Laura Ross

Sex Determination: Why So Many Ways of Doing It?

Sex is universal amongst most eukaryotes, yet a remarkable diversity of sex determining mechanisms exists. We review our current understanding of how and why sex determination evolves in animals and plants.

Horizontal Gene Transfer from Diverse Bacteria to an Insect Genome Enables a Tripartite Nested Mealybug Symbiosis

The smallest reported bacterial genome belongs to Tremblaya princeps, a symbiont of Planococcus citri mealybugs (PCIT). Tremblaya PCIT not only has a 139 kb genome, but possesses its own bacterial endosymbiont, Moranella endobia. Genome and transcriptome sequencing, including genome sequencing from a Tremblaya lineage lacking intracellular bacteria, reveals that the extreme genomic degeneracy of Tremblaya PCIT likely resulted from acquiring Moranella as an endosymbiont. In addition, at least 22 expressed horizontally transferred genes from multiple diverse bacteria to the mealybug genome likely complement missing symbiont genes. However, none of these horizontally transferred genes are from Tremblaya, showing that genome reduction in this symbiont has not been enabled by gene transfer to the host nucleus. Our results thus indicate that the functioning of this three-way symbiosis is dependent on genes from at least six lineages of organisms and reveal a path to intimate endosymbiosis distinct from that followed by organelles.

Tree of Sex: A database of sexual systems

The vast majority of eukaryotic organisms reproduce sexually, yet the nature of the sexual system and the mechanism of sex determination often vary remarkably, even among closely related species. Some species of animals and plants change sex across their lifespan, some contain hermaphrodites as well as males and females, some determine sex with highly differentiated chromosomes, while others determine sex according to their environment. Testing evolutionary hypotheses regarding the causes and consequences of this diversity requires interspecific data placed in a phylogenetic context. Such comparative studies have been hampered by the lack of accessible data listing sexual systems and sex determination mechanisms across the eukaryotic tree of life. Here, we describe a database developed to facilitate access to sexual system and sex chromosome information, with data on sexual systems from 11,038 plant, 705 fish, 173 amphibian, 593 non-avian reptilian, 195 avian, 479 mammalian, and 11,556 invertebrate species.

Genomic conflict in scale insects: the causes and consequences of bizarre genetic systems.

It is now clear that mechanisms of sex determination are extraordinarily labile, with considerable variation across all taxonomic levels. This variation is often expressed through differences in the genetic system (XX‐XY, XX‐XO, haplodiploidy, and so on). Why there is so much variation in such a seemingly fundamental process has attracted much attention, with recent ideas concentrating on the possible role of genomic conflicts of interest. Here we consider the role of inter‐ and intra‐genomic conflicts in one large insect taxon: the scale insects. Scale insects exhibit a dizzying array of genetic systems, and their biology promotes conflicts of interest over transmission and sex ratio between male‐ and female‐expressed genes, parental‐ and offspring‐expressed genes (both examples of intra‐genomic conflict) and between scale insects and their endosymbionts (inter‐genomic conflict). We first review the wide range of genetic systems found in scale insects and the possible evolutionary transitions between them. We then outline the theoretical opportunities for genomic conflicts in this group and how these might influence sex determination and sex ratio. We then consider the evidence for these conflicts in the evolution of sex determination in scale insects. Importantly, the evolution of novel genetic systems in scale insects has itself helped create new conflicts of interest, for instance over sex ratio. As a result, a major obstacle to our understanding of the role of conflict in the evolution of sex‐determination and genetic systems will be the difficulty in identifying the direction of causal relationships. We conclude by outlining possible experimental and comparative approaches to test more effectively how important genomic conflicts have been.

The evolution of genomic imprinting: theories, predictions and empirical tests.

The epigenetic phenomenon of genomic imprinting has motivated the development of numerous theories for its evolutionary origins and genomic distribution. In this review, we examine the three theories that have best withstood theoretical and empirical scrutiny. These are: Haig and colleagues’ kinship theory; Day and Bonduriansky’s sexual antagonism theory; and Wolf and Hager’s maternal–offspring coadaptation theory. These theories have fundamentally different perspectives on the adaptive significance of imprinting. The kinship theory views imprinting as a mechanism to change gene dosage, with imprinting evolving because of the differential effect that gene dosage has on the fitness of matrilineal and patrilineal relatives. The sexual antagonism and maternal–offspring coadaptation theories view genomic imprinting as a mechanism to modify the resemblance of an individual to its two parents, with imprinting evolving to increase the probability of expressing the fitter of the two alleles at a locus. In an effort to stimulate further empirical work on the topic, we carefully detail the logic and assumptions of all three theories, clarify the specific predictions of each and suggest tests to discriminate between these alternative theories for why particular genes are imprinted.

Ecology, Not the Genetics of Sex Determination, Determines Who Helps in Eusocial Populations

In eusocial species, the sex ratio of helpers varies from female only, in taxa such as the social Hymenoptera (ants, bees, and wasps) [1], to an unbiased mixture of males and females, as in most termites [2]. Hamilton suggested that this difference owes to the haplodiploid genetics of the Hymenoptera leading to females being relatively more related to their siblings [3]. However, it has been argued that Hamiltons hypothesis does not work [4-9] and that the sex of helpers could instead be explained by variation in the ecological factors that favor eusociality [10]. Here we test these two competing hypotheses, which focus on the possible importance of different terms in Hamiltons rule [2, 11], with a comparative study across all sexual eusocial taxa. We find that the sex ratio of helpers (1) shows no significant correlation with whether species are haplodiploid or diploid and (2) shows a strong correlation with the ecological factor that had favored eusociality. Specifically, when the role of helpers is to defend the nest, both males and females help, whereas when the role of helpers is to provide brood care, then helpers are the sex or sexes that provided parental care ancestrally. More generally, our results confirm the ability of kin selection theory to explain the biology of eusocial species, independently of ploidy, and add support to the idea that haplodiploidy has been more important for shaping conflicts within eusocial societies than for explaining its origins [6, 12-19].

Large population size predicts the distribution of asexuality in scale insects.

Understanding why some organisms reproduce by sexual reproduction while others can reproduce asexually remains an important unsolved problem in evolutionary biology. Simple demography suggests that asexuals should outcompete sexually reproducing organisms, because of their higher intrinsic rate of increase. However, the majority of multicellular organisms have sexual reproduction. The widely accepted explanation for this apparent contradiction is that asexual lineages have a higher extinction rate. A number of models have indicated that population size might play a crucial role in the evolution of asexuality. The strength of processes that lead to extinction of asexual species is reduced when population sizes get very large, so that the long‐term advantage of sexual over asexual reproduction may become negligible. Here, we use a comparative approach using scale insects (Coccoidea, Hemiptera) to show that asexuality is indeed more common in species with larger population density and geographic distribution and we also show that asexual species tend to be more polyphagous. We discuss the implication of our findings for previously observed patterns of asexuality in agricultural pests.

Sexual conflict, sex allocation and the genetic system

Decisions over what sex ratio to produce can have far-reaching evolutionary consequences, for both offspring and parents. However, the extent to which males and females come into evolutionary conflict over aspects of sex allocation depends on the genetic system: when genes are passed to the next generation unequally by the two sexes (as in haplodiploidy, for example), this biased transmission can facilitate a range of conflicts not seen in diploids. However, much less attention has been paid to these forms of sexual conflict, not least because it has not always been clear how the conflicts could be realized. Here we consider how biased gene transmission, as expressed in different genetic systems, enhances the opportunity for sex ratio conflict and give empirical examples that confirm that males and females have the opportunity to influence sex ratios.

Sex Determination, Sex Chromosomes, and Karyotype Evolution in Insects

Insects harbor a tremendous diversity of sex determining mechanisms both within and between groups. For example, in some orders such as Hymenoptera, all members are haplodiploid, whereas Diptera contain species with homomorphic as well as male and female heterogametic sex chromosome systems or paternal genome elimination. We have established a large database on karyotypes and sex chromosomes in insects, containing information on over 13000 species covering 29 orders of insects. This database constitutes a unique starting point to report phylogenetic patterns on the distribution of sex determination mechanisms, sex chromosomes, and karyotypes among insects and allows us to test general theories on the evolutionary dynamics of karyotypes, sex chromosomes, and sex determination systems in a comparative framework. Phylogenetic analysis reveals that male heterogamety is the ancestral mode of sex determination in insects, and transitions to female heterogamety are extremely rare. Many insect orders harbor species with complex sex chromosomes, and gains and losses of the sex-limited chromosome are frequent in some groups. Haplodiploidy originated several times within insects, and parthenogenesis is rare but evolves frequently. Providing a single source to electronically access data previously distributed among more than 500 articles and books will not only accelerate analyses of the assembled data, but also provide a unique resource to guide research on which taxa are likely to be informative to address specific questions, for example, for genome sequencing projects or large-scale comparative studies.

Haplodiploidy, Sex-Ratio Adjustment, and Eusociality

Hamilton’s “haplodiploidy hypothesis” holds that inflated sororal relatedness has promoted altruistic sib rearing in haplodiploids, potentially explaining their apparent predisposition to eusociality. Here, we suggest that haplodiploidy may instead promote eusociality simply by facilitating sex-ratio adjustment. Specifically, haplodiploidy may enable sex-ratio bias toward the more helpful sex, owing to “local resource enhancement,” and such sex-ratio bias may promote the evolution of helping by individuals of that sex, owing to the “rarer-sex effect.” This could explain why haplodiploidy appears to have been important for eusociality in taxa with only female helpers, such as ants, wasps, and bees, but not in taxa with both male and female helpers, such as termites.