Divergence in Reproductive Behaviors Is Associated with the Evolutionary Loss of Parental Care.

AbstractThe mechanisms underlying the divergence of reproductive strategies between closely related species are still poorly understood. Additionally, it is unclear which selective factors drive the evolution of reproductive behavioral variation and how these traits coevolve, particularly during early divergence. To address these questions, we quantified behavioral differences in a recently diverged pair of Nova Scotian three-spined stickleback (Gasterosteus aculeatus) populations, which vary in parental care, with one population displaying paternal care and the other lacking this. We compared both populations, and a full reciprocal F1 hybrid cross, across four major reproductive stages: territoriality, nesting, courtship, and parenting. We identified significant divergence in a suite of heritable behaviors. Importantly, F1 hybrids exhibited a mix of behavioral patterns, some of which suggest sex linkage. This system offers fresh insights into the coevolutionary dynamics of reproductive behaviors during early divergence and offers support for the hypothesis that coevolutionary feedback between sexual selection and parental care can drive rapid evolution of reproductive strategies.

Locomotor effects of a fibrosis-based immune response in stickleback fish.

The vertebrate immune system provides an impressively effective defense against parasites and pathogens. However, these benefits must be balanced against a range of costly side-effects including energy loss and risks of auto-immunity. These costs might include biomechanical impairment of movement, but little is known about the intersection between immunity and biomechanics. Here, we show that a fibrosis immune response to Schistocephalus solidus infection in freshwater threespine stickleback (Gasterosteus aculeatus) has collateral effects on their locomotion. Although fibrosis is effective at reducing infection, some populations of stickleback actively suppress this immune response, possibly because the costs of fibrosis outweigh the benefits. We quantified the locomotor effects of the fibrosis immune response in the absence of parasites to investigate whether there are incidental costs of fibrosis that could help explain why some fish forego this effective defense. To do this, we induced fibrosis in stickleback and then tested their C-start escape performance. Additionally, we measured the severity of fibrosis, body stiffness and body curvature during the escape response. We were able to estimate performance costs of fibrosis by including these variables as intermediates in a structural equation model. This model revealed that among control fish without fibrosis, there is a performance cost associated with increased body stiffness. However, fish with fibrosis did not experience this cost but rather displayed increased performance with higher fibrosis severity. This result demonstrates that the adaptive landscape of immune responses can be complex with the potential for wide-reaching and unexpected fitness consequences.

Locomotor effects of a fibrosis-based immune response in stickleback fish.

The vertebrate immune system provides an impressively effective defense against parasites and pathogens. However, these benefits must be balanced against a range of costly side-effects including energy loss and risks of auto-immunity. These costs might include biomechanical impairment of movement, but little is known about the intersection between immunity and biomechanics. Here, we show that a fibrosis immune response in threespine stickleback (Gasterosteus aculeatus) has collateral effects on their locomotion. When freshwater stickleback are infected with the tapeworm parasite Schistocephalus solidus, they face an array of fitness consequences ranging from impaired body condition and fertility to an increased risk of mortality. To fight the infection, some stickleback will initiate a fibrosis immune response in which they produce excess collagenous tissue in their coelom. Although fibrosis is effective at reducing infection, some populations of stickleback actively suppress this immune response, possibly because the costs of fibrosis outweigh the benefits. Here we quantify the locomotor effects of the fibrosis immune response in the absence of parasites to investigate whether there are collateral costs of fibrosis that could help explain why some fish forego this effective defense. To do this, we induce fibrosis in stickleback and then test their C-start escape performance. Additionally, we measure the severity of fibrosis, body stiffness, and body curvature during the escape response. We were able to estimate performance costs of fibrosis by including these variables as intermediates in a structural equation model. This model reveals that among control fish without fibrosis, there is a performance cost associated with increased body stiffness. However, fish with fibrosis did not experience this cost but rather displayed increased performance with higher fibrosis severity. This result demonstrates that the adaptive landscape of immune responses can be complex with the potential for wide reaching and unexpected fitness consequences.

Insights into Parental Care from Studies on Non-mammalian Vertebrates.

Parental care has attracted attention from both proximate and ultimate perspectives. While understanding the adaptive significance of care has been the focus of work in diverse organisms in behavioral ecology, most of what we know about the proximate mechanisms underlying parental care behavior comes from studies in mammals. Although studies on mammals have greatly improved our understanding of care, viewing parental care solely through a mammalian lens can limit our understanding. Here, we draw upon examples from non-mammalian vertebrate systems to show that in many ways mammals are the exception rather than the rule for caregiving: across vertebrates, maternal care is often not the ancestral or the most common mode of care and fathering is not derivative of mothering. Embracing the diversity of parental care can improve our understanding of both the proximate basis and adaptive significance of parental care and the affective processes involved in caregiving.

Population-level variation in parasite resistance due to differences in immune initiation and rate of response.

Closely related populations often differ in resistance to a given parasite, as measured by infection success or failure. Yet, the immunological mechanisms of these evolved differences are rarely specified. Does resistance evolve via changes to the host's ability to recognize that an infection exists, actuate an effective immune response, or attenuate that response? We tested whether each of these phases of the host response contributed to threespine sticklebacks' recently evolved resistance to their tapeworm Schistocephalus solidus. Although marine stickleback and some susceptible lake fish permit fast-growing tapeworms, other lake populations are resistant and suppress tapeworm growth via a fibrosis response. We subjected lab-raised fish from three populations (susceptible marine "ancestors," a susceptible lake population, and a resistant lake population) to a novel immune challenge using an injection of (1) a saline control, (2) alum, a generalized pro-inflammatory adjuvant that causes fibrosis, (3) a tapeworm protein extract, or (4) a combination of alum and tapeworm protein. With enough time, all three populations generated a robust fibrosis response to the alum treatments. Yet, only the resistant population exhibited a fibrosis response to the tapeworm protein alone. Thus, these populations differed in their ability to respond to the tapeworm protein but shared an intact fibrosis pathway. The resistant population also initiated fibrosis faster in response to alum, and was able to attenuate fibrosis, unlike the susceptible populations' slow but longer lasting response to alum. As fibrosis has pathological side effects that reduce fecundity, the faster recovery by the resistant population may reflect an adaptation to mitigate the costs of immunity. Broadly, our results confirm that parasite detection and immune initiation, activation speed, and immune attenuation simultaneously contribute to the evolution of parasite resistance and adaptations to infection in natural populations.

Microhabitat contributes to microgeographic divergence in threespine stickleback.

Since the New Synthesis, most migration-selection balance theory has predicted that there should be negligible differentiation over small spatial scales (relative to dispersal), because gene flow should erode any effect of divergent selection. Nevertheless, there are classic examples of microgeographic divergence, which theory suggests can arise under specific conditions: exceptionally strong selection, phenotypic plasticity in philopatric individuals, or nonrandom dispersal. Here, we present evidence of microgeographic morphological variation within lake and stream populations of threespine stickleback (Gasterosteus aculeatus). It seems reasonable to assume that a given lake or stream population of fish is well-mixed. However, we found this assumption to be untenable. We examined trap-to-trap variation in 34 morphological traits measured on stickleback from 16 lakes and 16 streams. Most traits varied appreciably among traps within populations. Both between-trap distance and microhabitat characteristics such as depth and substrate explained some of the within-population morphological variance. Microhabitat was also associated with genotype at particular loci but there was no genetic isolation by distance, implying that heritable habitat preferences may contribute to microgeographic variation. Our study adds to growing evidence that microgeographic divergence can occur across small spatial scales within individuals' daily dispersal neighborhood where gene flow is expected to be strong.

Investigating the association between armour coverage and parasite infection in an estuarine population of stickleback.

Background: When threespine stickleback colonized fresh water, they repeatedly evolved reduced armour plating via changes in Eda allele frequency. This evolution is typically attributed to differential predation pressure between marine and freshwater environments. However, the chromosomal region containing Eda is associated with many other phenotypes, including schooling, antipredator behaviour, and immunity. Consequently, the evolution of armour plating may be driven by multiple selective pressures acting on Eda or linked genes. Question: Is parasite infection associated with armour phenotype? Hypothesis: Parasite load differs between stickleback armour plate morphs. Organisms: An armour-polymorphic population of threespine stickleback (Gasterosteus aculeatus), and their parasites. Field site: In June 2009 and 2012, we sampled stickleback from a single human-made salt-marsh pool in the Campbell River Estuary on Vancouver Island. Methods: We counted macroparasites on approximately 100 fish per year and counted lateral armour plates. We used generalized linear models to test for correlations between armour morph and parasite load. Results: Most parasite species were not associated with armour. The gill parasite Thersitina was more abundant on more fully armoured fish in both years. The nematode Eustrongylides also exhibited a marginally significant positive trend. If parasitic infections reduce stickleback fitness, this positive covariance between armour and infection would accelerate the loss of armour plating in stickleback colonizing fresh water.