Ian G. Jamieson

Multimodel inference in ecology and evolution: challenges and solutions

Information theoretic approaches and model averaging are increasing in popularity, but this approach can be difficult to apply to the realistic, complex models that typify many ecological and evolutionary analyses. This is especially true for those researchers without a formal background in information theory. Here, we highlight a number of practical obstacles to model averaging complex models. Although not meant to be an exhaustive review, we identify several important issues with tentative solutions where they exist (e.g. dealing with collinearity amongst predictors; how to compute model‐averaged parameters) and highlight areas for future research where solutions are not clear (e.g. when to use random intercepts or slopes; which information criteria to use when random factors are involved). We also provide a worked example of a mixed model analysis of inbreeding depression in a wild population. By providing an overview of these issues, we hope that this approach will become more accessible to those investigating any process where multiple variables impact an evolutionary or ecological response.

Disentangling the roles of natural selection and genetic drift in shaping variation at MHC immunity genes

The major histocompatibility complex (MHC) forms an integral component of the vertebrate immune response and, due to strong selection pressures, is one of the most polymorphic regions of the entire genome. Despite over 15 years of research, empirical studies offer highly contradictory explanations of the relative roles of different evolutionary forces, selection and genetic drift, acting on MHC genes during population bottlenecks. Here, we take a meta‐analytical approach to quantify the results of studies into the effects of bottlenecks on MHC polymorphism. We show that the consequences of selection acting on MHC loci prior to a bottleneck event, combined with drift during the bottleneck, will result in overall loss of MHC polymorphism that is ∼15% greater than loss of neutral genetic diversity. These results are counter to general expectations that selection should maintain MHC polymorphism, but do agree with the results of recent simulation models and at least two empirical studies. Notably, our results suggest that negative frequency‐dependent selection could be more important than overdominance for maintaining high MHC polymorphism in pre‐bottlenecked populations.

How does the 50/500 rule apply to MVPs?

The 50/500 rule has been used as a guiding principle in conservation for assessing minimum viable effective population size (N(e)). There is much confusion in the recent literature about how the 500 value should be applied to assess extinction risk and set priorities in conservation biology. Here, we argue that the confusion arises when the genetic basis for a short-term N(e) of 50 to avoid inbreeding depression is used to justify a long-term N(e) of 500 to maintain evolutionary potential. This confusion can result in misleading conclusions about how genetic arguments alone are sufficient to set minimum viable population (MVP) thresholds for assessing the extinction risk of threatened species, especially those that emphasize that MVPs should be in the thousands to maintain evolutionary potential.

THE FUNCTIONAL APPROACH TO BEHAVIOR: IS IT USEFUL?

Natural selection is an axiom for a functional approach to studying behavior. Research is thus canalized toward observing the function of behaviors in relation to an organisms reproduction and/or survival. Explanations resulting from this approach can be instructive only if all or most behaviors under study are the consequence of natural selection. This assumption has no empirical basis, however. Predictions derived from selection theory are supported generally, but these predictions are not unique to the selection process and are therefore ambiguous. Behaviors can be induced environmentally without a change in the genotype, and they can be learned and transmitted culturally as well as genetically; all three processes can relate to increased measures of fitness. Which of these processes has led to the establishment of a behavioral pattern is not easily discernible from simple observations. Behaviors are extremely plastic in their development, and thus studies that assume heritable variation should be viewed with caution. The relative significance of these factors is not known because of the artificial dichotomization of behavioral explanations into proximate and ultimate causation, the functional approach being the paradigm of the latter. Therefore, a functional approach limits our understanding of the origins, diversity, and persistence of behaviors. An epigenetic approach is proposed as being more useful because it yields a more comprehensive understanding of behavioral processes.

Founder Effects, Inbreeding, and Loss of Genetic Diversity in Four Avian Reintroduction Programs

The number of individuals translocated and released as part of a reintroduction is often small, as is the final established population, because the reintroduction site is typically small. Small founder and small resulting populations can result in population bottlenecks, which are associated with increased rates of inbreeding and loss of genetic diversity, both of which can affect the long-term viability of reintroduced populations. I used information derived from pedigrees of four monogamous bird species reintroduced onto two different islands (220 and 259 ha) in New Zealand to compare the pattern of inbreeding and loss of genetic diversity among the reintroduced populations. Although reintroduced populations founded with few individuals had higher levels of inbreeding, as predicted, other factors, including biased sex ratio and skewed breeding success, contributed to high levels of inbreeding and loss of genetic diversity. Of the 10-58 individuals released, 4-25 genetic founders contributed at least one living descendent and yielded approximately 3-11 founder-genome equivalents (number of genetic founders assuming an equal contribution of offspring and no random loss of alleles across generations) after seven breeding seasons. This range is much lower than the 20 founder-genome equivalents recommended for captive-bred populations. Although the level of inbreeding in one reintroduced population initially reached three times that of a closely related species, the long-term estimated rate of inbreeding of this one population was approximately one-third that of the other species due to differences in carrying capacities of the respective reintroduction sites. The increasing number of reintroductions to suitable areas that are smaller than those I examined here suggests that it might be useful to develop long-term strategies and guidelines for reintroduction programs, which would minimize inbreeding and maintain genetic diversity.

Incestuous mating in a communal bird: a family affair

In the past, observations of animal dispersal has been taken as evidence of inbreeding avoidance. Reduced dispersal by the young of communal breeders makes them ideal for investigating the possibility of inbreeding and/or inbreeding avoidance. Communally breeding pukeko are especially suitable for such a study because they exhibit extreme philopatry, have a polygynandrous mating system, and engage in readily observed copulations. Results from a 7-yr study show that most pukeko remain and breed in their natal territory and incestuous matings are common. In contrast, incidents of dispersal out of the natal territory were infrequent, involving only males. Outbreeding appeared less common than inbreeding. Dispersal by breeding males that had mated previously with their offspring could not be logically linked to incest avoidance, but movements of nonbreeding subadults might have been related to either incest avoidance or intersexual dominance. Except for young nonbreeding males that tend to be subordinate to breeding females, male pukeko dominate females. A few subadult males that were stopped from copulating by the aggressive behavior of their mothers subsequently dispersed, whereas others showed reduced sexual behavior in the presence of their mothers. Both incest avoidance by the mothers (but not the sons) and parental dominance could explain these observations. Parental dominance seems to be a viable explanation because there were no examples of daughters avoiding matings with their fathers or sisters avoiding matings with brothers. Results from other studies of communally breeding birds also show various degrees of incestuous mating. Data from one in-depth study on acorn woodpeckers, from which incest-avoidance mechanisms have been postulated, is considered in detail; the results appear equivocal and do not exclude alternative explanations. Additional factors, such as a level of fecundity markedly higher than that of survival and a long history of communal (and presumably incestuous) habits in pukeko, lead us to question whether inbreeding among pukeko is likely to have deleterious genetic effects. The possibility of nonrandom fusion of gametes would also support this view. Overall, pukeko appear to demonstrate higher levels of incestuous matings than current research and theories on the evolution of vertebrate mating systems would have predicted. We argue that this conflict arises as a product of the unquestioning assumption by many workers that behavior leading to inbreeding has been selected against or that inbreeding-avoidance mechanisms have been selected for in animal populations.

Shared Paternity among Non-Relatives is a Result of an Egalitarian Mating System in a Communally Breeding Bird, the Pukeko

With extra-pair paternity now known to be common among many species of birds, it is not surprising that males of most species exhibit behaviour that minimizes the risk of losing paternity. The most common form of paternity assurance is mate guarding whereby the male closely follows his mate during her fertile period and attempts to prevent other males from copulating with her. Even in communal or cooperative breeding species where two or more males collaborate in defending a breeding territory, mate guarding by the alpha male still occurs. Here we report that within communally breeding groups of pukeko (.Porphyrio porphyrio) dominant males do not guard their mates and rarely interrupt the copulations of unrelated rival males. This population of pukeko meets the conditions of a model that predicts that unrelated individuals who form breeding coalitions should interact in an egalitarian manner. DNA fingerprinting revealed a tendency for alpha males to father the majority of offspring in a brood, but frequent, uninterrupted copulations by subordinate birds assured that most males within the group had at least some paternity. Because the timing of ovulation is difficult to predict in female pukeko, individual males may be unable to estimate the proportion of eggs that they have fertilized, which could explain why most males participate more or less equally in parental care.

Successful island reintroductions of New Zealand robins and saddlebacks with small numbers of founders

Populations established with a small number of founders are thought to have a high risk of extinction due to Allee effects, demographic stochasticity, inbreeding and reduced genetic variation. We tested whether the initial number of birds released was related to persistence in reintroductions of saddlebacks (Philesturnus carunculatus) and robins (Petroica australis) to New Zealand offshore islands. Data were analysed for 31 populations that had been observed for at least 3 years since reintroductions. The numbers released ranged from 5–188. Most of the populations (26) survived and grew, including five from less than 15 founders, and four out of the five extinctions were attributable to introduced mammalian predators. The number of individuals released did not significantly affect extinction probability. The ability of these small releases to establish populations can be attributed to the closed nature of the islands (allowing birds to find mates), low mortality rates following release and high growth rates at low density. Stochastic simulation models based on data from two reintroduced populations suggested that populations with four founders (two male, two female) would have a negligible chance of extinction through demographic stochasticity and would be able to grow even if there were high rates of egg failure through inbreeding.

The distribution and current status of New Zealand Saddleback Philesturnus carunculatus

This paper reviews and updates the distribution and status of two geographically distinct subspecies of New Zealand Saddleback Philesturnus carunculatus , a New Zealand forest passerine that is highly susceptible to predation by introduced mammals such as stoats and rats. The recovery of the North Island and South Island saddleback populations has been rapid since translocations to offshore islands free of exotic predators began in 1964, when both subspecies were on the brink of extinction. South Island saddlebacks have gone from a remnant population of 36 birds on one island to over 1,200 birds spread among 15 island populations, with the present capacity to increase to a maximum of 2,500 birds. We recommend that South Island saddleback be listed under the IUCN category of Near Threatened, although vigilance on islands for invading predators and their subsequent rapid eradication is still required. North Island saddlebacks have gone from a remnant population of 500 birds on one island to over 6,000 on 12 islands with the capacity to increase to over 19,000 individuals. We recommend that this subspecies be downgraded to the IUCN category of Least Concern. The factors that limited the early recovery of saddlebacks are now of less significance with recent advances in predator eradication techniques allowing translocations to large islands that were formerly unsuitable. The only two predators that still cohabit some islands with saddleback are Pacific rats or kiore Rattus exulans and Weka Gallirallus australis , a flightless native rail. Although North Island saddlebacks coexist with kiore, South Island saddlebacks do less well in their presence, possibly because the relict population had no previous history with this species of rat. The impact of Weka as predators of saddlebacks is less clear, but population growth rates appear to be slowed in their presence. It is recommended that while current recovery strategies involving island habitat restoration and translocations be maintained, management effort should also be directed towards returning saddlebacks to selected, “mainland island” sites, where introduced pests are either excluded by predator-proof fences or controlled at very low levels by intensive pest management.

Heterozygosity-fitness correlations and their relevance to studies on inbreeding depression in threatened species

The majority of reported multilocus heterozygosity–fitness correlations (HFCs) are from large, outbred populations, and their relevance to studies on inbreeding depression in threatened populations is often stressed. The results of such HFC studies conducted on outbred populations may be of limited application to threatened population management, however, as bottlenecked populations exhibit increased incidence of inbreeding, increased linkage disequilibrium, reduced genetic diversity and possible effects of historical inbreeding such as purging. These differences may affect both our ability to detect inbreeding depression in threatened species, and our interpretation of the underlying mechanisms for observed heterozygosity–fitness relationships. The study of HFCs in outbred populations is of interest in itself, but the results may not translate directly to threatened populations that have undergone severe bottlenecks.