Immunoecology of species with alternative reproductive tactics and strategies

Alternative reproductive tactics and strategies (ARTS) refer to polymorphic reproductive behaviours in which in addition to the usual two sexes, there are one or more alternative morphs, usually male, that have evolved the ability to circumvent direct intra-sexual competition. Each morph has unique morphological, ecological, developmental, behavioural, life-history, and physiological profiles that shift the balance between reproduction and selfmaintenance, one aspect being immunity. Immunoecological work on species with ARTS, which is the topic of this review, is particularly interesting because the alternative morphs make it possible to separate the effects of sex, per se, from other factors that in other species are inextricably linked with sex. We first summarize the evolution, development and maintenance of ARTS. We then review the main immunoecological hypotheses relevant to species with ARTS, dividing them into physiological, life-history, and ecological hypotheses. In context of these hypotheses, we critically review in detail all immunoecological studies we could find on species with ARTS. Several interesting patterns emerge. Generally, greater understanding would occur if hypotheses and predictions were always explicitly articulated. Oddly, there is a paucity of studies on insects, despite the many benefits that arise from working with insects: larger sample sizes, simple immune systems, and countless forms of alternative reproductive tactics and strategies. Of all the hypotheses reviewed, the immunocompetence handicap hypothesis and its derivatives have generated the greatest amount of work, but not necessarily the greatest level of understanding. Integration has been a one-way street, with ecologists delving deeper into physiology, seemingly at the cost of ignoring their organisms’ evolutionary history and ecology. One possible useful framework is to divide ecological and evolutionary factors affecting immunity into those that stimulate the immune system, and those that depress it. Finally, the contributions of genomics to ecology are being increasingly recognized, including in species with ARTS, but we must ensure that evolutionary and ecological hypotheses drive the effort. There is no grandeur in the strict reductionist view of life.