The danger within: the role of genetic, behavioural and ecological factors in population persistence of colour polymorphic species

Polymorphic species have been the focus of important work in evolutionary biology. It has been suggested that colour polymorphic species have specific evolutionary and population dynamics that enable them to persist through environmental changes better than less variable species. We suggest that recent empirical and theoretical work indicates that polymorphic species may be more vulnerable to extinction than previously thought. This vulnerability arises because these species often have a number of correlated sexual, behavioural, life history and ecological traits, which can have a simple genetic underpinning. When exacerbated by environmental change, these alternate strategies can lead to conflict between morphs at the genomic and population levels, which can directly or indirectly affect population and evolutionary dynamics. In this perspective, we identify a number of ways in which the nature of the correlated traits, their underpinning genetic architecture, and the inevitable interactions between colour morphs can result in a reduction in population fitness. The principles illustrated here apply to all kinds of discrete polymorphism (e.g. behavioural syndromes), but we focus primarily on colour polymorphism because they are well studied. We urge further empirical investigation of the genetic architecture and interactions in polymorphic species to elucidate the impact on population fitness

Sperm storage in a family-living lizard, the Tree Skink (Egernia striolata)

This work was supported by the Australian Research Council (ARC DP130102998 grant to MJW and RWB), Natural Sciences and Engineering Research Council of Canada (scholarship to JLR), the Australasian Society for the Study of Animal Behavior, the Australian Museum, and Macquarie University (scholarship to JLR).The ability to produce viable offspring without recently mating, either through sperm storage or parthenogenesis, can provide fitness advantages under a suite of challenging ecological scenarios. Using genetic analysis, we demonstrate that three wild-caught female Tree Skinks (Egernia striolata) reproduced in captivity with no access to males for over a year, and that this is best explained by sperm storage. To the best of our knowledge, this is the first time female sperm storage has been documented in any monogamous family-living reptile, including social Australian egerniine skinks (from the subfamily Egerniinae). Furthermore, by using paternal reconstruction of genotypes we show that captive-born offspring produced by the same females in the preceding year, presumably without sperm storage, were sired by different males. We qualitatively compared aspects of these females' mates and offspring between years. The parents of each litter were unrelated, but paternal and offspring genotypes from litters resulting from stored sperm were more heterozygous than those inferred to be from recent matings. Family-living egerniine skinks generally have low rates of multiple paternity, yet our study suggests that female sperm storage, potentially from outside social partners, offers the real possibility of benefits. Possible benefits include increasing genetic compatibility of mates and avoiding inbreeding depression via cryptic female choice. Sperm storage in Tree Skinks, a family-living lizard with a monogamous mating system, suggests that females may bet-hedge through extra-pair copulation with more heterozygous males, reinforcing the idea that females could have more control on reproductive outcomes than previously thought.PostprintPeer reviewe

The colour of paternity: extra-pair paternity in the wild Gouldian finch does not appear to be driven by genetic incompatibility between morphs.

In socially monogamous species, individuals can use extra-pair paternity and offspring sex allocation as adaptive strategies to ameliorate costs of genetic incompatibility with their partner. Previous studies on domesticated Gouldian finches (Erythrura gouldiae) demonstrated a genetic incompatibility between head colour morphs, the effects of which are more severe in female offspring. Domesticated females use differential sex allocation, and extra-pair paternity with males of compatible head colour, to reduce fitness costs associated with incompatibility in mixed-morph pairings. However, laboratory studies are an oversimplification of the complex ecological factors experienced in the wild, and may only reflect the biology of a domesticated species. This study aimed to examine the patterns of parentage and sex-ratio bias with respect to colour pairing combinations in a wild population of the Gouldian finch. We utilized a novel PCR assay that allowed us to genotype the morph of offspring before the morph phenotype develops, and to explore bias in morph paternity and selection at the nest. Contrary to previous findings in the laboratory, we found no effect of pairing combinations on patterns of extra-pair paternity, offspring sex ratio, or selection on morphs in nestlings. In the wild, the effect of morph incompatibility is likely much smaller, or absent, than was observed in the domesticated birds. Furthermore, the previously studied domesticated population is genetically differentiated from the wild population, consistent with the effects of domestication. It is possible that the domestication process fostered the emergence (or enhancement) of incompatibility between colour morphs previously demonstrated in the laboratory. This article is protected by copyright. All rights reserved

Variation in Reproductive Success Across Captive Populations: Methodological Differences, Potential Biases and Opportunities

Our understanding of fundamental organismal biology has been disproportionately influenced by studies of a relatively small number of model\u27 species extensively studied in captivity. Laboratory populations of model species are commonly subject to a number of forms of past and current selection that may affect experimental outcomes. Here, we examine these processes and their outcomes in one of the most widely used vertebrate species in the laboratory - the zebra finch (Taeniopygia guttata). This important model species is used for research across a broad range of fields, partly due to the ease with which it can be bred in captivity. However despite this perceived amenability, we demonstrate extensive variation in the success with which different laboratories and studies bred their subjects, and overall only 64% of all females that were given the opportunity, bred successfully in the laboratory. We identify and review several environmental, husbandry, life-history and behavioural factors that potentially contribute to this variation. The variation in reproductive success across individuals could lead to biases in experimental outcomes and drive some of the heterogeneity in research outcomes across studies. The zebra finch remains an excellent captive animal system and our aim is to sharpen the insight that future studies of this species can provide, both to our understanding of this species and also with respect to the reproduction of captive animals more widely. We hope to improve systematic reporting methods and that further investigation of the issues we raise will lead both to advances in our fundamental understanding of avian reproduction as well as to improvements in future welfare and experimental efficiency

Reply : colour polymorphism is likely to be disadvantageous to some populations and species due to genetic architecture and morph interactions

Polymorphism describes two or more distinct, genetically determined, phenotypes that co-occur in the same population, where the rarest morph is maintained at a frequency above the mutation rate (Ford 1945; Huxley 1955). In a recent opinion piece, we explored a new idea regarding the role of genetic architectures and morph interactions in colour polymorphisms and how this can negatively affect population performance (Bolton et al. 2015). In this issue of Molecular Ecology, Forsman (2016) thoroughly discusses the current evidence for polymorphisms enhancing population performance and critiques the validity of the definitions of polymorphism we use in our original paper. We respond by clarifying that the negative consequences of polymorphisms that we discussed are likely to be most pertinent in species that have a particular set of characteristics, such as strong sexual or social interactions between morphs and discrete genetic architectures. Although it was not our intention to redefine polymorphism, we do believe that there should be further discussion about refining or characterizing balanced polymorphisms with respect to the degree of morph sympatry, discreteness of traits and their underlying genetic architecture, and the types of selection that drive and maintain the variation. The latter describes whether polymorphism is primarily maintained by external factors such as predation pressure or internal factors such as interactions with members of the same species. The contribution of Forsman (2016) is useful to this discussion, and we hope that our exchange of opinions will inspire new empirical and theoretical ideas on the origin and maintenance of colour polymorphisms.6 page(s

Socioecology of the Australian Tree Skink (Egernia striolata)

Financial support for this research was provided by The Australian Research Council (ARC DP130102998 grant to MJW and RWB), the Australian Government (Endeavour Fellowship to JLR), the Australian Museum, the Australasian Society for the Study of Animal Behaviour, the Natural Science and Engineering Council of Canada (scholarship to JLR), and Macquarie University (research funding and scholarship to JLR).There is great diversity in social behavior across the animal kingdom. Understanding the factors responsible for this diversity can help inform theory about how sociality evolves and is maintained. The Australian Tree Skink (Egernia striolata) exhibits inter- and intra-population variability in sociality and is therefore a good system for informing models of social evolution. Here, we conducted a multi-year study of a Tree Skink population to describe intra-population variation in the social organization and mating system of this species. Skinks aggregated in small groups of 2–5 individuals, and these aggregations were typically associated with shared shelter sites (crevices and hollows within rocks and trees). Aggregations were typically made up of one or more adult females and, often, one male and/or juvenile(s). Social network and spatial overlap analyses showed that social associations were strongly biased toward kin. Tree skinks also exhibited high site fidelity regardless of age or sex. There were high levels of genetic monogamy observed with most females (87%) and males (68%) only breeding with a single partner. Our results indicate that Tree Skinks reside in small family groups and are monogamous, which corresponds with existing research across populations. Similar to previous work, our study area consisted of discrete habitat patches (i.e., rock outcrops, trees, or both), which likely limits offspring dispersal and promotes social tolerance between parents and their offspring. Our study clearly demonstrates that there is intra-population variability in Tree Skink social behavior, but it also provides evidence that there is a high degree of inter-population consistency in sociality across their geographic range. We also highlight promising possible avenues for future research, specifically discussing the importance of studying the nature and extent of Tree Skink parental care and quantifying the fitness outcomes of kin-based sociality in this species, which are topics that will further our understanding of the mechanisms underlying variation in vertebrate social behavior.Publisher PDFPeer reviewe

2009 Genotypes

Genotypes for individuals caught in 2009 for CERVUS analysis. In CERVUS format. Age classes & sexes in the Readme

Data from: The colour of paternity: extra-pair paternity in the wild Gouldian finch does not appear to be driven by genetic incompatibility between morphs

In socially monogamous species, individuals can use extra-pair paternity and offspring sex allocation as adaptive strategies to ameliorate costs of genetic incompatibility with their partner. Previous studies on domesticated Gouldian finches (Erythrura gouldiae) demonstrated a genetic incompatibility between head colour morphs, the effects of which are more severe in female offspring. Domesticated females use differential sex allocation, and extra-pair paternity with males of compatible head colour, to reduce fitness costs associated with incompatibility in mixed-morph pairings. However, laboratory studies are an oversimplification of the complex ecological factors experienced in the wild, and may only reflect the biology of a domesticated species. This study aimed to examine the patterns of parentage and sex-ratio bias with respect to colour pairing combinations in a wild population of the Gouldian finch. We utilized a novel PCR assay that allowed us to genotype the morph of offspring before the morph phenotype develops, and to explore bias in morph paternity and selection at the nest. Contrary to previous findings in the laboratory, we found no effect of pairing combinations on patterns of extra-pair paternity, offspring sex ratio, or selection on morphs in nestlings. In the wild, the effect of morph incompatibility is likely much smaller, or absent, than was observed in the domesticated birds. Furthermore, the previously studied domesticated population is genetically differentiated from the wild population, consistent with the effects of domestication. It is possible that the domestication process fostered the emergence (or enhancement) of incompatibility between colour morphs previously demonstrated in the laboratory

Nest data for Spatial EPP analysis

All breeding observations in nestboxes and hollows (without genetic samples) at Wyndham in 2008-2009, including anonymised co-ordinates for nest locations, where inter nest differences are preserved but do not reflect the real position on the globe. README file also includes the code used to calculate the number of synchronous nests and how far away they are

2008 Genotypes

Genotypes for individuals used in CERVUS analysis caught in 2008. Readme includes the age and sex of individuals used