Immunoecology of Species with Alternative Reproductive Tactics and Strategies

Abstract

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 its own morphological, ecological, developmental, behavioural, life-history, and physiological profile that shifts the balance between reproduction and self-maintenance, 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 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. 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 strategies and tactics. Of all the hypotheses considered, the immunocompetence handicap hypothesis has generated the greatest amount of work, but not necessarily the greatest level of understanding. Unfortunately, it is often used as a general guiding principle rather than a source of explicitly articulated predictions. Other hypotheses are usually considered a posteriori, but perhaps they should take centre stage. Whereas blanket concepts such as “immunocompetence” and “androgens” might be useful to develop a rationale, predictions need to be far more explicitly articulated. Integration so far has been a one-way street, with ecologists delving deeper into physiology, sometimes 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 and sometimes applied to species with ARTS, but we must ensure that evolutionary and ecological hypotheses drive the effort, as there is no grandeur in the strict reductionist view of life.