event. While these measures do not address loci under selection, neutral marker heterozygosity can reflect fitness (Coltman and Slate 2003). The mechanisms of such a relationship are debated (Balloux et al. 2004), however in bottlenecked populations the association between neutral and selected loci may be largely due to increased linkage disequilibrium resulting in hitch-hiking effects for neutral loci (Hansson et al. 2004).
Studies of rapid population declines in a range of species have demonstrated that loss of diversity can be severe when declines are sizable and persist for an extended time (e.g., Pastor et al. 2004, Weber et al. 2004, Roques and Negro 2005, but see Hailer et al. 2006). Similar effects might be expected of colonizing populations that go through a bottleneck during founding. However, there are key differences between a colonization event and a population crash. In species that successfully colonize and establish a population in a new location, there may be greater opportunity for rapid recovery following founding and the possibility for continued immigration from the original source or multiple sources, limiting the genetic effects of a bottleneck. The establishment of a new population is therefore not necessarily accompanied by a strong genetic founder effect, a conclusion reached in studies that report similar levels of diversity in long separated mainland and island-dwelling taxa (Seutin et al. 1993, Illera et al. 2007). However, island populations generally do have lower genetic diversity than those on mainlands (Frankham 1997), a feature variously attributed to combinations of founder events (Pruett and Winker 2005), repeated population bottlenecks following establishment (Bollmer et al. 2007), and gradual drift in small populations over extended time periods (Mundy et al. 1997, Bollmer et al. 2005, 2007, Ohnishi et al. 2007). In populations that represent an ancient colonization, distinguishing between the genetic effects of a pulse of drift associated with a founder event and long-term persistent drift over time is difficult because both mechanisms can result in decreased diversity and increased differentiation. Situations where colonization dates are recent and recorded, such as historically documented natural colonization events or artificial introductions, are therefore required to determine if colonization and population establishment results in an immediate and substantial effect on neutral genetic diversity.
Population size changes can result in varying genetic signatures depending on the type of genetic markers utilized, and ideally information from multiple types of markers would be considered when assessing the genetic impacts of population founding (Hawley et al. 2008). However, in the absence of a full suite of genetic markers, microsatellites are a suitably sensitive marker for assessing variation associated with founder events and population bottlenecks (Hawley et al. 2008), and have frequently been applied to founder event scenarios (table 11.1). I first discuss microsatellite studies of rare natural situations where information on the timing and sequence of single and multiple colonization events is available for colonizing bird species. Further examples of artificially introduced bird populations are reviewed to assess current empirical evidence of founding events as a perturbing force in island-colonizing birds.
The historically documented sequential colonization by the Tasmanian silvereye (Zosterops lateralis) to New Zealand and outlying islands over the last 180 years is a classic of ornithological literature (Mayr 1942, Lack 1971; see figure 11.1). In addition to recently colonized populations, successively older populations are represented by Z. l. chlorocephalus on Heron Island which is at most 4,000 years old (based on the length of time the island has been vegetated and mitochondrial DNA divergence [Hopley 1982, Degnan and Moritz 1992]) and extant endemics on Norfolk Island (Z. tenuirostris) and Lord Howe Island (Z. tephropleuris). The latter two populations are in the order of millions and hundreds of thousands of years old, respectively, based on mitochondrial DNA divergence estimates (Phillimore 2006). The combination of documented colonizations and evolutionarily older populations provided an opportunity to contrast the role of founder events versus long-term gradual drift in shaping neutral genetic diversity (Clegg et al. 2002a).
The quantification of neutral genetic diversity and divergence using microsatellites in Zosterops populations revealed that single founder events did not result in significant reductions in genetic diversity as measured by allelic diversity or expected heterozygosity (figures 11.2a and 11.2b). Nor did significant levels of population differentiation arise as a consequence of single founding events (figure 11.2c) (from Clegg et al. 2002a). While no pairwise test showed a significant reduction in diversity, sequential founder events were associated with a significant decreasing trend in allelic diversity, corresponding to a 40% reduction overall. No significant trend in heterozygosity was observed. The level of differentiation was associated with the number of founder events separating any two populations (figure 11.2c). When comparisons were restricted to those occurring in sequence, significant FST values were recorded in one of five cases where populations were separated by a single founder event, two of four separated by double founder events, two of two separated by triple founder events, and between the two populations separated by four founder events (table 11.1) (Clegg et al. 2002a). Three to four sequential founder events were required for allelic diversity to approach that seen in the older populations (figure 11.2a). In contrast, the decreased levels of heterozygosity seen in the older forms (on Norfolk Island and Lord Howe Island) were not even approached (figure 11.2b), despite the potential for sequential founder events to affect this measure (Motro and Thomson 1982, LeCorre and Kremer 1998). Lower diversity and increased divergence of old populations when compared to the mainland population resulted from loss of alleles along with often dramatic shifts in frequencies of the remaining alleles, resulting in fewer alleles with higher average frequencies in older populations. In half (9/18) of the locus/old population combinations, one or two alleles, not found in the mainland population, were detected. Some of these may represent replacement by mutation; however, mutation has not been sufficient to make up for allelic losses occurring in small, old populations. The level of diversity in old populations was not strictly related to island age, although the oldest population (Norfolk Island) had the lowest levels of diversity. A number of factors may account for this incongruity, including differences in long-term effective population sizes and the potential for rare immigration events to introduce alleles. The level of divergence between evolutionary old taxa was related to divergence time, with measures from the shortest divergence time being comparable to those recent populations that had experienced the most sequential founding events. Divergence among old forms separated for longer times far exceeded any level of divergence achieved via repeated founder events (figure 11.2c).
TABLE 11.1
Comparisons of Microsatellite Genetic Variability Between Source and Naturally Colonized or Translocated Bird Populations
Figure 11.1. Map of the southwest Pacific showing the historically documented colonization of the Tasmanian silvereye, Zosterops lateralis lateralis, to New Zealand and outlying islands. Numbered arrows show colonization sequence. Years: 1 = 1830s, 2 and 3 = 1856, 4 = 1865, 5 = 1904. Other Zosterops species and subspecies included in the genetic analysis occur on Norfolk Island, Lord Howe Island, Heron Island, and mainland Australia, represented by Brisbane.
Figure 11.2. Genetic diversity and divergence, (± standard errors), of Zosterops forms as measured by (A) allelic diversity, (B) heterozygosity, and (C) pairwise FST. Number of founder events is the number of island colonizations separating two populations. Numbered arrows refer to colonization sequence in figure 11.1. Numbers in parentheses are the number of pairwise comparisons among populations or among subspecies/species. Locations are ML = mainland (Brisbane, Australia), T = Tasmania, SI = South Island, New Zealand, CI = Chatham Island, PN = Palmerston North, A = Auckland, NIlat = Norfolk Island Z. lateralis, HI = Heron Island, LHI = Lord Howe Island, NIten = Norfolk Island Z. tenuirostris. Modified from Clegg et al. (2002a).
In the Zosterops system, the ineffectiveness of single founder events to perturb genetic diversity and divergence is repeatedly demonstrated. Differences accrued with sequential founder events, but in general a comparison of recent and old island forms pointed to a stronger influence of gradual drift over time on neutral genetic variation. Bayesian simulations of the founder events indicated that this result was likely due to a combination of substantial effective founder population size followed by rapid increases in population size (Estoup and Clegg 2003). Therefore, in island colonizations of Zosterops, founder events are neither long nor strong, and these features may be typical of bird species that colonize islands in small flocks.
Studies of the radiation of Darwin’s finches in the Galápagos have generated important insight into the evolution of island forms. Within this dynamic system, the opportunity to study effects of colonization was provided by the large ground finch, Geospiza magnirostris, which established a population on Daphne Major in 1982, with founding individuals derived from a number of other Galápagos islands (Grant and Grant 1995a, Grant et al. 2001). Allelic diversity and heterozygosity were tracked across 18 generations following the founding event (Grant et al. 2001) (see table 11.1). Initially, allelic variation decreased by approximately 32%, but this trend was reversed with the continued arrival of breeding immigrants. In contrast, there was no observed initial effect on heterozyosity in the generations immediately following founding, or after input from new immigrants (Grant et al. 2001). This example highlights both the robustness of heterozygosity to population change and the importance of low but continued immigration to island populations.
Similar island-type situations can develop when disjunct populations establish outside of a species range. Hansson et al. (2000) characterized the level of genetic similarity in pairs of great reed warblers, Acrocephalus arundinaceus, which founded a new population in southern Sweden in the late 1970s. They found that, over a period of 8 years, the level of genetic similarity between breeding pairs declined, as measured by microsatellite variation and multilocus DNA fingerprinting. While no comparison with a source population could be made, the temporal increase in genetic variation among individuals suggested that continued immigration into the population lessened the impact of the founder event.
In a final natural example, a small disjunct population of the dark-eyed junco, Junco hyemalis thurberi, established from an estimated seven effective founders in the 1980s outside of its natural range in California (Rasner et al. 2004). This population had significantly lower allelic richness (37% decrease) and to a lesser degree, lower heterozygosity (12% decrease) compared to populations in the natural range (Rasner et al. 2004) (table 11.1). In contrast to the Zosterops and Geospiza examples, both types of diversity measures were significantly affected. The decreased diversity was attributed to the small effective size of the population (32 individuals) averaged over the eight generations since founding (Rasner et al. 2004).
There are only a small number of natural colonization events that have been genetically characterized in birds; however, artificially introduced populations are potentially informative about the genetic effects of population founding. Merilä et al. (1996) summarized isozyme studies of introduced bird species, and concluded that there was “little or no evidence for reduced levels of genetic variability in introduced populations.” However, the inverse relationship between founder population size and genetic diversity was noted. Additional isozyme, minisatellite, and MHC studies of introduced bird populations have likewise reported maintenance of moderate levels of diversity (Ardern et al. 1997, Cabe 1998, Miller and Lambert 2004, Lambert et al. 2005).
Since Merilä et al.’s (1996) summary, studies of introduced bird populations have mostly used microsatellites as the genetic marker of choice (table 11.1). In general, the patterns seen are similar to natural colonizations, although each case also has its own idiosyncrasies. Allelic diversity was often affected, as seen in the ruddy duck introduction to Great Britain (Muñoz-Fuentes et al. 2006), one of the South Island robin introductions (Boessenkool et al. 2007), the house finch introduction to the eastern United States (Hawley et al. 2006), and one of the two wild turkey introductions in Indiana (Latch and Rhodes 2005). However, examples remain where allelic diversity was maintained (South Island saddleback, Taylor and Jamieson [2008]), or only eroded following multiple founder events (Laysan finch; Tarr et al. [1998]). Where heterozygosity was reduced, the extent was much less than for allelic diversity (e.g., house finch; Hawley et al. [2006]). Even multiple founder events often failed to perturb heterozygosity, as seen for the two saddleback subspecies (Lambert et al. 2005, Taylor and Jamieson 2008). Significant genetic divergence can appear quickly due to allele frequency differences, and the case of the North Island saddleback again demonstrates the amplifying effects of sequential bottlenecks in this regard. Three of eight single translocations resulted in significantly positive FST values, and a further three of five populations separated by two translocation events had significant and more pronounced FST values.
A common theme among the avian cases discussed here, whether natural or artificial colonizations, sourced from large outbred populations or small, threatened populations, is that single founder events rarely have a sizable impact on neutral genetic diversity. Loss of rare alleles can result in reduced allelic diversity, and is most evident after sequential founder events. Heterozygosity is not easily perturbed by single or multiple founder events. Shifts in allele frequency differences often result in significant divergence as measured by FST, but it is likely to be only a small fraction of what can accrue more gradually over time.
Multiple mechanisms could account for the generally mild effects on genetic variation noted in avian studies. One consideration is that species translocations often occur for conservation reasons, as exemplified by all but two of the artificial introduction examples (ruddy duck and house finch) in table 11.1. Such species are likely to have experienced reduced population size for some period of time to warrant conservation efforts. Therefore translocated populations, necessarily sourced from already depauperate populations, may not be expected to experience further significant losses of diversity (Taylor and Jamieson 2008). These situations may therefore provide more limited inference for understanding divergence of populations arising from natural colonization events.
In other cases, biological attributes of a species may buffer founded populations from loss of genetic diversity. In two of the documented natural colonizations mentioned above, continued immigration was identified as an important factor resulting in increased population variation (Grant et al. 2001, Hansson et al. 2000). Other studies of established populations note the positive effects of even limited gene flow in bolstering diversity in small populations (Keller et al. 2001, Ortego et al. 2007, Baker et al. 2008). The relatively high vagility of colonizing bird species may therefore limit genetic founder effects. In cases where continued immigration is less likely due to isolation, ample founder sizes may minimize founder effects, as suggested for the recent Zosterops colonizations (Estoup and Clegg 2003). Rapid recovery from small population size is theoretically one of the most important mechanisms to minimize loss of variation (Nei et al. 1975), and empirical results attest to its importance (Estoup and Clegg 2003, Miller and Lambert 2004, Brown et al. 2007). A comparison of MHC variation in two robin species in New Zealand, the Chatham Island black robin (Petroica traversi) and the South Island robin (Petroica australis australis), which both experienced population bottlenecks, found that the former species was monomorphic at MHC loci, whereas the latter species maintained moderate levels of MHC variation (Miller and Lambert 2004). This difference was attributed to the different types of bottlenecks experienced by the two species. The bottleneck in the Chatham Island black robin extended over 100 years of low population size before human-assisted recovery, whereas bottlenecks induced by translocation of South Island robins were short as the populations recovered quickly (Miller and Lambert 2004).
Mild neutral genetic effects of population founding have been reported in other fauna, including numerous mammals (e.g., rabbit [Zenger et al. 2003], brushtail possum [Taylor et al. 2004], ship rat [Abdelkrim et al. 2005], Rodrigues fruit bat [O’Brien et al. 2007], mouflon sheep [Kaeuffer et al. 2007], and Corsican red deer [Hajji et al. 2008]), and amphibians (natterjack toad [Rowe et al. 1998] and marsh frog [Zeisset and Beebee 2003]). As with the bird examples, allelic diversity in these studies was often impacted and heterozygosity less so. The minimal effects of founding were attributed to combinations of substantial numbers of founders, multiple introductions, and rapid recovery times (e.g., Rowe et al. 1998, Zeisset and Beebee 2003, Zenger et al. 2003, Taylor et al. 2004), introduction from an already depauperate source (Hajji et al. 2008), or selection at linked loci (Kaeuffer et al. 2007). In other studies, significant reductions in heterozygosity have indicated a relatively stronger impact of the founding event (e.g., Bennett’s wallabies [Le Page et al. 2000] and Caribbean anoles [Eales et al. 2008]).
In species that are less vagile, tend to colonize in very small numbers, or are less capable of rapid recovery from small population sizes, narrower and longer bottlenecks can amplify the loss of genetic variation and result in severe founder effects. Colonization by a single gravid female represents an extreme case and is a situation that could feasibly occur. Indeed, examples of more sizable neutral genetic impacts of founding have been reported for animals and plants. Severe founder events in introduced Drosophila pseudoobscura population in New Zealand (Reiland et al. 2002), and in an aquatic plant (Butomus umbellatus) invasion to North America (Kliber and Eckert 2005) were explained in part by small numbers of successful founders. Reductions in mitochondrial DNA diversity in introduced bluegill sunfish (Lepomis macrochirus) populations in North America were likewise attributed to a small number of founders in combination with subsequent stochastic processes (Yonekura et al. 2007). The impact of serial founder events may be greater for some species, such as that reported for dice snakes (Natrix tessellata) in Europe (Gautschi et al. 2002).
MacArthur and Wilson did not consider founder effect mechanisms to be of crucial importance in driving divergence of insular forms in general. In birds, empirical assessments of variation at neutral genetic loci in colonized and translocated populations support the conjecture that losses of genetic diversity do not occur on a scale that would precipitate a “genetic revolution.” While inferences from neutral genetic markers do not address loci under selection they can nevertheless be indicative of genome wide perturbations caused by founder effects. Bird colonizations and introductions are generally robust to losses in heterozygosity, suggesting that overall fitness is not compromised by founder events, at least when sourced from outbred populations. With respect to management of endangered, translocated populations, general increases in inbreeding can have important conservation implications (e.g., Jamieson et al. 2006, Hale and Briskie 2007). Losses in allelic diversity are often mild, although the effects of losing a few selectively advantageous alleles could have more serious effects. Allele frequency differences often translate into significant genetic divergence as measured by FST, but far more substantive divergence is likely to accrue over time. In the context of explaining divergence in naturally colonized and successfully established bird populations, an important or prevalent role for founder events as a divergence mechanism remains empirically unsupported.
Given time and isolation, gradual drift can result in divergence without needing to invoke the action of other mechanisms. Despite this, the role that neutral mechanisms play in promoting evolutionary change is often overlooked in favor of adaptive explanations (see Barton 1998, Lynch 2007). Divergence at neutral loci that are not subject to selective pressures illustrates how effective drift can be in gradually increasing levels of divergence in island forms. In contrast, divergence at morphological characters is often assumed to have a selective basis. Few studies have examined whether or not patterns of variation can be explained solely by drift without recourse to selective explanations (but see Lynch 1990, Westerdahl et al. 2004, Renaud et al. 2007).
There are a number of types of data that can be used to assess whether drift is sufficient to explain divergence in island environments. First, the random nature of drift is not expected to produce recurring patterns of morphological change in species that repeatedly colonize islands. Selection has been invoked when repeated patterns are observed, for example, the production of similar ecomorphs in Anoles lizards on Caribbean islands (Losos et al. 1998, this volume) and a tendency for dwarfism in insular sloths (Anderson and Handley 2002). Second, a decoupling of phenotypic and neutral genetic measures of divergence can be interpreted as evidence of selection acting on phenotypic traits (Barrowclough 1983, Spitze 1993, Leinonen et al. 2007, Renaud et al. 2007). In birds, this logic has been applied to reject drift as the sole mechanism of morphological differentiation in a geographically restricted set of song sparrow (Melospiza melodia) subspecies in the San Francisco Bay region (Chan and Arcese 2003), and also, with mixed results, for Atlantic island populations of Berthelot’s pipit (Anthus berthelotii) (Illera et al. 2007). Third, where time frames and effective population sizes are known or can be inferred, the rate at which a shift has occurred can be used to accept or reject drift as a sole mechanism of change (Lande 1976, Turelli et al. 1988, Lynch 1990). Small effective population sizes and low trait heritability can potentially result in large morphological shifts via drift alone (Turelli et al. 1988). If actual effective population sizes exceed the maximum effective population size that would explain the shift by drift alone, then additional microevolutionary mechanisms are required to explain the observed shift. This rationale has been used to reject drift as the sole mechanism of change in a sexually selected plumage trait (Yeh 2004) and morphometric traits (Rasner et al. 2004) in the recently founded Junco population in California discussed previously.
In insular Zosterops, repeated patterns and rates of morphological change imply a role for selection. Zosterops species show a tendency toward increased body size in island representatives (Lack 1971), a recurrent pattern also seen within the Zosterops lateralis species complex (figure 11.3a) (Mees 1969, Clegg et al. 2002b). Morphological shifts towards larger body size or bill size have occurred in most of the recent colonization events by Z. l. lateralis (figure 11.3b). Size increases are not universal however, with one population being significantly smaller in overall size and bill size. Additionally, morphological and genetic measures of differentiation in the recently colonized populations appear decoupled (Clegg et al. 2002b). The magnitude and rate of univariate shifts were often too large, whether toward increased or decreased size, to be accomplished by drift alone, with estimates of effective population sizes frequently too high for a chance mechanism of drift to completely account for the observed shifts (Clegg et al. 2002b). Selection is therefore required to explain morphological change in recently colonized populations. In contrast, rates of change in evolutionarily older Zosterops populations were consistent with a drift-alone mechanism when assuming a consistent rate of change since separation from the ancestor (Clegg et al. 2002b). This is unlikely to represent a difference in divergence mechanism between recently colonized and evolutionarily older forms. Rather, it becomes difficult to reject the null hypothesis of drift when considering divergence over long timescales because selection is unlikely to be consistent in strength or direction and effects are therefore averaged out over time (Kinnison and Hendry 2001). Indeed, divergent selection may be most effective early in the colonization history (Reznick et al. 1997). An alternative model applicable to island-colonizing species experiencing a novel environment is one of rapid displacement driven by directional selection followed by long periods of little change (Lande 1976, Estes and Arnold 2007). This type of model is consistent with divergence of the Capricorn silvereye on Heron Island when comparing patterns of morphological change over millennia, decades, and years (Clegg et al. 2008).
Figure 11.3. Multivariate representation (mean canonical variate (CV) scores summarized from 10 univariate traits) of shifts in morphology for the recently colonized Z. l. lateralis populations compared to the mainland subspecies (ML). A. Body size (CV1). B. Bill size (CV2). Arrows refer to colonization sequence. Location abbreviations as in figure 11.2. Modified from Clegg et al. (2002b).
While drift does have the potential to contribute to morphological diversification, natural selection is often required to explain morphological shifts in birds (Price 2008, chapter 3). Studies of patterns and rates of change, in combination with direct measurement of natural selection currently acting in bird populations (e.g., Grant 1985, Grant and Grant 1995b, Merilä et al. 2001, Grant and Grant 2002, Frentiu et al. 2007) and translocation or common garden studies showing that morphological differences among populations are likely to have a genetic basis (Merilä and Sheldon 2001, Price 2008), point to the importance of natural selection in driving morphological divergence in island bird populations. Other phenotypic characters may have a plastic rather than heritable response to a new environment and it remains important to continue to consider whether adaptive explanations of divergence are necessary for different traits and different organisms.
If we accept the contention that natural selection is a prominent micro-evolutionary process underlying divergence of island birds generally, a second line of questioning relates to how selection acts differently on islands compared to the mainland (MacArthur and Wilson 1967, p. 145). Specifically, do recurring abiotic and biotic features associated with island dwelling result in similar selection pressures across different islands?
There are numerous reasons why selective regimes on islands may systematically differ from the mainland. Island biota may be subject to reduced interspecific competition (Crowell 1962, Diamond 1970, Keast 1970), increased intraspecific competition (MacArthur et al. 1972, Blondel 1985), reduced predator pressure (Schoener and Toft 1983, Michaux et al. 2002, Blumstein 2002), changes in parasite prevalence and diversity, and disease susceptibility (Lindström et al. 2004, Fallon et al. 2005, Matson 2006), and various other shifts in biotic (e.g., resource availability and physical habitat structure; Abbott 1980, Martin 1992, Wu et al. 2006) and abiotic features (e.g., milder environments; Abbott 1980). These differences have been incorporated into adaptive explanations of diversification of island forms. Here I focus on how changes in inter- and intraspecific competition regimes have been used to explain the pattern of increased body size in island-dwelling passerines (Grant 1965, Clegg and Owens 2002) and whether empirical data are consistent with the proposed hypotheses.
One scenario linking competition shifts to body size changes is that reduced interspecific competition results in wider ecological niches and an increase in generalist behavior (Grant 1965, Van Valen 1965, Lack 1969, Carlquist 1974). Large body size, for example, may facilitate an increase in generalist behavior by increasing accessibility to a wider range of resources (Amadon 1953, Grant 1965, Keast 1970, Cody 1974, Grant 1979, Schlotfeldt and Kleindorfer 2006). Empirical support of an association between body size and generalist feeding was demonstrated in seed-eating medium ground finches (Geospiza fortis), where large-billed birds had access to a wider range of seed sizes than small-billed birds (Grant et al. 1976). Directional selection favoring larger forms might therefore be expected when there is an increase in generalist foraging behavior. Scott et al. (2003) outlined three expectations that need to be satisfied for an increase in generalist foraging behavior to provide a general explanation for increased body size in island populations of birds. First, it needs to be established that island populations are more generalist foragers; second, population-level generalist behavior needs to be achieved via individual-level generalist behavior rather than an amalgamation of different types of individual specialists; and finally there should be a positive association between degree of generalist behavior and body size.
The accumulation of studies that have quantified and compared aspects of niche width between island forms and their mainland relatives (e.g., Cox and Ricklefs 1977, Blondel et al. 1988, Carrascal et al. 1994, Scott et al. 2003, Föershler and Kalko 2006, Schlotfeldt and Kleindorfer 2006) support the view that increases in niche width and a shift toward more generalist foraging behavior in island birds is a common phenomenon (Diamond 1970, Keast 1970). The extent to which population-level generalist behavior can be explained by the presence of individual generalists or different types of individual specialists has long been recognized as an important ecological and evolutionary consideration (Van Valen 1965, Roughgarden 1974, Grant et al. 1976, Price 1987). However, few studies of island birds have established how population-level generalist behavior is achieved, most likely because it can be logistically difficult in natural situations to record ecological preferences of individually recognized birds.
Three examples where individual behavior has been quantified in island bird populations are the Capricorn silvereye (Zosterops lateralis chlorocephalus) on Heron Island, Australia (Scott et al. 2003), the Cocos Island finch (Pinoroloxias inornata) on Cocos Island, Costa Rica (Werner and Sherry 1987), and the Darwin’s medium ground finch (Geospiza fortis) on Daphne Major, Galápagos (Grant et al. 1976, Price 1987). Scott et al. (2003) showed that island Zosterops populations are more generalist with respect to foraging height and substrate than their mainland counterparts. However, detailed examination of the Capricorn silvereye on Heron Island revealed that the generalist population was composed of individuals that were more specialized foragers than expected by chance (Scott et al. 2003). The Cocos Island finch was found to be a highly generalist population with respect to foraging methods and this was achieved via individuals using an extremely limited range of resources compared to the population as a whole (Werner and Sherry 1987). In Darwin’s medium ground finch, Price (1987) reported that the population was generalist with respect to use of three seed types, but individuals exhibited some degree of specialization, utilizing only a subset of the seed types available to the population as a whole. The degree to which this occurred was influenced by food availability with more specialist individuals present when food was short (Price 1987).
The degree to which there was a positive relationship between generalist behavior and morphological size varied across the three studies. Capricorn silvereyes showed no relationship between morphology and degree of foraging generalization (Scott et al. 2003). Likewise, individual Cocos Island finches showed no relationship between morphology (or sex or age) and foraging behavior (Werner and Sherry 1987). In contrast, a relationship between morphology and foraging in Darwin’s medium ground finch was observed. Individuals with significantly larger bills utilized large and hard seeds that were unavailable to smaller-billed individuals, thereby displaying a positive association between a morphological character and one aspect of niche width (Grant et al. 1976, Price 1987). In this species, seeds are the predominant food source and are particularly relied upon when environmental conditions deteriorate (Price 1987). Grant et al. (1976) found no such relationship between bill size of medium ground finches and another, more easily accessed resource, Bursera berries. The relationship between morphology and foraging may be more likely to occur in cases where access to the food item is very tightly restricted by physical capabilities of the feeding apparatus. Such strong associations between bill size and resource have been reported in other seed-eaters, e.g., Pyrenestes finches in Africa (Smith 1987).
Of the limited examples available to examine individual niche width in island birds, each is a generalist population made up to some degree of individual specialists (with respect to all food types for the Capricorn silvereye and Cocos Island finch, or seed types for Darwin’s medium ground finch). Further empirical results for island populations are required before generalizations are made; however, Werner and Sherry (1987) point out that the conditions under which individual specialization is likely to arise, including high food availability, variety, and predictability, high population density, low interspecific competition, and low territoriality, are often met on oceanic islands. More broadly, generalist populations made up of individual specialists may be more common than previously appreciated (Bolnick et al. 2007). In the cases presented here, there is variation in the degree of individual specialization, being more pronounced in the case of the Cocos Island finch than the other two examples, or when food availability decreases in the case of the medium ground finch. A link between foraging characteristics and morphology was found for the medium ground finch only. The idea that an increase in generalist behavior favors selection for a large generalist form is not consistent with the occurrence of individual specialists, and the lack of morphological association with generalist foraging behavior in two of the three cases. While changes in interspecific competition regimes may influence body size evolution of island birds in other ways, direct links between reduced interspecific competition, increased generalist behavior, and selection for a generalist (large) body type are not strongly supported by the limited empirical evidence available.
A second scenario linking competition shifts to body size changes centers on the effects of increased intraspecific competition. Population density increases within a species are often a feature of island populations (MacArthur et al. 1972). This phenomenon has been observed in a range of taxa, including birds (Crowell 1962, Kikkawa 1976, Thiollay 1993, George 1987, Blondel et al. 1988), mammals (Adler and Levins 1994, Goltsman et al. 2005), and herpetofauna (Rodda and Dean-Bradley 2002, Buckley and Jetz 2007, Wu et al. 2006). Population density increases plausibly lead to increased intraspecific competition. In birds an increase in agonistic encounters can often occur (Stamps and Buechner 1985) and, in such a situation, some have proposed that selection should favor traits that provide an advantage in agonistic interactions, the outcome of which may ultimately affect survival or fecundity (Kikkawa 1980, Robinson-Wolrath and Owens 2003). One such potentially favorable factor is increased body size. At the interspecific level, the relationship between body size and the order of dominance or aggressive superiority has been demonstrated (e.g., Piper and Catterall 2003, Rychlik and Zwolak 2006). Within species, the relationship between body size and aggressive behavior is less clear; for example, aggression in bluebirds is not related to body size (Duckworth 2006). However, in the Capricorn silvereye on Heron Island, a study of agonistic encounters within juveniles during a single over-winter period found a significant positive relationship between body size and proportion of aggressive encounters won (Robinson-Wolrath and Owens 2003). The addition of data taken across a three-year period on birds of all ages showed that, after taking into account the strong effects of age and sex, where males and adults win more often, body size remains a significant predictor of the outcome of aggressive interaction (Clegg and Owens, unpublished). Such individual variation in aggression and morphology could be an important target of selection in this population. Whether or not selection for large aggressive individuals is a general phenomenon in densely populated insular settings remains to be seen.
Concentrating on the role of either intra- or interspecific competition may help to identify the direct selective mechanism producing a morphological pattern. In the examples presented here, reduced interspecific competition is unlikely to be a direct cause of increased body size in small island birds via a feeding generalization mechanism, whereas increased intraspecific competition may have more direct selective effects on body size via behavioral mechanisms. However, it is the shift in balance between inter- and intraspecific competition, where reduced interspecific competition facilitates increased intraspecific competition, that may be at the base of a sequence of changes that occur on islands and ultimately result in morphological changes. Further, the relationships between body size, niche width, and aggressive tendencies discussed here are unlikely to operate in isolation from other insular features of changes in predation, parasites, and other abiotic and biotic differences. Additionally, changes in sexual rather than natural selection regimes offer an alternative explanation for large body size. If strong genetic correlations exist between the sexes, then sexual selection for large male body size may drive larger size overall (Price 1984, Merilä et al. 1998). The interplay among these factors awaits further empirical investigations.
Drift and natural selection are two of the microevolutionary processes that can cause divergence in island forms. Population genetic studies of naturally colonized and introduced island bird populations demonstrate that drift during the founding event often does not have severe consequences for diversity and divergence. Sequentially founded populations are more susceptible to cumulative effects of founder-mediated drift, but, even then, loss of diversity can be surprisingly mild. As development of molecular markers continues, future studies will have the opportunity to address loci under selection and to track the impact of founding events on selectively advantageous alleles. Drift, either during founding or over longer time frames, can conceivably contribute to morphological divergence. Situations of extreme isolation due to geographic distance or dispersal limitations will provide greater opportunity for drift to be an effective mechanism. However, evidence of patterns and magnitudes of morphological differentiation suggests that natural selection is a relatively more important microevolutionary process than neutral mechanisms, and may be particularly important in generating divergence in the early stages of colonization history. Common biotic and abiotic factors associated with insularity could produce congruent selection regimes on islands. The extent to which this produces general patterns of diversification and the particular selective pressure responsible requires more case studies. In particular, more studies at the individual level would be valuable for understanding the interplay among different selection pressures, and which may be of more direct influence in producing evolutionary change in island birds.
I thank Ian Owens, Jiro Kikkawa, Craig Moritz, Sandie Degnan, Susan Scott, and Sarah Robinson-Wolrath for discussions on topics presented in this chapter and Robert Ricklefs, Jonathan Losos, Peter Grant, Albert Phillimore, Jessica Worthington Wilmer, and an anonymous reviewer for helpful comments on the manuscript.
Abbott, I. 1980. Theories dealing with the ecology of landbirds on islands. Advances in Ecological Research 11:329–71.
Abdelkrim, J., M. Pascal, and S. Samadi. 2005. Island colonization and founder effects: The invasion of the Guadeloupe islands by ship rats (Rattus rattus). Molecular Ecology 14:2923–31.
Adler, G. H., and R. Levins. 1994. The island syndrome in rodent populations. Quarterly Review of Biology 69:473–90.
Amadon, D. 1953. Avian systematics and the evolution in the Gulf of Guinea. Bulletin of the American Museum of Natural History 100:393–452.
Anderson, R. P., and C. O. Handley, Jr. 2002. Dwarfism in insular sloths: Biogeography, selection and evolutionary rate. Evolution 56:1045–58.
Ardern, S. L., D. M. Lambert, A. G. Rodrigo, and I. G McLean. 1997. The effects of population bottlenecks on multilocus DNA variation in robins. Journal of Heredity 88:179–86.
Baker, M. C., M.S.A. Baker, and L. M. Tilghman. 2006. Differing effects of isolation on evolution of birds songs: Examples from an island-mainland comparison of three species. Biological Journal of the Linnean Society 89:331–42.
Baker, A. J., A. D. Greenslade, L. M. Darling, and J. C. Finlay. 2008. High genetic diversity in the blue-listed British Columbia population of the purple martin maintained by multiple sources of immigrants. Conservation Genetics 9:495–505.
Balloux, F., W. Amos, and T. Coulson. 2004. Does heterozygosity estimate inbreeding in real populations? Molecular Ecology 13:3021–31.
Barrowclough, G. F. 1983. Biochemical studies of microevolutionary processes. In Perspectives in Ornithology, ed. A. H. Brush and J.G.A. Clark, 223–61. New York: Cambridge University Press.
Barton, N. H., and B. Charlesworth. 1984. Genetic revolutions, founder effects and speciation. Annual Review of Ecology and Systematics 15:133–64.
Barton, N. H. 1998. Natural selection and random genetic drift as causes of evolution on islands. In Evolution on Islands, ed. P. R. Grant, 102–23. Oxford: Oxford University Press.
Berry, R. J. 1998. Evolution of small mammals. In Evolution on Islands, ed. P. R. Grant, 35–50. Oxford: Oxford University Press.
Blondel, J. 1985. Habitat selection in island versus mainland birds. In Habitat Selection in Birds, ed. M. Cody, 477–516. Orlando, FL: Academic Press.
Blondel, J., D. Chessel, and B. Frochot. 1988. Bird species impoverishment, niche expansion and density inflation in Mediterranean island habitats. Ecology 69:1899–917.
Blumstein, D. 2002. Moving to suburbia: Ontogenetic and evolutionary consequences of life on predator-free islands. Journal of Biogeography 29:685–92.
Boessenkool, S., S. S. Taylor, C. K. Tepolt, J. Komdeur, and I. G. Jamieson. 2007. Large mainland populations of South Island robins retain greater genetic diversity than offshore island refuges. Conservation Genetics 8:705–14.
Bollmer, J. L., N. K. Whiteman, M. D. Cannon, J. C. Bednarz, T. De Vries, and P. G. Parker. 2005. Population genetics of the Galapagos hawk (Buteo galapagoensis): genetic monomorphism within isolated populations. Auk 122:1210–24.
Bollmer, J. L., F. Hernán Vargas, and P. G. Parker. 2007. Low MHC variation in the endangered Galápagos penguin (Spheniscus mendiculus). Immunogenetics 59:593–602.
Bolnick, D. I. R. Svanbäck, M. S. Araujo, and L. Persson. 2007. Comparative support for the niche variation hypothesis that more generalized populations also are more heterogeneous. Proceedings of the National Academy of Sciences U.S.A. 104:10075–79.
Brown, J. W, P. J. Van Coeverden de Groot, T. P. Birt, G. Seiutin, P. T. Boag, and V. L. Friesen. 2007. Appraisal of the consequences of the DDT-induced bottleneck on the level and geographic distribution of neutral genetic variation in Canadian peregrine falcons, Falco peregrinus. Molecular Ecology 16:327–43.
Buckley, L. B., and W. Jetz. 2007. Insularity and the determinants of lizard population density. Ecology Letters 10:481–89.
Cabe, P. R. 1998. The effects of founding bottlenecks on genetic variation in the European starling (Sturnus vulgaris) in North America. Heredity 80:519–25.
Carlquist, S. 1974. Island Biology. New York: Columbia University Press.
Carrascal, L. M., E. Moreno, and A. Valido. 1994. Morphological evolution and changes in foraging behaviour of island and mainland populations of Blue Tit (Parus caeruleus)—a test of convergence and ecomorphological hypotheses. Evolutionary Ecology 8:25–35.
Carson, H. L., and A. R. Templeton. 1984. Genetic revolutions in relation to speciation phenomena: the founding of new populations. Annual Review of Ecology and Systematics 15:97–131.
Chan, Y., and P. Arcese. 2003. Morphological and microsatellite differentiation in Melopsiza melodia (Aves) at a microgeographic scale. Journal of Evolutionary Biology 16:939–47.
Clegg, S. M., S. M. Degnan, J. Kikkawa, C. Moritz, A. Estoup and I. P. F. Owens. 2002a. Genetic consequences of sequential founding events by and island-colonizing bird. Proceedings of the National Academy of Sciences U.S.A. 99:8127–32.
Clegg, S. M., S. M. Degnan, C. Moritz, A. Estoup, J. Kikkawa, and I. P. F. Owens. 2002b. Microevolution in island forms: the roles of drift and directional selection in morphological divergence of a passerine bird. Evolution 56:2090–99.
Clegg, S. M., D. F. Frentiu, J. Kikkawa, G. Tavecchia, and I. P. F. Owens. 2008. 4000 years of phenotypic change in an island bird: heterogeneity of selection over three microevolutionary timescales. Evolution 62:2393–410.
Clegg, S. M., and I.P.F. Owens. 2002. The ‘island-rule’ in birds: medium body size and its ecological explanation. Proceedings of the Royal Society of London, Series B 269:1359–65.
Cody, M. 1974. Competition and the Structure of Bird Communities. Princeton, NJ: Princeton University Press.
Coltman, D., and J. Slate. 2003. Microsatellite measures of inbreeding: A meta-analysis. Evolution 57:971–83.
Cox, G. W., and R. E. Ricklefs. 1977. Species diversity and ecological release in Caribbean land bird faunas. Oikos 28:113–22.
Coyne, J. A., and H. A. Orr. 2004. Speciation. Sunderland, MA: Sinauer Associates.
Crowell, K. 1962. Reduced interspecific competition among the birds of Bermuda. Ecology 43:75–88.
Degnan, S. M., and C. Moritz. 1992. Phylogeography of mitochondrial DNA in two species of white-eyes in Australia. Auk 109:800–811.
Diamond, J. M. 1970. Ecological consequences of island colonization by Southwest Pacific Birds, I: Types of niche shifts. Proceedings of the National Academy of Sciences U.S.A. 67:529–36.
Duckworth, R. 2006. Aggressive behaviour affects selection on morphology by influencing settlement patterns in a passerine bird. Proceedings of the Royal Society of London, Series B 273:1789–95.
Eales, J., R. S. Thorpe, and A. Malhotra. 2008. Weak founder effect signal in a recent introduction of Caribbean Anolis. Molecular Ecology 17:1416–26.
Estes, S., and S. J. Arnold. 2007. Resolving the paradox of stasis: Models with stabilizing selection explain evolutionary divergence on all timescales. Evolution 169:227–44.
Estoup, A., and S. M. Clegg. 2003. Bayesian inferences on the recent island colonization history by the bird Zosterops lateralis lateralis. Molecular Ecology 12:657–74.
Fallon, S. M., E. Bermingham, and R. E. Ricklefs. 2005. Host specialization and geographic localization of avian malaria parasites: a regional analysis in the Lesser Antilles. American Naturalist 165:466–80.
Förschler, M. I., and E.K.V. Kalko. 2006. Breeding ecology and nest site selection in allopatric mainland Citril finches Carduelis [citrinella] citrinella and insular Corsican finches Carduelis [citrinella] corsicanus. Journal of Ornithology 147:553–64.
Frankham, R. 1997. Do island populations have less genetic variation than mainland populations? Heredity 78:311–27.
Frentiu, F. D., S. M Clegg, M. W. Blows, and I. P. F. Owens. 2007. Large body size in an island-dwelling bird: a microevolutionary analysis. Journal of Evolutionary Biology 20:639–49.
Gautschi, B., A. Widmer, J. Joshi, and J. C. Koella. 2002. Increased frequency of scale anomalies and loss of genetic variation in serially bottlenecked populations of dice snake, Natrix tessellata. Conservation Genetics 3:235–45.
George, T. L. 1987. Greater land bird densities on island vs. mainland: relation to nest predation level. Ecology 68:1393–1400.
Goltsman, M., E. P. Kruchenkova, S. Sergeev, I. Velodin, and D. W. Macdonald. 2005. ‘Island syndrome’ in a population of Arctic foxes (Alopex lagopus) from Mednyi Island. Journal of Zoology 267:40–18.
Grant, B. R. 1985. Selection on bill characteristics in a population of Darwin’s finches: Geospiza conirostris on Isla Genovesa, Galápagos. Evolution 39:523–32.
Grant, P. R. 1965. The adaptive significance of some size trends in island birds. Evolution 19:355–67.
———. 1979. Ecological and morphological variation of Canary Island blue tits, Parus caeruleus (Aves: Paridae). Biological Journal of the Linnean Society 11:103–29.
——— 1998. Speciation. In Evolution on Islands, ed. P. R. Grant, 83–101. Oxford: Oxford University Press.
——— 2001. Reconstructing the evolution of birds on islands: 100 years of research. Oikos 92:385–403.
Grant, P. R., and B. R. Grant. 1995a. The founding of a new population of Darwin’s finches. Evolution 49:229–40.
———. 1995b. Predicting microevolutionary responses to directional selection on heritable variation. Evolution 49:241–51.
———. 2002. Unpredictable evolution in a 30-year study of Darwin’s finches. Science 296:707–11.
Grant, P. R., B. R. Grant, and K. Petren. 2001. A population founded by a single pair of individuals: establishment, expansion, and evolution. Genetica 112–13:359–82.
Grant, P. R., B. R. Grant, J.N.M. Smith, I. J. Abbott, and L. K. Abbott. 1976. Darwin’s finches: Population variation and natural selection. Proceedings of the National Academy of Sciences U.S.A. 73:257–61.
Hailer, F., B. Helander, A. O. Folkestad, S. A. Ganusevich, S. Garstad, P. Hauff, C. Koren, T. Nygård, V. Volke, C. Vilá, and H. Ellegren. 2006. Bottlenecked but long-lived: High genetic diversity retained in white-tailed eagles upon recovery from population decline. Biology Letters 2:316–19.
Hajji, G. M., F. Charfi-Cheikrouha, R. Lorenzini, J-D. Vigne, G. B Hartl, and F. E. Zachos. 2008. Phylogeography and founder effect of the endangered Corsican red deer (Cervus elaphus corsicanus). Biodiversity and Conservation 17:659–73.
Hale, K. A., and J. V. Briskie. 2007. Decreased immunocompetence in a severely bottlenecked population of an endemic New Zealand bird. Animal Conservation 10:2–10.
Hansson, B., S. Bensch, D. Hasselquist, B-G. Lillandt, L. Wennerberg, and T. Von Schantz. 2000. Increase of genetic variation over time in a recently founded population of great reed warblers (Acrocephalus arundinaceus) revealed by microsatellites and DNA fingerprinting. Molecular Ecology 9:1529–38.
Hansson, B., H. Westerdahl, D. Hasselquist, M. Åkesson, and S. Bensch. 2004. Does linkage disequilibrium generate heterozygosity-fitness correlations in great reed warblers? Evolution 58:870–79.
Hawley, D. M., J. Briggs, A. A. Dhondt, and I. J. Lovette. 2008. Reconciling molecular signatures across markers: mitochondrial DNA confirms founder effect in invasive North American house finches (Carpodacus mexicanus). Conservation Genetics 9:637–43.
Hawley, D. M., D. Hanley, A. A. Dhondt, and I. J. Lovette. 2006. Molecular evidence of a founder effect in invasive house finch (Carpodacus mexicanus) populations experiencing an emergent disease epidemic. Molecular Ecology 15:263–75.
Hopley, D. 1982. The Geomorphology of the Great Barrier Reef: Quaternary Development of Coral Reefs. New York: John Wiley and Sons.
Illera, J. C., B. C. Emerson, and D. S. Richardson. 2007. Population history of Berthelot’s pipit: colonization, gene flow and morphological divergence in Macaronesia. Molecular Ecology 16:4599–612.
Jamieson, I. G., G. P. Wallis, and J. V Briskie. 2006. Inbreeding and endangered species management: Is New Zealand out of step with the rest of the world? Conservation Biology 20:38–47.
Kaeuffer, R., D. W. Coltman, J-L. Chapuis, D. Pontier, and D. Réale. 2007. Unexpected heterozygosity in an island mouflon population founded by a single pair of individuals. Proceedings of the Royal Society of London, Series B 274:527–33.
Keast, A. 1970. Adaptive evolution and shifts in niche occupation in island birds. Biotropica 2:61–75.
Keller, L. F., K. J. Jeffery, P. Arcese, M. A. Beaumont, W. M. Hochachka, J. N. M. Smith, and M W. Bruford. 2001. Immigration and the ephemerality of a natural population bottleneck: Evidence from molecular markers. Proceedings of the Royal Society of London, Series B 268:1387–94.
Kikkawa, J. 1976. The birds of the Great Barrier Reef. In Biology and Geology of Coral Reefs, ed. O. A. Jones and R. Endean, 279–341. New York: Academic Press.
———. 1980. Winter survival in relation to dominance classes among silvereyes Zosterops lateralis chlorocephala of Heron Island, Great Barrier Reef. Ibis 122:437–46.
Kinnison, M. T., and A. P. Hendry. 2001. The pace of modern life II: From rates of contemporary microevolution to pattern and process. Genetica 112-113:145–64.
Kliber, A., and C. G. Eckert. 2005. Interaction between founder effect and selection during biological invasion in an aquatic plant. Evolution 59:1900–1913.
Lack, D. 1969. The number of bird species on islands. Bird Study 16:193–209.
———. 1971. Ecological Isolation in Birds. Oxford: Blackwell Scientific Publications.
Lambert, D. M., T. King, L. D. Shepherd, A. Livingston, S. Anderson, and J. L. Craig. 2005. Serial population bottlenecks and genetic variation: translocated populations of the New Zealand Saddleback (Philesturnus carunculatus rufaster). Conservation Genetics 6:1–14.
Lande, R. 1976. Natural selection and random genetic drift in phenotypic evolution. Evolution 30:314–34.
———. 1980. Genetic variation and phenotypic evolution during allopatric speciation. American Naturalist 116:463–79.
Latch, E. K., and O. E. Rhodes, Jr. 2005. The effects of gene flow and population isolation on the genetic structure of reintroduced wild turkey populations: Are genetic signatures of source populations retained? Conservation Genetics 6:981–97.
Le Corre, V., and A. Kremer. 1998. Cumulative effects of founding events during colonization on genetic diversity and differentiation in an island and stepping-stone model. Journal of Evolutionary Biology 11:495–512.
Le Gouar, P., F. Rigal, M. C. Boisselier-Dubayle, F. Sarrazin, C. Arthur, J. P. Chlisy, O. Hatzofe, S. Henriquet, P. Lécuyer, C. Tessier, G. Susie, and S. Samadi. 2008. Genetic variation in a network of natural and reintroduced populations of Griffon vulture (Gyps fulvus) in Europe. Conservation Genetics 9:349–59.
Le Page, S. L., R. A. Livermore, D. W. Cooper, and A. C. Taylor. 2000. Genetic analysis of a documented population bottleneck: Introduced Bennett’s wallabies (Macropus rufogriseus rufogriseus) in New Zealand. Molecular Ecology 9:753–63.
Leinonen, T., R. B. O’Hara, J. M. Cano, and J. Merilä. 2007. Comparative studies of quantitative trait and neutral marker divergence: A meta-analysis. Journal of Evolutionary Biology 21:1–17.
Lindström, K. M., J. Foufopoulos, H. Pärn, and M. Wikelski. 2004. Immunological investments reflect parasite abundance in island populations of Darwin’s finches. Proceedings of the Royal Society of London, Series B 271:1513–19.
Losos, J. B. T. R. Jackman, A. Larson, K. De Queiroz, and L. Rodriguez-Schettino. 1998. Contingency and determinism in replicated adaptive radiations of island lizards. Science 279:2115–17.
Lynch, M. 1990. The rate of morphological evolution in mammals from the standpoint of the neutral expectation. American Naturalist 136:727–41.
———. 2007. The frailty of adaptive hypotheses for the origins of organismal complexity. Proceedings of the National Academy of Sciences U.S.A. 104:8597–604.
MacArthur, R. H., J. M. Diamond, and J. R. Karr. 1972. Density compensation in island faunas. Ecology 53:330–42.
MacArthur, R. H., and E. O. Wilson. 1967. The Theory of Island Biogeography. Princeton, NJ: Princeton University Press.
Martin, J-L. 1992. Niche expansion in an insular bird community: An autecological perspective. Journal of Biogeography 19:375–81.
Matson, K. D. 2006. Are there differences in immune function between continental and insular birds? Proceedings of the Royal Society of London, Series B 273:2267–74.
Mayr, E. 1942. Systematics and the Origin of Species. New York: Colombia University Press.
———. 1954. Changes of genetic environment and evolution. In Evolution as a Process, ed. J. Huxley, A. C. Hardy, and E. B. Ford, 157–80. London: Allen and Unwin.
Mees, G. F. 1969. A systematic review of the Indo-Australian Zosteropidae (Part III). Zoologische Verhandelingen 102:1–390.
Merilä, J., M. Björklund, and A. J. Baker. 1996. The successful founder: genetics of introduced Carduelis chloris (greenfinch) populations in New Zealand. Heredity 77:410–22.
Merilä, J., L.E.B. Kruuk, and B. C. Sheldon. 2001. Natural selection on the genetical component of variance in body condition in a wild bird population. Journal of Evolutionary Biology 14:918–29.
Merilä, J., and B. C. Sheldon. 2001. Avian quantitative genetics. In Current Ornithology, ed. V. Nolan and C. F. Thompson, 179–255. New York: Kluwer.
Merilä, J., B. C. Sheldon, and H. Ellegren. 1998. Quantitative genetics of sexual size dimorphism in the collared flycatcher, Ficedula albicollis, Evolution 52:870–76.
Michaux, J. R., J. G. de Bellocq, M. Sarà, and S. Morand. 2002. Body size increases in insular rodent populations: A role for predators? Global Ecology and Biogeography 11:427–36.
Miller, H. C., and D. M. Lambert. 2004. Genetic drift outweighs balancing selection in shaping post-bottleneck major histocompatibility complex variation in New Zealand robins (Petroicidae). Molecular Ecology 13:3709–21.
Mock, K. E., E. K. Latch, and O. E. Rhodes, Jr. 2004. Assessing losses of genetic diversity due to translocation: long-term case histories in Merriam’s turkey (Meleagris gallopavo merriami). Conservation Genetics 5:631–45.
Motro, U., and G. Thomson. 1982. On heterozygosity and the effective size of populations subject to size changes. Evolution 36:1059–66.
Muñoz-Fuentes, V., A. J. Green, M. D. Sorenson, J. J. Negro, and C. Vilá. 2006. The ruddy duck Oxyura jamaicensis in Europe: Natural colonization or human introduction? Molecular Ecology 15:1441–53.
Mundy, N. I., C. S. Winchell, T. Burr, and D. S. Woodruff. 1997. Microsatellite variation and microevolution in the critically endangered San Clemente Island loggerhead shrike (Lanius ludovicianus mearnsi). Proceedings of the Royal Society of London, Ser. B 264:869–75.
Nei, M., T. Maruyama, and R. Chakraborty. 1975. The bottleneck effect and genetic variability in populations. Evolution 29:1–10.
O’Brien, J., G. F. McCracken, L. Say, and T. J. Hayden. 2007. Rodrigues fruit bats (Pteropus rodricensis, Megachiroptera: Pteropodidae) retain genetic diversity despite population declines and founder events. Conservation Genetics 8:1073–82.
Ohnishi, N. T. Saitoh, Y. Ishibashi, and T. Oi. 2007. Low genetic diversities in isolated populations of the Asian black bear (Ursus thibetanus) in Japan, in comparison with large stable populations. Conservation Genetics 8:1331–37.
Ortego, J., J. M. Aparicio, G. Calbuig, and P. J. Cordero. 2007. Increase of heterozygosity in a growing population of lesser kestrels. Biology Letters 3:585–88.
Pastor, T., J. C. Garza, P. Allen, W. Amos, and A. Aguilar. 2004. Low genetic variability in the highly endangered Mediterranean monk seal. Journal of Heredity 95:291–300.
Phillimore, A. B. 2006. The ecological basis of speciation and divergence in birds. Ph.D. dissertation, Department of Biological Sciences, Imperial College, London.
Piper, S. D., and C. P. Catterall. 2003. A particular case and a general pattern: hyperaggressive behaviour by one species may mediate avifaunal decreases in fragmented Australian forests. Oikos 101:602–14.
Price, T. 1984. The evolution of sexual size dimorphism in Darwin’s finches (Geospiza fortis). American Naturalist 123:500–518.
———. 1987. Diet variation in a population of Darwin’s finches. Ecology 68:1015–28.
———. 2008. Speciation in Birds. Westview Village, CO: Roberts and Company.
Provine, W. B. 1989. Founder effects and genetic revolutions in microevolution and speciation: An historical perspective. In Genetics, Speciation and the Founder Principle, ed. L. V. Giddings, K. Y. Kaneshiro, and W. W. Anderson, 43–76. New York: Oxford University Press.
Pruett, C. L., and K. Winker. 2005. Northwestern song sparrow populations show genetic effects of sequential colonization. Molecular Ecology 14:1421–34.
Rasner, C. A., P. Yeh, L. S. Eggert, K. E. Hunt, D. S. Woodruff, and T. D. Price. 2004. Genetic and morphological evolution following a founder event in the dark-eyed junco, Junco hyemalis thurberi. Molecular Ecology 13:671–81.
Reiland, U., S. Hodge, and M. A. F. Noor. 2002. Strong founder effect in Drosophila pseudoobscura colonizing New Zealand from North America. Journal of Heredity 93:415–20.
Renaud, S., P. Chevret, and J. Michaux. 2007. Morphological vs. molecular evolution: ecology and phylogeny both shape the mandible of rodents. Zoologica Scripta 35:525–35.
Reznick, D. N., F. H. Shaw, F. H. Rodd, and R. G. Shaw. 1997. Evaluation of the rate of evolution in natural populations of guppies (Poecilia reticulata). Science 275:1934–37.
Rice, W., and E. Hostert. 1993. Laboratory experiments on speciation: What have we learned in 40 years? Evolution 47:1637–53.
Robinson-Wolrath, S. I., and I. P. F. Owens. 2003. Large size in an island-dwelling bird: intraspecific competition and the Dominance Hypothesis. Journal of Evolutionary Biology 16:1106–14.
Rodda, G. H., and Dean-Bradley K. 2002. Excess density compensation in island herpetofaunal assemblages. Journal of Biogeography 29:623–32.
Roques, S., and J. J. Negro. 2005. MtDNA genetic diversity and population history of a dwindling raptorial bird, the red kite (Milvus milvus). Biological Conservation 126:41–50.
Roughgarden, J. 1974. Niche width: biogeographic patterns among Anolis lizard populations. American Naturalist 108:429–42.
Rowe, G., T. J. C. Beebee, and T. Burke. 1998. Phylogeography of the natterjack toad Bufo calamita in Britain: Genetic differentiation of native and translocated populations. Molecular Ecology 7:751–60.
Rychlik, L., and R. Zwolak. 2006. Interspecific aggression and behavioural dominance among four sympatric species of shrews. Canadian Journal of Zoology 84:434–48.
Schlotfeldt, B. E., and S. Kleindorfer. 2006. Adaptive divergence in the Superb Fairy-wren (Malurus cyaneus): A mainland versus island comparison of morphology and foraging behaviour. Emu 106:309–19.
Schoener, T. W., and C. A. Toft. 1983. Spider populations: Extraordinarily high densities on islands without top predators. Science 219:1353–55.
Scott, S. N., S. M Clegg, S. P. Blomberg, J. Kikkawa, and I. P. F. Owens. 2003. Morphological shifts in island-dwelling birds: The roles of generalist foraging and niche expansion. Evolution 57:2147–56.
Seutin, G., J. Brawn, R. E. Ricklefs, and E. Bermingham. 1993. Genetic divergence among populations of a tropical passerine, the streaked saltator (Saltator albicollis). Auk 110:117–26.
Slatkin, M. 1996. In defense of founder-flush theories of speciation. American Naturalist 147:493–505.
Smith, T. B. 1987. Bill size polymorphism and intraspecific niche utilization in an African finch. Nature 329:717–19.
Spitze, K. 1993. Population structure in Daphnia obtusa: Quantitative genetic and allozymic variation. Genetics 135:367–74.
Stamps, J. A., and Buechner. 1985. The territorial defense hypothesis and the ecology of insular vertebrates. Quarterly Review of Biology 60:155–81.
Tarr, C. L., S. Conant, and R. C. Fleischer. 1998. Founder events and variation at microsatellite loci in an insular passerine bird, the Laysan finch (Telespiza cantans). Molecular Ecology 7:719–31.
Taylor, A. C., P. E. Cowan, B. L. Fricke, S. Geddes, B. D. Hansen, M. Lam, and D. W. Cooper. 2004. High microsatellite diversity and differential structuring among populations of the introduced common brushtail possum, Trichosurus vulpecula, in New Zealand. Genetical Research 83:101–11.
Taylor, S. S., and I. G. Jamieson. 2008. No evidence for loss of genetic variation following sequential translocations in extant populations of a genetically depauperate species. Molecular Ecology 17:545–56.
Templeton, A. R. 1996. Experimental evidence for the genetic-transilience model of speciation. Evolution 50:909–15.
———. 2008. The reality and importance of founder speciation in evolution. Bioessays 30:470–79.
Thiollay, J-M. 1993. Habitat segregation and the insular syndrome in two congeneric raptors in New Caledonia, the White-bellied Goshawk Accipter haplochrous and the Brown Goshawk A. fasciatus. Ibis 135:237–46.
Turelli, M., J. H. Gillespie, and R. Lande. 1988. Rate tests for selection on quantitative characters during macroevolution and microevolution. Evolution 42:1085–89.
Van Valen, L. 1965. Morphological variation and width of the ecological niche. American Naturalist 99:377–90.
Walsh, H. E., I. L. Jones, and V. L. Friesen. 2005. A test of founder effect speciation using multiple loci in the Auklets (Aethia spp.). Genetics 171:1885–94.
Weber, D. S., B. S. Stewart, and N. Lehman. 2004. Genetic consequences of a severe population bottleneck in the Guadalupe fur seal (Arctocephalus townsendi). Journal of Heredity 95:144–53.
Werner, T. K., and T. W. Sherry. 1987. Behavioral feeding specialization in Pinarolaxias inornata, the “Darwin’s Finch” of the Cocos Island, Costa Rica. Proceedings of the National Academy of Sciences U.S.A. 84:5506–10.
Westerdahl, H., B. Hansson, S. Bensch, and D. Hasselquist. 2004. Between-year variation of MHC allele frequencies in great reed warblers: selection or drift? Journal of Evolutionary Biology 17:485–92.
Wright, S. 1931. Evolution in Mendelian populations. Genetics 16:97–159.
Wu, Z, Y. Li, and B. R. Murray. 2006. Insular shifts in body size of rice frogs in the Zhoushan Archipelago, China. Journal of Animal Ecology 75:1071–80.
Yeh, P. J. 2004. Rapid evolution of a sexually selected trait following population establishment in a novel habitat. Evolution 58:166–74.
Yonekura, R., K. Kawamura, and K. Uchii. 2007. A peculiar relationship between genetic diversity and adaptability in invasive exotic species: Bluegill sunfish as a model species. Ecological Research 22:911–19.
Zeisset, I., and T. J. C. Beebee. 2003. Population genetics of a successful invader: The marsh frog Rana ridibunda in Britain. Molecular Ecology 12:639–46.
Zenger, K. R., B. J. Richardson and A-M. Vachot-Griffin. 2003. A rapid population expansion retains genetic diversity within European rabbits in Australia. Molecular Ecology 12:789–94.
